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Volume 20 No. 3 — Summer 2016
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Summer 2016
Volume 20 No. 3
A peer-reviewed journal of medical science,
social science in medicine, and medical humanities
Original Research & Contributions
4 Weight Loss and the Prevention of Weight
Regain: Evaluation of a Treatment Model
of Exercise Self-Regulation Generalizing
to Controlled Eating
18 A Pharmacist-Staffed, Virtual Gout
Management Clinic for Achieving Target Serum
Uric Acid Levels: A Randomized Clinical Trial
THE PERMANENTE JOURNAL
Follow @PermanenteJ
24 Exploring the Reality of Using Patient
Experience Data to Provide Resident
Feedback: A Qualitative Study of Attending
Physician Perspectives
31 Physicians Experiencing Intense Emotions
While Seeing Their Patients: What Happens?
38 Difference in Effectiveness of Medication
Adherence Intervention by Health Literacy
Level
45 Lifestyle and Self-Management by Those Who
Live It: Patients Engaging Patients in a Chronic
Disease Model
Special Reports
51 Improving Care in Older Patients with
Diabetes: A Focus on Glycemic Control
57 Evidence-Based Workflows for Thyroid and
Parathyroid Surgery
74 The Truth about Truth-Telling in American
Medicine: A Brief History
Review Articles
78 Hyperparathyroidism of Renal Disease
84 Recurrence of Epithelioid Hemangioendothelioma during Pregnancy: Case Report and
Systematic Review
Narrative Medicine
102 The Use of Narrative as a Treatment Approach
for Obesity: A Storied Educational Program
Description
107 You Are Not Alone: Ten Strategies for
Surviving a Malpractice Lawsuit
Printed on acid-free paper.
ISSN 1552-5767
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Summer 2016/ Volume 20 No. 3
PermanenteJournal
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Mission: The Permanente Journal advances
knowledge in scientific research, clinical
medicine, and innovative health care delivery.
Circulation: 25,000 print readers per
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ON THE COVER:
Roman Stonemason
by Tom Janisse, MD, MBA
A Roman stonemason
works to repair the vulnerable corner of a 1000-yearold structure. He stands
sturdy in his fashionably
buckled black boots, blue
jeans with plaster-clouded
knees, and traditional
blue work coat with lapels.
Kneepads wait to support
his delicate work close to the ground, hammering
additional bits of marble, variously sized, to fit all filling
defects. He restores a historic work of masonry 30
generations after its construction and reconstruction,
done just like this in just this way, in a process first
learned during the transition from wood to stone.
Some hours into mixing mud, his dextrous hands with
precision and artistry carefully prep the faces for a final
fresh surface coat, smooth to the touch. When he is
done, the pads, hammer, slab, and bits all fit into his
metal pail, then into his bicycle basket for a ride home
through Roman traffic. He looks back to view with
pleasure and a sure sense of contribution his master
work of art.
Dr Janisse is the Editor-in-Chief of The Permanente
Journal and Publisher of The Permanente Press.
112
CME EVALUATION FORM
The Permanente Journal
500 NE Multnomah St, Suite 100
Portland, Oregon 97232
www.thepermanentejournal.org
ISSN 1552-5767
Follow @PermanenteJ
ORIGINAL RESEARCH
& CONTRIBUTIONS
4 Weight Loss and the Prevention of
Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation
Generalizing to Controlled Eating.
James J Annesi, PhD, FAAHB, FTOS,
FAPA; Ping H Johnson, PhD;
Gisèle A Tennant, PhD; Kandice J Porter,
PhD; Kristin L McEwen
For decades behavioral weight-loss treatments have been unsuccessful beyond
the short term. In this study, women with
obesity were randomized into either a
comparison treatment that incorporated
a print manual plus telephone follow-ups
(n = 55) or into an experimental treatment
of The Coach Approach exercise-support
protocol followed after 2 months by group
nutrition sessions focused on generalizing
self-regulatory skills from an exercise
support to a controlled eating context
(n = 55). Improvements in all psychological
measures, physical activity, and fruit and
vegetable intake were significantly greater
in the experimental group. Change in
self-regulation best predicted weight loss,
whereas change in self-efficacy best predicted maintenance of lost weight.
18 A Pharmacist-Staffed, Virtual Gout
Management Clinic for Achieving
Target Serum Uric Acid Levels:
A Randomized Clinical Trial.
Robert Goldfien, MD; Alice Pressman,
PhD, MS; Alice Jacobson, MS; Michele Ng,
PharmD; Andrew Avins, MD, MPH
The authors conducted a parallel-group,
randomized, 26-week, controlled trial of a
pharmacist-staffed, telephone-based program for managing hyperuricemia vs usual
care. Among 37 participants randomized
to the intervention group, 13 (35%) had a
serum uric acid level (sUA) ≤ 6.0 mg/dL at
26 weeks vs 5 of 40 participants (13%) in
the control group (p = 0.03). A structured
pharmacist-staffed program was more effective than usual care for achieving target
sUA levels. These results suggest that
a structured program could significantly
improve gout management.
24 Exploring the Reality of Using Patient
Experience Data to Provide Resident
Feedback: A Qualitative Study of
Attending Physician Perspectives.
Steffanie Campbell, MD; Heather
Honoré Goltz, PhD, LMSW, MEd; Sarah
Njue, MPH; Bich Ngoc Dang, MD
From 7/2013 to 8/2013, in-depth, faceto-face, semistructured interviews were
conducted with 9 attending physicians
who precept residents in internal medicine
at 2 continuity clinics (75% of eligible attendings). Content analysis identified 6
potential barriers in using patient experience survey data: 1) perceived inability
of residents to learn or to incorporate
feedback, 2) punitive nature of feedback,
3) lack of training in the delivery of action-
able feedback, 4) lack of timeliness in the
delivery of feedback, 5) unclear benefit of
patient experience survey data as a tool for
providing resident feedback, and 6) lack of
individualized feedback.
31 Physicians Experiencing Intense
Emotions While Seeing Their Patients:
What Happens? Joana Vilela da Silva,
MD; Irene Carvalho, PhD
A self-report survey was completed by 127
physicians, with 52 (43%) reporting experiencing intense emotions frequently. Coping
strategies to deal with the emotion at the
moment included behavioral and cognitive
approaches. Choking-up/crying, touching, smiling, and providing support were
significantly associated with an immediate
positive impact on the physician-patient
relationship. Withdrawing from the situation, imposing, and defending oneself were
associated with a negative impact.
38 Difference in Effectiveness of
Medication Adherence Intervention
by Health Literacy Level. Ashli A
Owen-Smith, PhD, SM; David H Smith,
PhD, RPh; Cynthia S Rand, PhD; Jeffrey
O Tom, MD, MS; Reesa Laws; Amy
Waterbury, MPH; Andrew Williams,
PhD; William M Vollmer, PhD
Promoting Adherence to Improve Effectiveness of Cardiovascular Disease Therapies
(PATIENT) was a randomized clinical trial
designed to test the impact, compared
with usual care, of two technology-based
interventions that leveraged interactive
voice recognition to promote medication
adherence. The differences in intervention
effects for high vs low health literacy in this
exploratory analysis are consistent with
the hypothesis that individuals with lower
health literacy may derive greater benefit
from this type of intervention compared
with individuals with higher health literacy.
Your Guy’s Guide to Gynecology:
A Reference for Men and Women
Bruce Bekkar, MD; Uda Wahn, MD
ISBN-10: 0965506746
ISBN-13: 978-0965506748
East Sandwich, MA: North Star Publications
(Ant Hill Press); 2000.
Hardcover: 325 pages
$24.95
Picking up the Pieces:
What Everyone Needs to
Know When a Child Dies
Adrienne L Burnell, RN, MS, PhD;
George M Burnell, MD
ISBN-10: 1516859405
ISBN-13: 978-1516859405
createspace.com; 2015
Paperback: 206 pages
$26.45
If you are a Permanente author and would like your book cited here,
send an e-mail to [email protected].
45 Lifestyle and Self-Management by Those
Who Live It: Patients Engaging Patients
in a Chronic Disease Model. Michelle T
Jesse, PhD; Elizabeth Rubinstein; Anne
Eshelman, PhD, ABPP; Corinne Wee;
Mrunalini Tankasala; Jia Li, PhD; Marwan
Abouljoud, MD, CPE, MMM, FACS
Of 1862 patient satisfaction surveys, 823
were returned (44.2%). Patients and their
supports appreciated that the program
volunteer was a transplant recipient and
noted gratitude for the lifestyle information.
Five areas were associated with the success of Transplant Living Community: 1)
a “champion”; 2) a receptive health care
environment; 3) a high level of visibility
to physicians and staff; 4) a lifestyle plan
(“Play Your ACES” [Attitude, Compliance,
Support, and Exercise]), and 5) a strong
volunteer structure. It is feasible to integrate a sustainable patient-led lifestyle and
self-management educational group into
a busy tertiary care clinic for patients with
complex chronic illnesses.
The Permanente Journal/Perm J 2016 Summer:20(3)
For information and/or rates for placing an
announcement here, please contact [email protected].
CME credits are available
online at www.tpjcme.org.
The mail-in CME form can
be found on page 112.
Special Report
51 Improving Care in Older Patients with
Diabetes: A Focus on Glycemic Control.
Eric A Lee, MD; Nancy E Gibbs, MD;
John Martin, MD; Fred Ziel, MD;
Jennifer K Polzin, PharmD; Darryl
Palmer-Toy, MD, PhD
Diabetes affects more than 25% of
Americans older than age 65 years.
This article discusses the seminal
research findings that strongly suggest
that hemoglobin A1c goals should be
relaxed in older patients. The authors
then recommend an age-specific and
functionally appropriate hemoglobin A1c
reference range for patients receiving
medications to improve glycemic control.
Other interventions are suggested that
should make diabetes care safer in
older patients receiving hypoglycemic
medications.
Special Report
57 Evidence-Based Workflows for Thyroid
and Parathyroid Surgery.
Charles Meltzer, MD; Amer Budayr, MD;
Annette Chavez, MD; Richard Dlott,
MD; William Greif, MD; Deepak Gurushanthaiah, MD; Andrew Klonecke, MD;
Matthew Lando, MD; Joyce Leary, MD;
Sundeep Nayak, MD; Ryan Niederkohr,
MD; Judith Park, MD; Alison Savitz,
MBA, MD; Henry Schwartz, MD
A need exists to reduce care variations by
standardizing the practice of thyroid and
parathyroid surgery. During the course of
a year, a task force developed algorithms
representing decision points and workflows
based on American Thyroid Association
guidelines and on three internal studies
of surgical practices in the Northern and
Southern California Regions of Kaiser
Permanente conducted in collaboration
with Health Information Technology
Transformation & Analytics (HITTA).
Special Report
74 The Truth about Truth-Telling in
American Medicine: A Brief History.
Bryan Sisk, MD; Richard Frankel, PhD;
Eric Kodish, MD; J Harry Isaacson, MD
Transparency has become an ethical
cornerstone of American medicine. For
most of American history, the intentional
withholding of information was the
accepted norm in medical practice. The
authors trace the ethics and associated
practices of truth-telling during the past two
centuries and outline the many pressures
that influenced physician behavior during
that time period. They conclude that the
history of disclosure is not yet finished,
as physicians still struggle to find the best
way to share difficult information without
causing undue harm to their patients.

REVIEW ARTICLES
78 Hyperparathyroidism of Renal Disease.
Noah K Yuen, MD; Shubha Ananthakrishnan,
MD; Michael J Campbell, MD
Patients with renal hyperparathyroidism
(rHPT) experience increased rates of cardiovascular problems and bone disease. Guidelines recommend that screening and management be initiated for all patients with chronic
kidney disease stage III (estimated glomerular
filtration rate, < 60 mL/min/1.73 m2). Improving medical management with vitamin D
analogs, phosphate binders, and calcimimetic
drugs has expanded the treatment options
for patients with rHPT, but some patients still
require a parathyroidectomy to mitigate the
sequelae of this challenging disease.
84 Recurrence of Epithelioid Hemangioendothelioma during Pregnancy: Case
Report and Systematic Review. Michael
McCulloch, LAc, MPH, PhD; Michael
Russin, MD; Arian Nachat, MD
The authors present a case of a 28-year-old
woman whose epithelioid hemangioendothelioma (EHE) recurred during pregnancy,
suggesting hormonal involvement. They
conducted a systematic review to provide
analysis and interpretation of the potential
significance of her disease recurring, with
fatal outcome, during pregnancy. Very little
research has explored the use of individual
hormonal markers. Strongly positive expression of 17-beta estradiol receptors have
been reported. Expression of placenta growth
factor (PlGF) is noteworthy in our case, in that
our patient’s disease quickly and dramatically
flared in the 25th week of pregnancy, near the
peak in maternal PlGF production.
COMMENTARY
90 Quality Over Quantity: Integrating
Mental Health Assessment Tools into
Primary Care Practice.
Darrell L Hudson, PhD, MPH
Depression is one of the most common,
costly, and debilitating psychiatric disorders
in the US. Yet, mental health services are
underutilized throughout the US. Recent
policy changes have encouraged depression
screening in primary care settings. However,
there is not much guidance about how depression screeners are administered. There
are people suffering from depression who
are not getting the treatment they need. It is
important to consider whether enough care
is being taken when administering depression screeners in primary care settings.
93 Plant-Based Diets: A Physician’s Guide.
Julieanna Hever, MS, RD, CPT
This article provides physicians and other
health care practitioners with an overview of
the myriad benefits of a plant-based diet as
well as details on how best to achieve a wellbalanced, nutrient-dense meal plan. It also
defines notable nutrient sources, describes
how to get started, and offers suggestions
on how health care practitioners can encourage their patients to achieve goals, adhere
to the plan, and experience success.
NARRATIVE MEDICINE
102 The Use of Narrative as a Treatment
Approach for Obesity: A Storied
Educational Program Description.
Marcus Griffith, MD; Jeana Griffith, PhD;
Mellanese Cobb, MPH; Vladimir Oge, MPH
The authors wrote an interventional children’s book and workbook (The Tale of
Two Athletes: The Story of Jumper and The
Thumper) and developed a three-step intervention based on the narrative. The intervention’s purpose is to increase public awareness, reduce stigma, and help members of
underserved communities become more
comfortable discussing obesity. Interactive
storytelling is the first step. The second step
is reading. Practicing positive behaviors
and decision making through games and
exercises from the companion workbook is
the final step.
107 You Are Not Alone: Ten Strategies
for Surviving a Malpractice Lawsuit.
Audrey Sheridan, MD
I wasn’t even scheduled to work that morning.
I had just gone into the office for a meeting.
Most physicians, about 60%, will be sued
at some point in their careers. Physicians
typically do feel intense strain when faced
with a lawsuit. We are more likely to suffer
depression and burnout. Ten techniques
are offered for coping that really work: resist
isolation, use your strengths, retrain your
brain, take care of yourself, give yourself a
break, set priorities, approach law as a foreign
culture, regain perspective, use distraction,
and focus on what you can control.
109 The Handshake Layer Cake: Meeting
and Regreeting Difficulties for a
Non-French Surgeon in France.
Colin G Murphy, MCh, FRCSI
As always, the first work-greeting of the
day, be it a handshake or les bises, is
complicated by context: age, seniority, work
status, employer/employee status, family,
familiarity, the other people present at that
interaction, whether it is break/coffee time.
All of this has to be balanced against the
unthinkable, not greeting someone at all, or
thinking (like an idiot) that the wave or nod
from a distance that you gave earlier in the
day constituted a greeting.
111Disconnection.
Ahmed Obeidat, MD, PhD
It was a very familiar object that I asked her
to identify. She started to look, feel, think,
and she said, “It has buttons, numbers, and
glass, but I can’t put them together. I am
unsure!” The last task I asked her to perform
was to write a sentence, which thrilled me
when she wrote in beautiful script, “Doctor,
I want to know what is wrong with me.”
This was alexia (word blindness) without
agraphia. She was a creative writer in her
third decade.
Contents continued on next page.
1
ONLINE
More content is available at: www.thepermanentejournal.org.
Refining Reporting Mechanisms in Oregon’s
Patient-Centered Primary Care Home
Program to Improve Performance.
Sherril Gelmon, DrPH; Billie Sandberg, PhD;
Nicole Merrithew, MPH; Rebekah Bally, MPH
To achieve the Triple Aim, the Oregon Health
Authority implemented the Patient-Centered
Primary Care Home (PCPCH) Program in
2009. To assist in evaluating 500 primary care
practices’ achievement along its 6 core attributes
the research team developed an innovative
scoring method. Initial results demonstrate that
the scores enable stakeholders to compare
results across similar practices and across
the model’s core attributes, and to identify
opportunities for improvement and technical
assistance. This strategy could be replicated
in other states. The article offers insights on
implementation strategies, efficacy of the PCPCH
model, and lessons learned.
Metastatic Renal Cell Carcinoma Presenting
as Painful Chewing Successfully Treated with
Combined Nivolumab and Sunitinib.
Fade Mahmoud, MD, FACP; Al-Ola Abdallah,
MD; Konstantinos Arnaoutakis, MD; Issam
Makhoul, MD
Metastatic renal cell carcinoma to the head and
neck is the third-most common cause of distant
metastasis to the head and neck, after breast
cancer and lung cancer. A 71-year-old man with
a single complaint of a one-year history of pain
while chewing food, but without painless hematuria, weight loss, anorexia, fatigue, or anemia. An
almost complete response of the metastatic disease occurred with the combination of nivolumab
and sunitinib.
Treatment of Tracheoinnominate Fistula
with Ligation of the Innominate Artery:
A Case Report.
Rhiana S Menen, MD; Jimmy J Pak, MD;
Matthew A Dowell, PA; Ashish R Patel, MD;
Simon K Ashiku, MD; Jeffrey B Velotta, MD
A 76-year-old man who underwent emergent
tracheostomy placement presented on
postoperative day 10 with massive hemorrhage
concerning for tracheoinnominate fistula and
was treated with median sternotomy and ligation
of the innominate artery. The key to good
outcomes is quick diagnosis and urgent surgical
intervention.
Monoarticular Poncet Disease after
Pulmonary Tuberculosis: A Rare Case Report
and Review of Literature. Paritosh Garg, MD;
Nikhil Gupta, MD, MBBS; Mohit Arora, MS
The authors describe an atypical presentation of
active pulmonary tuberculosis with monoarticular
Poncet disease of the right knee in a 24-yearold woman. The diagnosis of Poncet disease is
mainly clinical with exclusion of other causes. It
generally presents as an acute or subacute form;
however, chronic forms have been described in
the literature.
Image Diagnosis: Pott Puffy Tumor.
Diane Apostolakos, MD, MS; Ian Tang, MD
A 20-year-old man was admitted to our hospital
with complaints of frontal headache, sinusitis,
and fever for one week. Sir Percivall Pott (17141788), a surgeon at St. Bartholomew’s Hospital
in London, first described it as Pott Puffy tumor,
referring to one of the four historic manifestations
of inflammation noted by Aulus Cornelius Celsus
(c 25 BC-c 50 AD): rubor (redness), tumor
(swelling), calor (warmth), and dolor (pain).
Image Diagnosis: Tubo-ovarian Abscess
with Hydrosalpinx. Kiersten L Carter, MD;
Gus M Garmel, MD, FACEP, FAAEM
Risk factors of tubo-ovarian Abscess include
younger age, multiple sexual partners, nonuse
of barrier contraception, and a history of pelvic
inflammatory disease. Compared with ultrasonography, computed tomography has increased
sensitivity to detect thick-walled, rim-enhancing
adnexal masses. The aim of therapeutic management is to be as noninvasive as possible.
However, if this approach fails to yield clinical
improvement within 3 days, reassessment of the
antibiotic regimen, with consideration for laparoscopy, laparotomy, adnexectomy, hysterectomy, or
image-guided abscess drainage is necessary.
Image Diagnosis: Gastric Migration of
Hookworms in a Patient with Anemia.
Chalapathi Rao Achanta, MD
A 65-year-old man presented to our hospital with
4 months of fatigue and weakness. He denied
any bleeding manifestations and had pallor
on examination. The patients’ esophagus was
normal, but there were motile hookworms in the
gastric antrum and heavy loads of hookworms in
the duodenum.
Image Diagnosis: Encephalopathy Resulting
from Dural Arteriovenous Fistula.
Ana Filipa Santos, MD; Célia Machado, MD;
Sara Varanda, MD; João Pinho, MD;
Manuel Ribeiro, MD; Jaime Rocha, MD;
Ricardo Maré, MD
A 69-year-old woman presented to the Neurology Department with 2 months of progressive
psychomotor slowing, inability to concentrate,
and periods of disorientation. Her past medical
history was unremarkable, and she was taking no
medication. There was no history of trauma. The
initiating events that led to the development of
these symptoms are not clear, but the literature
reports association with trauma, infection, recent
surgery, and dural sinus thrombosis.
Future Challenges of Robotics and Artificial
Intelligence in Nursing: What Can We Learn
from Monsters in Popular Culture?
Henrik Erikson, RNT, PhD; Martin SalzmannErikson, RN, MHN, PhD
The authors propose that monsters in popular
culture might be studied with the hope of learning
about situations and relationships that generate
empathic capacities in their monstrous existences. The aim of the article is to introduce the
theoretical framework and assumptions behind
this idea. Both robots and monsters are posthuman creations. The knowledge we present here
gives ideas about how nursing science can address the postmodern, technologic, and global
world to come.
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Copyright © 2016 The Permanente Journal
2

PermanenteJournal
The
EDITOR-IN-CHIEF: Tom Janisse, MD, MBA
ASSOCIATE EDITOR-IN-CHIEF: Lee Jacobs, MD
SENIOR EDITORS
Vincent Felitti, MD Preventive Medicine, Book Reviews
Gus M Garmel, MD, FACEP, FAAEM Clinical Medicine
Arthur Klatsky, MD Original Articles
Eric Macy, MD Research
Scott Rasgon, MD Corridor Consult
ASSOCIATE EDITORS
Mikel Aickin, PhD
Biostatistics
James J Annesi, PhD, FAAHB, FTOS, FAPA
Health Behavior Research
Ricky Chen, MD
Medicine in Society
Gary W Chien, MD
Surgery
Carrie Davino-Ramaya, MD
National Practice Guidelines
Charles Elder, MD
Integrative Medicine
Philip I Haigh, MD, MSc, FRCSC, FACS
Surgery
Lisa Herrinton, PhD
Health Systems Research
Robert Hogan, MD
Family Medicine, Health Information Technology
Ashok Krishnaswami, MD, MAS
Cardiology
David Riley, MD
Case Reports
Ruth Shaber, MD
Women’s Health
John Stull, MD, MPH
Spirit of Medicine Dialogues
Gretchen Summer, PhD, RN
Nursing Research and Practice
KM Tan, MD
Continuing Medical Education
Calvin Weisberger, MD
Cognitive Clinical Medicine
Winston F Wong, MD, MS
Community Benefit, Disparities
Improvement and Quality Initiatives
Scott S Young, MD
Care Management Institute and Quality
EDITORIAL & PUBLISHING OFFICE
Merry Parker: Managing Editor & Publisher
Lynette Leisure: Creative Director
Amy Eakin: Business & Publishing Operations Manager
Max McMillen, ELS: Senior Editor & Staff Writer
Christopher Dauterman, MBA: Web Developer & Analyst
Ian Kimmich, ELS: Copy Editor & Publishing Coordinator
The Permanente Press
EDITORIAL BOARD
Maher A Abbas, MD, FACS, FASCRS
Chief, Digestive Disease Institute,
Cleveland Clinic, Abu Dhabi, UAE;
Professor of Surgery, Cleveland
Clinic Lerner College of Medicine
of Case Western Reserve University,
Cleveland, Ohio
Richard Abrohams, MD
Internal Medicine and Geriatrics,
The Southeast Permanente Medical
Group, Atlanta, Georgia
Fábio Ferreira Amorim, MD, PhD
Professor of Medicine, Escola
Superior de Ciências da Saúde in
the Department of Research and
Scientific Communication, Brasilia,
Brazil
Ellen Cosgrove, MD
Vice Dean, Academic Affairs and
Education, University of Nevada, Las
Vegas School of Medicine, Las Vegas,
Nevada
Quentin Eichbaum, MD, PhD, MPH,
MFA, MMCH, FCAP
Assistant Dean for Program Development; Associate Director of Transfusion Medicine; Associate Professor
of Pathology; Associate Professor of
Medical Education and Administration; Director, Fellowship Program
in Transfusion Medicine; Member,
Vanderbilt Institute for Global
Health; Vanderbilt University School
of Medicine, Nashville, Tennessee
Stanley W Ashley, MD
Chief Medical Officer, Brigham and
Women’s Hospital; Frank Sawyer
Professor of Surgery, Harvard Medical
School; Attending Surgeon, Gastrointestinal Cancer Center, Dana Farber
Cancer Institute; Chief, General
Surgery, Harvard Vanguard Medical
Associates, Boston, Massachusetts
Linda Fahey, RN, NP, MSN
Regional Manager, Quality and
Patient Safety, Patient Care Services,
Kaiser Permanente, Southern
California, Pasadena
Thomas Bodenheimer, MD
Professor, Dept of Family and
Community Medicine, University
of California, San Francisco
Carol Havens, MD
Family Practice and Addiction
Medicine, Director of Clinical
Education, The Permanente Medical
Group, Oakland, California
Brian Budenholzer, MD
Associate Clinical Professor in the
Department of Family Medicine at
the Brody School of Medicine at
East Carolina University, Greenville,
North Carolina
Alexander M Carson, RN, PhD
Associate Dean of Research and
Enterprise at the Institute of Health,
Medical Sciences and Society at
Glyndwr University in Wrexham,
Wales, United Kingdom
Rita Charon, MD, PhD
Professor of Medicine, Founder and
Executive Director of the Program
in Narrative Medicine at Columbia
University Medical Center, New York,
New York
Dan Cherkin, PhD
Senior Research Investigator, Group
Health Cooperative, and Affiliate
Professor, Dept of Family Medicine
and School of Public Health—Health
Services, University of Washington,
Seattle
Marilyn Chow, RN, DNSc, FAAN
Vice President, Patient Care Services,
Kaiser Foundation Health Plan;
Associate Clinical Professor, Dept of
Community Health Systems, School
of Nursing, University of California,
San Francisco
Robert R Cima, MD, FACS, FASCRS
Associate Professor of Surgery,
Division of Colon and Rectal Surgery;
Vice Chairman, Department of
Surgery, Mayo Clinic, Rochester,
Minnesota
Richard Frankel, PhD
Professor of Medicine and Psychiatry,
University of Indiana School of
Medicine, Indianapolis
James T Hardee, MD
Internal Medicine, Colorado
Permanente Medical Group;
Associate Clinical Professor of
Medicine, University of Colorado
School of Medicine, Westminster
Arthur Hayward, MD
Internal Medicine and Geriatrics,
CMI Clinical Lead for Elder Care;
Assistant Clinical Professor, Division
of General Medicine, Dept of
Internal Medicine, Oregon Health
Sciences University, Portland
Catherine Hickie, MBBS
Director of Clinical Training,
Bloomfield Hospital, Greater Western
Area Health Service; Conjoint Senior
Lecturer in Psychiatry, University of
New South Wales, Australia
Thomas E Kottke, MD
Medical Director for Population
Health, HealthPartners; Consulting
Cardiologist, HealthPartners Medical
Group; Senior Clinical Investigator,
HealthPartners Institute for
Education and Research; Professor of
Medicine, University of Minnesota,
Minneapolis
Tieraona Low Dog, MD
Director, Integrative Medicine
Concepts, Pecos, New Mexico;
President, My Own Health; Director,
Scientific and Regulatory Affairs,
Healthy Lifestyle Brands; Tempe,
Arizona
Lewis Mehl-Madrona, MD, PhD, MPhil
Director of Geriatric Education, Maine
Dartmouth Family Medicine Residency;
Director of Education and Training,
Coyote Institute, Augusta, Maine
Michel M Murr, MD, FACS
Professor of Surgery, Director of
Bariatric Surgery, University of South
Florida Health Science Center,
Tampa, Florida
Sylvestre Quevedo, MD
Department of Medicine and Global
Health Sciences, University of
California, San Francisco
Ilan Rubinfeld, MD, MBA, FACS, FCCP
Director, Surgical Intensive Care;
Associate Program Director,
General Surgery Residency; Henry
Ford Hospital, Detroit, Michigan;
Assistant Professor of Surgery, Wayne
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Detroit, Michigan
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Ambassador for Creative Projects
and Global Affairs, and Senior
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Petaluma, California
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Associate Professor, Dept of
Anesthesia, Co-Director, Biomedical
Ethics & Medical Humanities
Scholarly Concentration, Stanford
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Specialist Leader, Electronic
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Swee Yaw Tan, MBchB (Edin),
MRCP (UK), ACSM, FAMS
Senior Consultant Cardiologist,
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3
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain:
Evaluation of a Treatment Model of Exercise
Self-Regulation Generalizing to Controlled Eating
James J Annesi, PhD, FAAHB, FTOS, FAPA; Ping H Johnson, PhD;
Gisèle A Tennant, PhD; Kandice J Porter, PhD; Kristin L McEwen
Perm J 2016 Summer;20(3):15-146
E-pub: 02/01/2016http://dx.doi.org/10.7812/TPP/15-146
ABSTRACT
Context: For decades, behavioral weight-loss treatments have been unsuccessful beyond
the short term. Development and testing of innovative, theoretically based methods that
depart from current failed practices is a priority for behavioral medicine.
Objective: To evaluate a new, theory-based protocol in which exercise support methods
are employed to facilitate improvements in psychosocial predictors of controlled eating
and sustained weight loss.
Methods: Women with obesity were randomized into either a comparison treatment
that incorporated a print manual plus telephone follow-ups (n = 55) or an experimental
treatment of The Coach Approach exercise-support protocol followed after 2 months by
group nutrition sessions focused on generalizing self-regulatory skills from an exercise
support to a controlled eating context (n = 55). Repeated-measures analysis of variance
contrasted group changes in weight, physical activity, fruit and vegetable intake, mood, and
exercise- and eating-related self-regulation and self-efficacy over 24 months. Regression
analyses determined salient interrelations of change scores over both the weight-loss phase
(baseline-month 6) and weight-loss maintenance phase (month 6-month 24).
Results: Improvements in all psychological measures, physical activity, and fruit and
vegetable intake were significantly greater in the experimental group where a mean weight
loss of 5.7 kg (6.1% of initial body weight) occurred at month 6, and was largely maintained at a loss of 5.1 kg (5.4%) through the full 24 months of the study. After establishing
temporal intervals for changes in self-regulation, self-efficacy, and mood that best predicted
improvements in physical activity and eating, a consolidated multiple mediation model
suggested that change in self-regulation best predicted weight loss, whereas change in
self-efficacy best predicted maintenance of lost weight.
Conclusions: Because for most participants loss of weight remained greater than that
required for health benefits, and costs for treatment administration were comparatively low,
the experimental protocol was considered successful. After sufficient replication, physician
referral and applications within health promotion and wellness settings should be considered.
INTRODUCTION
Approximately 69% of US adults are at
a weight high enough to be considered unhealthy (body mass index [BMI], calculated
as weight in kilograms divided by height in
meters squared, ≥ 25 kg/m2).1 Approximately 36% of US women are obese (BMI ≥ 30
kg/m2).1 As degree of overweight increases,
so do health risks such as diabetes mellitus,
hypertension, heart disease, and certain
cancers.2 Although improving one’s dietary
behaviors (eg, increasing intake of fruits
and vegetables; reducing the consumption
of fats and sweets) and increasing physical
activity will reliably reduce weight by at
least the 5% required to obtain clinically
important health benefits,3 maintenance
of those behaviors has been very difficult
for almost all individuals.4,5 It can reliably
be predicted that weight lost over the first
approximately 6 months will mostly (if
not all) be regained within 1 to 3 years.4,5
Even a more modest weight loss of at least
3% of original body weight sustained for 2
years, sometimes considered to be a marker
of both weight-loss maintenance and some
health-risk reductions,6 has been difficult
to attain.7 Repeating the pattern of weight
loss and regain may have adverse effects on
both health risks and subsequent attempts
at weight loss.8,9
Previous Behavioral Treatments
Interventions based on educating individuals on the need to lose weight by eating more healthfully and by being more
physically active are the most common but
have been ineffective.4 Their absence of
foundation in established behavior-change
theories and research is a proposed reason
for this lack of success.10 Cognitive-behavioral methods consistent with Bandura’s
social cognitive11 and self-efficacy12 theories (eg, goal setting, cognitive restructuring) have occasionally had more favorable
effects13,14 and are presently considered to be
state-of-the-art by many researchers. Several
reviews, however, suggest that even those
types of interventions simply defer weight regain.4,5,15 Summaries of research also suggest
that longer treatments (eg, 6 to 12 months,
or longer) have had somewhat better effects
than shorter treatments; but initial weight
loss, energy-intake requirements, financial
incentives, and focusing on fat vs kilocalories
(kcal) do not affect the rate of weight regain
after approximately 6 months.5 Research has
rarely sought to determine the psychosocial
factors that predict weight-loss outcomes.16
James J Annesi, PhD, FAAHB, FTOS, FAPA, is the Director of Wellness Advancement, YMCA of Metropolitan Atlanta,
and Professor in the Department of Health Promotion and Physical Education at Kennesaw State University in GA.
E-mail: [email protected]. Ping H Johnson, PhD, is a Professor in the Department of Health Promotion and
Physical Education at Kennesaw State University in GA. E-mail: [email protected]. Gisèle A Tennant, PhD, is
the President of Tennant Solutions in Calgary, Alberta, Canada. E-mail: [email protected]. Kandice J Porter, PhD, is
an Associate Professor in the Department of Health Promotion and Physical Education at Kennesaw State University
in GA. E-mail: [email protected]. Kristin L McEwen, is the Empower Healthy Living Lead at the YMCA of
Metropolitan Atlanta in GA. E-mail: [email protected].
4
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
A group of behavioral researchers from
Oxford University recently incorporated
the extant theory and research to develop
a highly structured Cognitive Behavioural
Therapy protocol (Oxford CBT) in which
maintenance of lost weight was targeted
from the start.17 Their intervention model
is instructive because it embodies much
of the current thinking on both obtaining and sustaining weight loss through
evidence-based behavioral methods such
as self-monitoring the time, location, kcal,
and type of foods and drinks consumed;18
regular self-weighing;19 and actively countering lifestyle barriers.20 Components of
the Oxford CBT, which were administered
by mostly clinical psychologists during individual 50-minute consultations, included
“the role of body image in weight loss,”
“addressing barriers to weight loss,” “encouraging acceptance,” “common primary
goals,” and “developing long-term weight
maintenance skills.”17 Tracking of foods, initially limiting to a 1500 kcal intake per day,
and weighing and graphing weight changes
were key elements of the modular protocol.
The 24 sessions over 44 weeks designated
the initial 24 to 30 weeks as a weight-loss
phase, with the remainder devoted to
weight maintenance. More in common
with the available treatments, though, was
that exercise was not emphasized. The treatment developers suggested that its minor
impact on kcal totals render physical activity
as being of minor concern for weight loss,
and could possibly interfere with dietary
compliance. Thus, initiating physical activity could be deferred by up to 6 months.17
Although the Oxford CBT was expensive
at an estimated professional cost of between
US$3000 and US$4500 per participant,
it proved to be no more effective than
standard behavioral treatment.21 With its
sample of 49 women with obesity (ie, BMI
of 30-40 kg/m2) who were tested, approximately 68% of lost weight was regained at
the 2-year point, and 91% was regained
3 years past treatment initiation. Possibly
because even this strongly evidence-based
and well-administered approach was judged
by its developers to be ineffective at sustaining weight loss, they stated that it might
be “ethically questionable to claim that
psychological [behavioral] treatments for
obesity ‘work’ in the absence of [favorable]
data on their longer-term outcome.”21p712 In
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
further consideration of their findings and
the entire body of research on intervention
outcomes, they pessimistically, yet possibly realistically, concluded their report by
questioning whether continuing behavioral
research in the area of weight management
is even warranted any longer.21
Suggested Treatment Improvements
Other researchers disagreed with the above
conclusions, but it was acknowledged that
many of the presently held assumptions
and methods around behavioral weight-loss
treatments are ineffective and “fresh ideas
are needed for attacking the problem.”5p14
Following from this suggestion, the National Institutes of Health commissioned
a multidisciplinary working group on “Innovative Research to Improve Maintenance
of Weight Loss” in 2014.22 Its final report
summarized that 1) although adherence
issues need to be addressed first, exercise
has promising implications for maintaining
weight loss that go well beyond its obvious
expenditure of energy; and 2) learning behavioral skills before starting on weight loss might
be beneficial for weight-loss maintenance.22
In an unrelated review of treatment results,
Mann and her colleagues4 also recommended
further research on exercise as possibly being
the “potent factor” (for long-term weight
loss), in lieu of any additional work on dieting or composition of the diet.
Although a program of regular exercise
has been shown to be the strongest predictor
of success with maintaining weight loss for
some time,23-25 it remains difficult to maintain with an expected dropout rate of 50%
to 65% within 3 to 6 months of its initiation.26,27 On the basis of accelerometer data
from both the 2003-2004 and 2005-2006
National Health and Nutritional Examination Surveys, less than 4% of US women
complete the equivalent of at least 5 moderate-intensity walks per week,28,29 which is
considered to be the minimum threshold
for health benefits.30 Pilot research indicates
that even when dropout from exercise is successfully countered, typical frequencies for
formerly sedentary participants with obesity
are only 2 to 3 sessions per week, with an
estimated energy expenditure of less than
150 kcal per session (which amounts to only
approximately 0.5 kg of weight loss every 9
to 10 weeks31). Although there have been
advances in improving adherence to exercise
through standardized cognitive-behavioral
methods (eg, The Coach Approach protocol32), it was proposed that the relationship of exercise with maintained weight
loss is more because of its association with
improvements in psychological predictors
of controlled eating than associated energy
expenditures.33 For example, if self-regulatory
skills (eg, thought-stopping) could first be internalized within an intervention component
designed to facilitate regular exercise, possibly
treatment elements could be constructed to
promote generalization of such behavioral
skills to controlled eating.33 This, however,
runs in opposition to treatments such as the
Oxford CBT17 and some basic research34
that suggests that self-regulation used for
one behavior (here exercise) might deplete an
individual’s limited capacity of self-regulation
for success with a second behavior (here reduced kcal eating). It was also proposed that
self-efficacy, or one’s feelings of ability and
mastery, could be increased by demonstrating to one’s self a better control of exercise
behaviors through the use of newly learned
self-regulatory skills to counter barriers.33
Improved self-efficacy to control exercise
might, in turn, also generalize to controlled
eating, the other critical weight-loss behavior of interest.33,35 Improvements in mood,
a well-established by-product of initiating
even manageable amounts of exercise,33,36
might serve to counter the common problem
(especially for women) of emotional eating,37
and “… lead to a healthier psychological
climate in which individuals have more
cognitive and emotional resources, as well as
motivation and energy, to sustain a long-term
commitment to a weight-loss program.”35p320
Adherence to just 2 to 3 sessions per week
of behaviorally supported exercise has been
associated with significant improvements
in self-regulation, self-efficacy, and mood,38
which were found to be the most critical
psychological predictors of improvements in
eating and weight over 6 months, even when
previously suggested factors such as selfconcept and body image35 were considered.39
Additional studies are, however, required to
determine psychological predictors of longerterm weight-loss maintenance that might
inform both theory and the architecture of
improved behavioral treatments. Although
exercise is frequently incorporated into
weight-loss interventions, we have found no
longer-term research where its primary focus
5
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
was on improving psychological predictors of
controlled healthy eating.
Thus, as an extension to earlier research
on short-term psychological, behavioral,
and weight-loss effects,33,40-42 the present
study was conducted. It incorporated 1) an
experimental treatment that initiated supported exercise 2 months before any changes
in nutrition in attempts to improve targeted
psychological and behavioral correlates of
improved eating and weight loss, and 2) a
comparison treatment of participants’ use
of a manual that simultaneously encouraged
healthy eating, physical activity, and reasonable expectations, which was supplemented
by telephone follow-ups. Both treatments
were based on accepted behavioral theory,
yet there were substantial differences. On
the basis of a research consensus indicating
that the initial approximately 6 months after treatment start is a time of weight loss,
whereas beyond 6 months weight regain
(often complete regain) can be reliably
predicted,4,5 the present study investigated
1) treatment-associated weight change, 2)
behavioral predictors of weight change (ie,
changes in healthy eating and physical activity), and 3) hypothesized psychological
predictors of the behavioral changes (ie,
self-regulation, self-efficacy, mood) during
those 2 time frames. Data were measured
at baseline and months 3, 6, 12, and 24.
This allowed contrasts of dynamic changes
in targeted variables by group, and analyses
of which of the possible temporal intervals
best predicted weight change and weight
change-related behavioral improvements.
Such findings could be instrumental for
determining when, and to what degree, corresponding treatment processes should be
emphasized. To enhance clarity, this report
is expressed in 3 parts corresponding to the
aforementioned 3 areas. Hypotheses and
research questions are as follows.
Hypotheses
1.Reduction in weight from baseline-month
6 (weight-loss phase) will be greater, and
regain in weight from month 6-month
24 (weight-loss maintenance phase) will
be less, in the experimental group when
contrasted with the comparison group.
2.Improvements in the targeted behaviors
of physical activity and fruit and vegetable intake will be greater during both the
weight-loss and weight-loss maintenance
6
phases in the experimental group when
contrasted with the comparison group.
3.Improvements in the targeted psychological variables of mood, self-regulation, and
self-efficacy—related to both exercise and
eating—will be greater during both the
weight-loss and weight-loss maintenance
phases in the experimental group when
contrasted with the comparison group.
Research Questions
1.Was change in physical activity and
fruit and vegetable intake from baselinemonth 3, baseline-month 6, or month
3-month 6 the better predictor of weight
change during the weight-loss phase?
What temporal interval of change in
physical activity and fruit and vegetable
intake best predicted weight change during the weight-loss maintenance phase?
2.Was change in each psychological variable from baseline-month 3, baselinemonth 6, or month 3-month 6 the
better predictor of physical activity and
fruit and vegetable intake change during
the weight-loss phase? What temporal
interval of change in each psychological variable best-predicted behavioral
changes during the weight-loss maintenance phase?
3.Did changes in mood and/or aggregated
(exercise- and eating-related) measures
of self-regulation and self-efficacy
significantly mediate relationships between treatment type (comparison and
experimental) and changes in weight
during the weight-loss and weight-loss
maintenance phases?
Because participant characteristics,
initial weight, cognitive-behavioral treatment orientation, and focus on weight-loss
maintenance were designed to be similar to
those of the previously published Oxford
CBT study,21 the present weight-change
data were also contrasted with the Oxford
CBT findings.
METHODS
Participants
Participant recruitment was through
local print and electronic media. Inclusion criteria were 1) women of at least 21
years of age, 2) BMI ≥ 30 and < 40 kg/
m2, and 3) a self-reported goal of weight
loss. Exclusion criteria based on selfreport were 1) present or soon-planned
Abbreviations Keys
FV = Fruit and vegetable intake
Mood = Overall negative mood
PA = Physical activity
SE-eating = Self-efficacy for controlling
eating
SE-exercise = Self-efficacy for exercise
SR-eating = Self-regulation for
controlled eating
SR-exercise = Self-regulation for exercise
pregnancy; 2) present use of medications
for weight loss or a psychological/psychiatric condition; 3) current participation
in a medical, commercial, or self-help
weight-loss program; and 4) participation in a program of regular physical
activity/exercise that averaged at least 20
minutes per week during the year before
the start of the study. Treatments were
administered at small, community-based
wellness/fitness centers in the Eastern US.
Because the chance of cross-contamination of participants through intergroup
interactions within the same facility
would have been high, randomization to
either the comparison (COM) treatment
(n = 55) or the experimental (EXP) treatment (n = 55) was by site (3 sites each).
Institutional review board approval and
written informed consent from each participant were received. The research was
conducted in accordance with requirements of the Helsinki Declaration.
Independent t- and χ2 tests indicated no
significant group difference in age (mean± standard deviation (SD) = 48.2 ±
overall
7.8 years), BMI (35.3 ± 3.2 kg/m 2), or
racial/ethnic make-up (overall 83% white,
11% African American, and 6% of other
racial/ethnic groups). On the basis of selfreported family income, most participants
were middle class (overall 11% below
$24,999, 21% = $25,000-$49,999, 41% =
$50,000-$99,999, and 27% = $100,000 or
greater). Attrition from initial study acceptance to actual treatment participation was
minimal at 7% and also did not significantly
differ by group. This attrition was associated
with either a reported illness, a newly arisen
orthopedic issue, transportation issues, or
an inability of study staff to make further
contact after 3 attempts. There was no cost
or financial compensation for participation.
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
Measures
The self-report measures used in this
study were 1) physical activity (PA)
through weekly energy expenditure,
2) healthy eating through daily fruit and
vegetable intake (FV), 3) self-regulation
for exercise (SR-exercise), 4) self-regulation
for controlled eating (SR-eating), 5) selfefficacy for exercise (SE-exercise), 6) overall
negative mood (Mood), and 7) self-efficacy
for controlling eating (SE-eating). Descriptions of each of these measures, along with
data on their reliability and validity, are
presented below (Table 1). Body weight
was measured in kilograms through the
use of a recently calibrated scale (800KL;
Healthometer, Buffalo Grove, IL).
Procedure
Participants initially received a group
orientation to their assigned EXP or COM
protocol. Wellness counselors administering
treatments were trained in only one of the
protocols and masked to the treatment differences and the study’s research goals. Both
the EXP and COM treatments were based
on the social cognitive11 and self-efficacy12
theories of behavior where individuals are
viewed as 1) directing their own actions
through self-organization, 2) being able to
manage their environments, and 3) possessing capabilities to be self-reflective of their
internal abilities. Both the EXP and COM
curricula incorporated cognitive-behavioral
methods designed to empower participants
with self-regulatory skills and abilities to
deal with barriers to managing their weight
effectively, while increasing their feelings of
mastery and competence (ie, self-efficacy).
Both treatment protocols informed participants of the recommended volume of weekly
exercise to gain health benefits,30 but also
suggested that any amount was also likely to
be beneficial. However, the administration
formats and the proposed role of physical
Table 1. Description of study measures
Measure
Physical activity
(PA)
Measurement
instrument
Godin-Shephard
Leisure-Time
Physical Activity
Questionnaire43
Healthy eating
measured by fruit
and vegetable
intake (FV)
Self-report survey
of FV48
Self-regulation for
exercise (SRexercise) and
self-regulation for
controlled eating
(SR-eating)
Self-efficacy
for exercise
(SE-exercise)
Adaptation of
a previously
validated scale56,57
Overall negative
mood (Mood)
Profile of Mood
States Short
Form scale
of Total Mood
Disturbance60
Weight Efficacy
Lifestyle Scale61
Self-efficacy for
controlling eating
(SE-eating)
Exercise SelfEfficacy Scale58
Instrument description
Requires entry of number of weekly sessions of strenuous (~ 9 METs; eg,
running), moderate (~ 5 METs; eg, fast walking), and light (~ 3 METs; eg, easy
walking) physical exertion for “more than 15 minutes.” Incorporates METs, or
the energy costs associated with specific physical activity intensities (1 MET
approximates the use of 3.5 ml of O2/kg/minute).44
Foods and beverages consumed “in a typical day over the past week” are
based on examples and serving sizes of fruits (eg, apple, banana, peach [1
small or 118 mL or 4 ounces canned]; raisins, dates [0.59 mL or 2 ounces];
100% fruit juice [118 mL or 4 ounces]) and vegetables (eg, broccoli, carrots,
tomatoes, green beans [118 mL or 4 ounces]; raw spinach [236 mL or 8
ounces]) that correspond to both the US Department of Agriculture’s current
MyPlate and former Food Guide Pyramid.49 Increases in FV were strongly
associated with both weight loss and weight-loss maintenance,50 and an
increase in FV was a stronger predictor of weight loss than reduction in fat
intake.51 Previous research indicates that FV alone is a strong predictor of
overall energy consumption and healthfulness of the diet.52,53
The 10 items for SR-exercise (eg, “I say positive things to myself about being
physically active”) and SR-eating (eg, “I make formal agreements with myself
regarding my eating”) assess the degree that barriers to those behaviors are
addressed through the use of self-regulatory skills. Responses range from 1
(never) to 5 (often), and are summed. A higher score indicates a greater use of
self-regulation.
After beginning with the stem, “I am confident I can participate in regular
exercise when ...,” each of the scale’s 5 items end with a possible barrier to
overcome (eg, “I am tired,” “I have more enjoyable things to do”). Responses
range from 1 (not at all confident) to 7 (very confident), and are summed. A
higher score indicates greater self-efficacy.
The 30 items (5 items per factor) assess feelings during the past week on
depression (eg, “sad”), tension/anxiety (eg, “tense”), vigor (eg, “energetic”),
fatigue (eg, “weary”), anger (eg, “angry”), and confusion (eg, “forgetful”).
Responses range from 0 (not at all) to 4 (extremely) and are summed after
reversing the scores of the vigor factor. A lower score indicates better mood.
The 20 items (4 per factor) assess feelings of ability to control eating when
the following situations are present: negative emotions (eg, “I can resist eating
when I am anxious [nervous]”), food availability (eg, “I can resist eating even
when I am at a party”), physical discomfort (eg, “I can resist eating when I am
uncomfortable”), positive activities (eg, “I can resist eating when I am watching
TV”), and social pressure (eg, “I can resist eating even when I have to say ‘no’
to others”). Responses range from 0 (not confident) to 9 (very confident), and
are summed. A higher score indicates greater self-efficacy.
Reliability and validity
Test-retest reliability (2 weeks) was
0.74.45 Construct validity was indicated
through strong correlations with both
accelerometer and peak volume of
oxygen uptake measurements.46,47
Test-retest reliability (3 weeks) was
0.77-0.83 for women.33 Validated
against comprehensive food frequency
questionnaires,54 in which pilot research
indicated strong correlations (r-values =
0.70-0.85) with the full-length Block Food
Frequency Questionnaire.54,55
Cronbach α-values for internal
consistency were 0.75,56 0.83, and 0.80
for the present versions and sample,
respectively. Test-retest reliability (2
weeks) was 0.77.56
Cronbach α-values for internal
consistency were 0.76-0.82. Test-retest
reliability (2 weeks) was 0.90.59 Cronbach
α-value for internal consistency for the
present sample was 0.80.
Cronbach α-values for internal
consistency were 0.84-0.95 across
factors,60 and 0.79-0.89 for the present
sample. Test-retest reliability (3 weeks)
averaged 0.69.60
Cronbach α-values for internal
consistency were 0.70-0.90 across its
factors,61 and 0.74-0.81 for the present
sample.
MET = metabolic equivalent; TV = television.
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
7
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
activity/exercise in facilitating changes in eating behaviors differed substantially between
the EXP and COM treatments.
The EXP treatment incorporated The
Coach Approach exercise-support protocol32 paired with a nutrition behaviorchange component developed for this
research. It was based on 1) results from
previous behavioral weight-management
treatments,14,17,33,62-64 2) exploratory studies
of psychosocial predictors of weight-loss
behaviors,33,39,57 3) findings suggesting that
behavioral mechanisms required to foster
weight loss differ from those required to
maintain lost weight,16,65 and 4) the suggested benefits of targeting specific and
measurable behaviors for change (eg, increasing FV rather than addressing numerous and detailed elements of the diet).66
Beginning at baseline, The Coach Approach
protocol32 supported adherence to newly
initiated exercise through six 45-minute
meetings with a trained wellness counselor
possessing at least 1 national certification
(eg, American College of Sports Medicine).
These were conducted in a private office
over 6.5 months. Each participant’s exercise
plan, both initially and in revisions during
subsequent meetings, was based on the participant’s preferred type of physical activity
and tolerance. Most of the meeting time was,
however, spent on the development of specific self-regulatory skills such as long- and
short-term goal setting paired with progress
monitoring, dissociation from discomfort,
cognitive restructuring, stimulus control,
behavioral contracting, controlling behavioral prompts and triggers, and relapse prevention. Exercise-induced changes in mood
(eg, anxiety, energy level) were assessed both
in response to a single bout of physical activity and for 1 to 2 months, and displayed
through responses to items embedded in the
supporting computer application.
After 8 weeks of concentration exclusively on maintaining regular exercise, the
components for eating behavior change
were sequentially added. First, guidance
and practice on methods for kcal tracking
was individually provided in two 30-minute
meetings over 2 weeks. Energy-intake goals
were based on each participant’s weight (eg,
1500 kcal/day for a weight range of 79-99
kg), and various methods for recording food
and corresponding kcal intake were made
available (eg, through an approved Web
site, an approved application for hand-held
devices, or a provided paper form and use of
an approved “calorie counter” book). Next,
10 nutrition sessions of 60 minutes each
focused on weight reduction were administered by trained wellness counselors (supported by a manual) at 2-week intervals in
groups of 8-15 participants. Their primary
aim was to generalize, adapt, and extend
self-regulatory skills developed during The
Figure 1. Timeline of the Experimental Treatment, Comparison Treatment, and Oxford Cognitive Behavioural Therapy.
B = baseline; kcal = kilocalories; LEARN = lifestyle, exercise, attitudes, relationships, nutrition.
8
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
Coach Approach exercise-support protocol,32 to self-regulating eating behaviors
(eg, dissociating from exercise-induced
discomfort was generalized to dissociating
from feelings of hunger; recovering from and
rescheduling a missed exercise session was
generalized to recovering from a day of excess
kcal intake and immediately recommitting
to the appropriate limit for the next day).
There was a combination of brief lectures,
individual tasks, and group activities within
each session. The next component, now 28
weeks after baseline, was 4 group sessions in
which self-regulatory skills were addressed in
the context of maintaining lost weight. The
final 10 sessions of the EXP treatment covered skills of self-regulation in both weightloss and weight-loss maintenance contexts
(Figure 1). Treatment content related to the
diet was primarily concentrated on increasing FV intake, although there was a limited
focus on minimizing the consumption of
fat and sugar. Because meeting time was
primarily centered on the development of
self-regulatory skills and the ability to increase self-efficacy for controlling overeating,
participants were referred to the ChooseMyPlate.gov Web site67 for access to detailed,
evidence-based information on nutrition.
The COM treatment replicated methods
used previously in studies,21,42 and consisted
of participants reviewing 1 of the 12 “lessons” of a 265-page print manual entitled
The LEARN (lifestyle, exercise, attitudes,
relationships, nutrition) Program for Weight
Management (10th edition)68 every 2 weeks.
Sections related to behavior change included
“Dealing with Pressures to Eat,” “Preventing
Lapse, Relapse, and Collapse,” “Interpreting Your Progress,” and “Making Physical
Activity Count.” Sections related to diet
included “Fast Foods,” “Rating Your Diet,”
“Vegetables in Your Diet,” and “Breads,
Cereals, Rice, and Pasta in Your Diet.”
Each lesson was followed by a 15-minute
phone conversation initiated by a wellness
counselor to clarify chapter contents, review
each participant’s plans for carrying out
behavioral changes, and answer the participant’s questions. The process of participants
reading chapters and obtaining telephone
follow-ups started at baseline and lasted 24
weeks (Figure 1). The LEARN manual68 suggested that women limit their energy intake
to 1200 kcal per day. A paper monitoring
form was provided for participants to record
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
Figure 2. Representation of mediation models.
foods and drinks consumed, the amount
consumed and their associated kcal, their
corresponding food group categorization,
and optional comments.
Fidelity checks were completed on approximately 15% of treatment components
by study staff. Minor protocol violations
were primarily related to adherence to required time frames within sessions and were
easily rectified through study staff-instructor
interactions. Surveys and weight measurements were completed in a private area.
Data Analyses
To avoid inappropriately inflated effect
sizes such as those reported in the many
studies where data from only weight-loss
program “completers” were included, the
conservative intention-to-treat approach
was used, as suggested.13 Thus, data were
retained from all participants who engaged
in treatment processes. The expectationmaximization algorithm 69 was used to
impute data for the 14% of missing scores.
The required criteria of missing at random
(no systematic bias) was indicated because
participants who were missing data at any
assessment time did not significantly differ
from the sample as a whole on demographic
characteristics or any other study measure.
On the basis of the planned multiple regression equations incorporating 3 predictor
variables, and to detect the moderate effect
of f2 = 0.15 that was indicated in pilot research33 at the statistical power of 0.90 (α =
0.05), a minimum of 98 total participants
was required.70 In tests during the weightloss phase, tolerances (0.60-0.82) and variance inflation factors (1.23-1.67) indicated
a low degree of multicollinearity. During the
weight-loss maintenance phase, tolerances
(0.22-0.86) and variance inflation factors
(1.16-4.58) indicated a low-moderate degree
of multicollinearity.71 Inspection of residual
scatterplots indicated homogeneity of variances and linearity in the data. Both skewness and kurtosis values were < 2 standard
errors. Consistent with previous suggestions
for research within the present context,
change scores were unadjusted for baseline
values.72 Statistical significance was set at α =
0.05 (2-tailed) unless otherwise noted. Statistical analyses were conducted using SPSS,
version 22 (IBM, Armonk, NY).
For all study measures, general linear
model mixed-model repeated measures analyses of variance (ANOVAs) were computed
to determine whether there were significant
score changes across the 5 measurement
times (baseline; months 3, 6, 12, and 24),
and whether those changes differed between
the EXP and COM groups. These were
followed up by planned t tests to assess and
contrast within-group changes during the
weight-loss phase (using 1-tailed tests) and
the weight-loss maintenance phase. Their
associated effect sizes were computed as
Cohen’s d ([meanpost - meanpre]/SDpre). Effect
sizes for ANOVA models were calculated
using partial η-squared (η2p = SSeffect/[SSeffect
+ SSerror]). For d and η2p, 0.20, 0.50, 0.80;
and 0.01, 0.06, 0.14 denote small, moderate, and large effects, respectively.
Part 1: Weight Change
After completing planned ANOVAs and
follow-up tests on weight, and on the basis
of research suggesting that ≥ 5% weight loss
9
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
is the threshold for health benefits,3 the
percentage of participants attaining this
criterion was reported for month 6 (end
of the weight-loss phase) and month 24
(end of the study), by group. Because ≥
3% loss has been the suggested criterion
for maintained weight loss,6 attainment of
this change was also reported at month 24.
Weight-change data previously published
on the Oxford CBT21 were also adapted for
additional contrasting.
for the prediction of change in weight over
the weight-loss phase, were then contrasted.
Given the data collected, all possible temporal intervals of changes in PA and FV during
the course of the 24-month investigation
were similarly contrasted for predicting
change in weight during the weight-loss
maintenance phase. As was previously
suggested,73 wherever possible, behavioral
changes occurring during the weight-loss
phase were statistically controlled for.
Part 2: Behavioral Predictors
of Weight Changes
Part 3: Psychological Predictors
of Behavioral Changes
After completing planned ANOVAs and
follow-up tests on PA and FV, data were
aggregated across groups. The strengths
of bivariate relationships between changes
in PA and FV from baseline-month 3,
baseline-month 6, and month 3-month 6,
After completing planned ANOVAs
and follow-up tests on the five psychological variables, data were aggregated
across groups. Analyses of relationships
of changes in the psychological variables
using temporal intervals and methods
identical to Part 2 were then completed.
Data from the temporal intervals found
to have the strongest relationships served
as the predictors of PA and FV changes in
multiple regression equations.
Because 1) the EXP treatment focus
was on the carry-over of exercise-related
self-regulation and self-efficacy to eatingrelated self-regulation and self-efficacy, 2)
their strong interrelations had previously
been supported,33 and 3) previous theory
suggested their interactions,35,65 after normalizing (centering and standardizing)
scores and confirming expected interrelations, the exercise- and eating-related
self-regulation and self-efficacy measures
were merged for further analyses. Multiple
mediation models incorporating 20,000
bootstrapped resamples74 were specified
where the predictor variable was treatment
Table 2a. Descriptive statistics of study measures and analyses of their changes over 24 months, by groupa
Baseline
(mean ± SD)
Weight (kg)
Experimental
94.95 ± 11.44
Comparison
95.36 ± 10.56
Oxford CBTd
92.34 ± 8.81
Physical activity (METs/week)
Experimental
8.31 ± 7.30
Comparison
9.65 ± 8.14
Fruit and vegetable intake (servings/day)
Experimental
3.95 ± 1.97
Comparison
3.30 ± 1.81
Self-regulation for exercise
Experimental
22.53 ± 6.32
Comparison
23.07 ± 6.32
Self-efficacy for exercise
Experimental
25.87 ± 9.47
Comparison
22.36 ± 9.73
Total mood disturbance
Experimental
25.69 ± 15.45
Comparison
21.71 ± 11.50
Self-regulation for controlled eating
Experimental
23.75 ± 5.60
Comparison
22.05 ± 5.78
Self-efficacy for controlled eating
Experimental
87.82 ± 31.21
Comparison
88.24 ± 33.80
Month 3
(mean ± SD)
Month 6
(mean ± SD)
Month 12
(mean ± SD)
Month 24
(mean ± SD)
Effect for timeb
(F(4, 432) [η2p])
Time × group
interaction
(F(4, 432) [η2p])
92.03 ± 11.84
94.46 ± 10.63
NA
89.21 ± 11.57
93.27 ± 10.44
83.29 ± 10.39
89.40 ± 11.86
93.51 ± 11.07
84.33 ± 11.11
89.84 ± 13.58
94.11 ± 11.23
89.45 ± 11.48
26.25c [0.196]
6.84c [0.060]
28.65 ± 13.56
23.51 ± 15.44
32.77 ± 15.47
22.02 ± 12.82
32.44 ± 15.16
23.20 ± 12.60
23.59 ± 15.15
22.40 ± 12.26
89.01c [0.452]
9.50c [0.081]
5.81 ± 2.39
4.25 ± 2.04
6.42 ± 2.14
4.46 ± 2.23
6.23 ± 2.24
4.73 ± 1.99
5.56 ± 1.90
4.62 ± 1.98
38.92c [0.265]
4.55e [0.040]
32.51 ± 4.36
26.96 ± 6.12
33.04 ± 4.28
26.58 ± 6.91
32.27 ± 4.59
26.58 ± 6.75
29.87 ± 5.96
26.56 ± 6.69
64.03c [0.372]
14.63c [0.119]
33.38 ± 10.08
25.47 ± 10.89
34.98 ± 10.52
25.29 ± 12.25
33.25 ± 11.73
25.98 ± 11.22
29.36 ± 11.82
25.49 ± 10.84
14.64c [0.119]
4.27e [0.038]
9.17 ± 15.00
12.25 ± 8.12
4.55 ± 11.54
13.89 ± 11.50
7.96 ± 11.88
12.78 ± 11.88
9.38 ± 13.87
13.47 ± 11.51
53.56c [0.332]
8.62c [0.074]
31.25 ± 4.57
26.91 ± 5.54
32.51 ± 4.00
26.78 ± 5.59
31.96 ± 4.19
26.44 ± 5.23
29.82 ± 5.68
26.29 ± 5.20
64.16c [0.373]
5.64c [0.050]
114.96 ± 26.95
104.65 ± 27.17
126.48 ± 26.51
108.00 ± 30.76
127.26 ± 26.90
110.35 ± 30.45
124.69 ± 28.34
108.18 ± 29.90
47.29c [0.305]
4.39e [0.039]
Experimental group, n = 55; comparison group, n = 55.
Analysis of variance effects for time, and time × group interactions, contrast changes from baseline to month 24.
p < 0.001.
d
These data were adapted from previous research21 for contrasting purposes.
e
p < 0.01.
CBT = Cognitive Behavioural Therapy; MET = metabolic equivalent; SD = standard deviation.
a
b
c
10
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ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
type (0 = COM; 1 = EXP), the outcome
variable was weight change during the
weight-loss or weight-loss maintenance
phase, and the possible mediators were
changes in mood and the merged selfregulation and self-efficacy measures. In
a multiple mediation model, significance
of a mediator is identified when its corresponding 95% confidence interval for an
indirect effect does not include 0. A graphical representation of mediation models is
given in Figure 2.
Table 2b. Planned follow-up t-test results over the weight-loss phase
(baseline-month 6) and weight-loss maintenance phase (months 6-12), by groupa
Weight (kg) change
Weight-loss phase
Weight-loss maintenance phase
Entire study period
(baseline-month 24)
Physical activity change (METs/week)
Weight-loss phase
Weight-loss maintenance phase
Fruit and vegetable intake change (servings/day)
Weight-loss phase
Weight-loss maintenance phase
Self-regulation for exercise change
Weight-loss phase
Weight-loss maintenance phase
Self-efficacy for exercise change
Weight-loss phase
Weight-loss maintenance phase
Total mood disturbance change
Weight-loss phase
Weight-loss maintenance phase
Self-regulation for controlled eating change
Weight-loss phase
Weight-loss maintenance phase
Self-efficacy for controlled eating change
Weight-loss phase
Weight-loss maintenance phase
Group
t(54)
p vaue
d
EXP
COM
EXP
COM
EXP
COM
-11.18
-5.13
0.61
1.87
-4.59
-1.86
< 0.001
< 0.001
0.274
0.033
< 0.001
0.068
0.50
0.20
0.05
0.08
0.45
0.12
EXP
COM
EXP
COM
11.83
8.89
-4.42
0.30
< 0.001
< 0.001
< 0.001
0.764
3.18
1.52
0.59
0.03
EXP
COM
EXP
COM
7.67
3.90
-3.07
1.04
< 0.001
< 0.001
0.003
0.302
1.24
0.64
0.40
0.07
EXP
COM
EXP
COM
10.79
4.56
-4.54
-0.03
< 0.001
< 0.001
< 0.001
0.974
1.66
0.56
0.53
0.003
EXP
COM
EXP
COM
8.56
0.79
-4.10
0.19
< 0.001
0.039
< 0.001
0.848
0.96
0.30
0.53
0.02
EXP
COM
EXP
COM
-9.21
-5.58
2.86
-0.44
< 0.001
< 0.001
0.006
0.663
1.37
0.68
0.42
0.04
EXP
COM
EXP
COM
10.33
6.54
-4.25
-1.25
< 0.001
< 0.001
0.001
0.218
1.56
0.81
0.67
-0.08
EXP
COM
EXP
COM
8.15
4.37
-0.46
0.13
< 0.001
< 0.001
0.646
0.899
1.24
0.58
0.07
0.01
Experimental group (EXP), n = 55; Comparison group (COM), n = 55.
MET = metabolic equivalent.
a
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
If a significant mediator was found in
the above analysis over the weight-loss
phase, follow-up simple mediation models
(eg, models with only a single mediator)
were then specified to determine whether
change in that psychological variable and
weight demonstrated a reciprocal relationship. A reciprocal relationship is identified
if, after reversing the position of the original outcome and mediator variable within
a complementary mediation model, both
equations demonstrate significant mediation.42 Because the presence of a reciprocal
relationship may not be assessed directly
through multiple mediation, or with covariates, these analyses were possible during only the weight-loss phase.
RESULTS
There was no significant difference at
baseline between the EXP and COM
groups on any study measure. Table 2a
provides descriptive statistics of data at
baseline and at months 3, 6, 12, and 24.
For all variables, there was a significant
overall effect and a significant time × group
interaction during the 24-month study
(Table 2a). Results of follow-up, withingroup t-tests, are given in Table 2b.
Part 1: Weight Change
During the weight-loss phase, although
within-group reductions in weight in the
EXP group (-5.73 kg) and COM group
(-2.09 kg) were both significant, the EXP
group had a significantly greater betweengroup reduction in weight, t(108) = 5.56, p
< 0.001, d = 1.07. During the weight-loss
maintenance phase, within-group weight
regain in the EXP group (0.63 kg) was
not significant, whereas it was significant
in the COM group (0.84 kg). During
the full 24-month duration of the study,
reduction of weight was significant in the
EXP group (-5.11 kg), but not significant
in the COM group (-1.25 kg). Betweengroup reduction in weight was significantly
greater over 24 months in the EXP group,
t(108) = 2.95, p = 0.004, d = 0.58.
At month 6, ≥ 5% weight loss was
found in 65.5% of EXP and 18.2%
of COM participants. At month 24,
≥ 5% weight loss was found in 52.7% of
EXP and 16.4% of COM participants. At
month 24, ≥ 3% weight loss was found
in 63.6% of EXP and 38.2% of COM
11
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
participants. Figure 3 provides a graphic representation of percentages of weight change
for 24 months, including data adapted from
research on the Oxford CBT.21
Part 2: Behavioral Predictors
of Weight Changes
Physical Activity
During the weight-loss phase, although
within-group increases in PA in the EXP
group and the COM group were both
significant, the EXP group had a significantly greater between-group increase,
t(108) = 4.86, p < 0.001, d = 0.94. There
was a significant between-group difference in PA change during the weight-loss
maintenance phase, t(108) = -3.93, p
< 0.001, d = 0.77, with the EXP group
demonstrating a significant within-group
reduction and the COM group showing
no significant change.
Eating
During the weight-loss phase, withingroup increases in FV in the EXP group
and the COM group were both significant,
and significantly greater in the EXP group,
t(108) = 2.97, p = 0.002, d = 0.57. There
was a significant between-group difference in FV change during the weight-loss
maintenance phase, t(108) = -3.20, p
= 0.002, d = 0.64, with the EXP group
having a significant within-group reduction and the COM group exhibiting no
significant change.
Prediction of Weight Change
The temporal interval that was the strongest predictor of weight change during the
weight-loss phase was baseline-month 6 for
both PA and FV. β(standard error)-values
were -0.38(0.05) and -0.30(0.33), respectively; p values < 0.001. The temporal
interval that was the strongest predictor
of weight change during the weight-loss
maintenance phase was month 6-month
24 for both PA and FV. β(standard error)values were -0.45(0.11) and -0.28(0.87),
respectively; p values < 0.001 and 0.018,
respectively.
the EXP group, t(108) = 5.64, p < 0.001,
d = 1.09. There was a significant betweengroup difference in SR-exercise reduction
during the weight-loss maintenance phase,
t(108) = -3.51, p = 0.001, d = 0.67, with
the EXP group demonstrating a significant
within-group reduction and the COM
group showing no significant change.
Self-Efficacy for Exercise
During the weight-loss phase, withingroup increases in SE-exercise in the EXP
group and the COM group were both significant, and significantly greater in the EXP
group, t(108) = 2.94, p = 0.007, d = 0.52.
There was a significant between-group difference in SE-exercise change during the
weight-loss maintenance phase, t(108) =
-3.39, p = 0.001, d = 0.65, with the EXP
group showing a significant within-group
reduction and the COM group having no
significant change.
Mood
During the weight-loss phase, within-group reductions in Mood score in
both the EXP group and the COM
group were significant, and significantly
greater in the EXP group, t(108) = -4.98,
p = 0.002, d = 0.98. There was a significant between-group difference in Mood
change during the weight-loss maintenance phase, t(108) = 2.70, p = 0.008,
d = 0.54, with the EXP group demonstrating a significant within-group score
increase and the COM group exhibiting
no significant change.
Self-Regulation for Controlled Eating
During the weight-loss phase, withingroup increases in SR-eating in the EXP
group and the COM group were both
significant, and significantly greater in the
EXP group, t(108) = 3.64, p < 0.001, d =
1.08. There was a significant between-group
difference in SR-eating reduction during
the weight-loss maintenance phase, t(108)
= -2.57, p = 0.012, d = 0.52, with the EXP
group having a significant within-group
reduction and the COM group showing
no significant change.
Self-Efficacy for Controlled Eating
During the weight-loss phase, withingroup increases in SE-eating in the EXP
group and the COM group were significant, and significantly greater in the EXP
group, t(108) = 2.88, p = 0.005, d = 0.55.
There was no significant between-group
difference in SE-eating change during the
weight-loss maintenance phase, t(108) =
-0.48, p = 0.635, d = 0.10, with neither
the EXP or COM group demonstrating a
significant within-group change.
Prediction of Physical Activity Change
The temporal interval that was the
strongest predictor of change in PA
during the weight-loss phase was from
baseline-month 6 for SR-exercise,
SE-exercise, and Mood. β(standard error)values were 0.58(0.15), 0.50(0.10), and
-0.46(0.08), respectively; all p values <
0.001. The temporal interval that was the
strongest predictor of change in PA during
Part 3: Psychological Predictors
of Behavioral Changes
Self-Regulation for Exercise
During the weight-loss phase, withingroup increases in SR-exercise in the EXP
group and the COM group were both
significant, and significantly greater in
12
Figure 3. Percentage of body weight change over 24 months, by group.
CBT = Cognitive-Behavioural Therapy.
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
the weight-loss maintenance phase was baseline-month 24 for SR-exercise, SE-exercise,
and Mood. β(standard error)-values were
0.65(0.24), 0.57(0.14), and -0.52(0.17),
respectively; all p values < 0.001.
After incorporating the above temporal
intervals into the following two models,
the multiple regression equation predicting
PA change during the weight-loss phase
was significant. Changes in SR-exercise,
SE-exercise, and Mood were each significant independent predictors (after controlling for one another). The prediction of
PA change during the weight-loss maintenance phase was significant. Changes
in SR-exercise and SE-exercise, but not
Mood, were significant independent predictors (Table 3).
during the weight-loss maintenance phase
was month 12-month 24 for SR-eating,
and baseline-month 24 for both SE-eating
and Mood. β(standard error)-values were
0.19(0.04), 0.47(0.01), and -0.31(0.02),
respectively; all p values < 0.050.
After incorporating the above temporal
intervals, the multiple regression equation
predicting FV change during the weightloss phase was significant. Changes in
SR-eating, SE-eating, and Mood were
each significant independent predictors
(after controlling for one another) (Table
3). The prediction of FV change over the
weight-loss maintenance phase was significant. Neither changes in SR-eating,
SE-eating, nor Mood were significant
independent predictors (Table 3).
The temporal interval that was the
strongest predictor of change in FV during the weight-loss phase was the same for
baseline-month 3 and baseline-month 6
for SR-eating, and was baseline-month 6
for both SE-eating and Mood. β(standard
error)-values were 0.41(0.03), 0.45(0.01),
and -0.37(0.08), respectively; all p values
< 0.001. The temporal interval that was
the strongest predictor of change in FV
As expected, correlations of baseline,
baseline-month 6, and month 6-month
24 scores between the exercise- and eatingrelated self-regulation measures (r-values =
0.61-0.66), and exercise- and eating-related
self-efficacy measures (r-values = 0.40-0.48)
were significant (all p values < 0.001). This
further supported merging the exerciseand eating-related self-regulation (ie, SRmerged) and self-efficacy (ie, SE-merged)
Prediction of Eating Change
Consolidated Model for Weight-Loss Effects
Table 3. Results of multiple regression analyses for the prediction of changes in
physical activity and fruit and vegetable intake
Predictor
β
Δ Physical activity, baseline-month 6
Model
Δ Self-regulation for exercise
0.36
Δ Self-efficacy for exercise
0.21
Δ Overall negative mood
-0.25
Δ Physical activity, month 6-month 24
Model
Δ Self-regulation for exercise
0.42
Δ Self-efficacy for exercise
0.27
Δ Overall negative mood
-0.23
Δ Fruit and vegetable intake baseline-month 6
Model
Δ Self-regulation for controlled eating
0.20
Δ Self-efficacy for controlled eating
0.26
Δ Overall negative mood
-0.19
Δ Fruit and vegetable intake month 6-month 24
Model
Δ Self-regulation for controlled eating
0.12
Δ Self-efficacy for controlled eating
0.33
Δ Overall negative mood
-0.15
Δ = change in.
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
Standard
error
R2
F
df
p value
0.42
25.96
3, 109
< 0.001
< 0.001
0.028
0.003
0.59
9.19
6, 109
0.006
< 0.001
0.044
0.093
0.52
13.08
3, 109
< 0.001
0.048
0.013
0.049
0.19
0.11
0.08
0.28
0.16
0.13
0.04
0.01
0.01
0.46
0.04
0.01
0.02
4.57
6, 109
< 0.001
0.202
0.080
0.352
measures for the planned mediation analyses. The same Mood scale was used in both
exercise and eating contexts so no such
merger was needed.
In a consolidated model, the SRmerged, SE-merged, and Mood measures
(changes from baseline-month 6) were
entered as possible mediators of the relationship between treatment type (COM
or EXP) and weight change during the
weight-loss phase. The overall model was
significant, R2 = 0.35, F(4, 105) = 14.23,
p < 0.001. Only change in SR-merged was
a significant mediator within the equation (Table 4, Analysis I). In the planned
simple mediation follow-ups, change in
SR-merged significantly mediated the
relationship between treatment type and
weight change; and weight change significantly mediated the relationship between
treatment type and change in SR-merged.
This indicated a reciprocal relationship
between increases in self-regulation and
lost weight during the weight-loss phase
(Table 4, Analysis I-a).
The SR-merged, SE-merged, and Mood
measures (changes from month 6 to month
24) were entered as possible mediators of
the relationship between treatment type
and weight change during the weight-loss
maintenance phase. The overall model was
significant, R2 = 0.20, F(7, 102) = 3.61, p
= 0.002. Only change in SE-merged was
a significant mediator within the equation
(Table 4, Analysis II).
Post Hoc Tests
In post hoc analyses of only the EXP
group, a significant quadratic (invertedU) effect was found during the 24 months
of the study in each of the psychological
variables, which suggested a reduction in
gains acquired during the initial 6 to12
months. Effect sizes (η2p) associated with
those significant ANOVA models (all p
values < 0.001) were stronger than for
the corresponding linear relationship for
SR-exercise (0.611), SE-exercise (0.417),
Mood (0.504), and SR-eating (0.600); but
not SE-eating (0.374).
DISCUSSION
Overall, findings associated with the EXP
treatment were promising. The absence
of significant regain of that group’s weight
loss of more than 6% was atypical, and
represented a notable success (Figure 3).4,5
13
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
The experimental format not only elucidated psychological correlates of behavioral prerequisites to weight reduction,
it highlighted temporal implications for
their application within both weight-loss
and weight-loss maintenance phases.
Innovative treatment components and
administrative formats were successfully
incorporated within a practical setting
that suggests potential for widespread
application. The cost associated with
implementation of the EXP treatment
approximated US$400 per participant.
This was about 10% to 15% of the cost estimated for both the Oxford CBT and an
average of the 3 commercial weight-loss
programs currently having the strongest
market share.75
Specific Findings
Part 1 clearly demonstrated the superiority of the EXP treatment over the COM
treatment for weight loss at all measured
time points. Regain of weight in the EXP
group was only a nonsignificant 0.7% of
participants’ original weight, which has
not been observed in the great majority
of treatment studies of individuals with
obesity where a climb toward baseline
weight (or higher) almost always occurred
after about 6 months of loss.4,5 When contrasted with the Oxford CBT (Figure 1),
the EXP treatment had a far less acute slope
of weight regain and a much larger proportion of participants who maintained ≥ 5%
weight loss at month 24 (52.7% vs 38.8%)
(Figure 3).21 This suggested substantial improvements in health risks within the EXP
group. In Part 2, effect sizes for increases
in both PA and FV during the weight-loss
phase were about twice as large in the EXP
group. Those large behavioral improvements demonstrated a partial reversal during the second year. In Part 3, within the
weight-loss phase, effect sizes of improvements on the psychosocial predictors of PA
and FV within the EXP group were also
double those in the COM group (all large
effects with d-values of 0.96-1.66). However, an inversion of some of those gains appeared between month 12 and month 24.
Because these trajectories could adversely
impact participants’ weight-management
behaviors and weight in subsequent years,
extensions of this research are presently
evaluating noninvasive methods to lessen
such “slippage” through periodic telephone
and/or e-mail follow-ups after in-person
treatment components conclude. These
follow-up contacts will aim to bolster the
use of previously addressed self-regulatory
skills and feelings of control over behaviors
associated with weight management. Part
3 of this study determined that changes
in self-regulation, self-efficacy, and mood
during the full 6 months of the weight-loss
phase best-predicted increased PA and FV.
Findings also suggested that changes in
self-regulation applied to eating changes
might be particularly important within
the first several months of treatment.
Changes in those 3 psychological factors
over the entire weight-maintenance phase
(months 6-24) best predicted a favorable
direction for PA and FV. However, findings suggested that self-regulation for
controlled eating is especially important
during the second year. When the above
results were consolidated, important findings also emerged. Data suggested that
an emphasis on self-regulation during the
weight-loss phase, and an emphasis on selfefficacy during the weight-loss maintenance
phase, will optimize weight-management
Table 4. Results from multiple mediation and reciprocal effects analyses (N = 110)a
Predictor
Mediatorc
Outcome
Analysis I: Weight-loss phase (multiple mediation)
Treatment typed
Δ Self-regulation Δ Weight
Treatment type
Δ Self-efficacy
Δ Weight
Treatment type
Δ Mood
Δ Weight
Pathb a
β ± standard error
(p value)
Path b
β ± standard error
(p value)
Path c
β ± standard
error (p value)
Path c’
β ± standard
error (p value)
Indirect effect
β ± standard
error (95% CI)
1.13 ± 0.24
(< 0.001)
-2.13 ± 0.70
(0.002)
-8.03 ± 1.44
(< 0.001)
-4.61 ± 1.55
(0.004)
-2.42 ± 1.05
(-4.81, -0.65)
0.77 ± 0.24 (0.002)
0.20 ± 0.71 (0.780)
-8.03 ± 1.44
(< 0.001)
-8.03 ± 1.44
(< 0.001)
-4.61 ± 1.55
(0.004)
-4.61 ± 1.55
(0.004)
0.16 ± 0.71
(-1.27, 1.71)
-1.16 ± 0.71
(-2.79, 0.06)
-8.03 ± 1.44
(< 0.001)
1.13 ± 0.24
(< 0.001)
-5.46 ± 1.47
(< 0.001)
0.63 ± 0.25
(0.015)
-2.56 ± 0.81
(-4.53, -1.23)
0.51 ± 0.14
(0.26, 0.82)
1.91 ± 2.88
(0.509)
1.91 ± 2.88
(0.509)
1.91 ± 2.88
(0.509)
1.42 ± 2.72
(0.604)
1.42 ± 2.72
(0.604)
1.42 ± 2.72
(0.604)
0.98 ± 1.21
(-2.20, 3.32)
-1.09 ± 0.77
(-3.77, -0.10)
0.60 ± 0.60
(-0.14, 2.36]
-0.86 ± 0.17
1.35 ± 0.79 (0.093)
(< 0.001)
Analysis I-a: Weight-loss phase (simple mediation for reciprocal effects analysis)
Treatment type
Δ Self-regulation Δ Weight
1.13 ± 0.24
-2.27 ± 0.54
(< 0.001)
(< 0.001)
Treatment type
Δ Weight
Δ Self-8.03 ± 1.44
-0.06 ± 0.15
regulation
(< 0.001)
(< 0.001)
Analysis II: Weight-loss maintenance phase (multiple mediation)
Treatment type
Δ Self-regulation Δ Weight
-0.17 ± 0.20
-5.91 ± 1.52
(0.415)
(< 0.001)
Treatment type
Δ Self-efficacy
Δ Weight
-0.38 ± 0.20
2.87 ± 1.75 (0.104)
(0.055)
Treatment type
Δ Mood
Δ Weight
0.16 ± 0.14 (0.055) 3.81 ± 2.07 (0.068)
Analyses are based on a bootstrapping procedure for multiple mediation incorporating 20,000 resamples.74
Path a = predictor→mediator; Path b = mediator→outcome; Path c = predictor→outcome; Path c’ = predictor→outcome, controlling for the mediator.
c
Δ = change from baseline-month 6 for Analysis I and I-a; or baseline-month 24, controlling for changes from baseline-month 6 (for Analysis II).
d
For treatment type, 0 = comparison group, 1 = experimental group.
Δ change in; 95% CI = 95% confidence interval.
a
b
14
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
outcomes. During the weight-loss phase,
changes in self-regulation and weight
appeared to reinforce one another mutually. Overall, results supported the EXP
treatment’s ability to improve mood and
increase self-regulation and self-efficacy related to both physical activity and healthy
eating behaviors.
Fit with Previous Research
Although most weight-loss treatments
employ an educational approach that focuses upon restricting energy intake, the
use of cognitive-behavioral methods and
exercise within weight-loss interventions
is not novel. However, comprehensive
reviews suggest that even the most stateof-the-art, theory-based approaches primarily targeting eating changes have been
unsuccessful beyond the very short term.4
Within this report, findings from a previously described17 and tested21 weight-loss/
weight-loss maintenance protocol (Oxford
CBT) was contrasted with the EXP treatment because of its theoretical similarity,
similar research design, and seemingly
strong cognitive-behavioral approach. As
has been typical, however, exercise was
treated as a favorable adjunct to nutritional
change rather than a key component of
that protocol, and its maintenance of
weight loss was unsuccessful.21 Guided by
suggestions of the consistent relationship
between exercise and maintained weight
loss,23-25 previous experimental research
on (modifiable) psychosocial correlates
of weight loss,40-42,76 our own program of
research on the generalization of exerciseinduced psychological changes to eating
changes during the short term,33,77-85 and
recommendations from the National Institutes of Health to address adherence to
exercise and establish relevant behavioral
skills before attempting weight loss,22 we
substantially modified and extended previous approaches. We incorporated assumptions that cognitive-behaviorally supported
exercise can facilitate changes in eating and
weight through associated psychological
changes. Although the present data cannot determine precisely what treatment
component(s) or implementation methods
were most associated with the present positive results, future research designs might
facilitate a more comprehensive decomposition of findings to determine the most
The Permanente Journal/Perm J 2016 Summer;20(3):15-146
salient treatment components and, thus,
further enhance effects. We encourage future related research to also study weightloss and weight-loss maintenance phases
separately through behavioral changes and
their psychological predictors, because
processes within these phases appear to
differ from one another. Continued evaluation of temporal aspects might facilitate
a more precise process that further refines
the benefits of emphasizing specific treatment components at specific times, which
might also vary by personal characteristics
(eg, initial weight, psychological profile).
The present determination that weight loss
might most benefit from a concentration
on self-regulation, whereas weight-loss
maintenance might most benefit from a
concentration on self-efficacy, is a start
in that direction. Although this research
based the architecture of the EXP treatment and the selection and measurement
of behavioral and psychological constructs
on social cognitive and self-efficacy theory
and the many studies following from those
paradigms, additional theories (eg, selfdetermination theory, theory of planned
behavior) might also serve as a basis in
extensions of this research. The contrast
of those results with the present findings
will undoubtedly be instructive.
Study Limitations
To increase confidence in findings and
assess their generalizability for application, present limitations such as the use
of a homogeneous sample of primarily
white and middle-class women who were
motivated enough to volunteer for treatment require attention. Thus, replications
with men, with other racial/ethnic and
socioeconomic groups, and possibly with
participants who were strongly referred by
medical practitioners (to minimize effects
of volunteerism) will be beneficial. Replications are also required with overweight
participants and participants with a more
severe degree of obesity (ie, class 3/morbid
obesity). Other limitations of this research
indicate a need for better controls for social
support and expectation effects that are
likely to bias results when interventions
differ in length and amount of in-person
contact, as was the case here.86 Thus, the
use of an attention-matched, or a waitlist, control group might also be useful
in replications of this research. Although
the repeated-measures design of this study
was a strength, multiple administrations of
the same self-report instrument increases
its measurement error.87 Although it is
difficult to accomplish in field settings
(that benefit the applicability of findings88,89), the use of more objective and
comprehensive measures of exercise (eg,
accelerometry) and dietary intake (eg,
more extensive nutrition recall instruments) would increase accuracy of the
behavioral outcomes. Within the present
study, however, because of the length of
time required for completion of the seven
self-report surveys, any additional time
burden placed on participants might have
challenged the quality of their responses.90
CONCLUSION
Although the above limitations should
be acknowledged, and replications are
needed, the EXP treatment has considerable possibilities for dissemination. Its
format allows for low-cost implementation
in community-based health-promotion
settings by staff members with general
wellness credentials. It also has a strong
potential for physician referral. Whereas
pharmacologic and surgical interventions
for obesity are available, improving physical activity and eating behaviors will effectively address obesity and their associated
health risks for most affected individuals.
Despite the fact that sustained improvements in eating and exercise have been difficult for behavioral medicine to effectuate,
the present research introduced innovative
behavior-change methods that empowered
individuals to effectively deal with dayto-day barriers that consistently served
as impediments to maintaining clinically
important losses in body weight. The use
of manageable amounts of exercise to build
the self-regulatory skills and improvements
in mood that promote a newfound sense of
control over eating behaviors might prove
to be one of the most viable solutions to
the longstanding epidemic of obesity. v
Disclosure Statement
The authors have no conflicts of interest to
disclose.
Acknowledgment
Mary Corrado, ELS, provided editorial assistance.
15
ORIGINAL RESEARCH & CONTRIBUTIONS
Weight Loss and the Prevention of Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation Generalizing to Controlled Eating
How to Cite this Article
Annesi JJ, Johnson PH, Tennant GA, Porter KJ,
McEwen KL. Weight loss and the prevention of
weight regain: Evaluation of a treatment model of
exercise self-regulation generalizing to controlled
eating. Perm J 2016 Summer;20(3):15-146. DOI:
http://dx.doi.org/10.7812/TPP/15-146.
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17
credits available for this article — see page 112.
ORIGINAL RESEARCH & CONTRIBUTIONS
A Pharmacist-Staffed, Virtual Gout Management Clinic
for Achieving Target Serum Uric Acid Levels:
A Randomized Clinical Trial
Robert Goldfien, MD; Alice Pressman, PhD, MS;
Alice Jacobson, MS; Michele Ng, PharmD; Andrew Avins, MD, MPH
E-Pub: 07/01/2016 http://dx.doi.org/10.7812/TPP/15-234
ABSTRACT
Context: Relatively few patients with gout receive appropriate treatment.
Objective: To determine whether a pharmacist-staffed gout management program is
more effective than usual care in achieving target serum uric acid (sUA) levels in gout
patients.
Design: A parallel-group, randomized controlled trial of a pharmacist-staffed,
telephone-based program for managing hyperuricemia vs usual care. Trial duration
was 26 weeks.
Main Outcome Measures: Primary outcome measure was achieving sUA levels at or
below 6 mg/dL at the 26-week visit. Secondary outcome was mean change in sUA levels
in the control and intervention groups. Participants were adults with recurrent gout and
sUA levels above 6.0 mg/dL. Participants were randomly assigned to management by a
clinical pharmacist following protocol or to monitoring of sUA levels but management
of their gout by their usual treating physician.
Results: Of 102 patients who met eligibility criteria, 77 subjects obtained a baseline
sUA measurement and were entered into the trial. Among 37 participants in the intervention group, 13 (35%) had sUA levels at or below 6.0 mg/dL at 26 weeks, compared
with 5 (13%) of 40 participants in the control group (risk ratio = 2.8, 95% confidence
interval [CI] = 1.1 to 7.1, p = 0.03). The mean change in sUA levels among controls
was +0.1 mg/dL compared with -1.5 mg/dL in the intervention group (sUA difference =
-1.6, 95% CI = -0.9 to -2.4, p < 0.001).
Conclusions: A structured pharmacist-staffed program was more effective than usual
care for achieving target sUA levels. These results suggest a structured program could
greatly improve gout management.
INTRODUCTION
Gout is the most common inflammatory arthritis in men.1,2 It is well recognized
that successful long-term management of
gout and hyperuricemia remains elusive.3-5
Unlike other common forms of inflammatory arthritis, gout is not an autoimmune
disease and instead is understood to be
a manifestation of chronic elevation of
serum uric acid (sUA). Studies of gouty
arthritis have provided important insights
into other inflammatory conditions that
are of great interest to rheumatologists.6,7
Perm J 2016 Summer;20(3):15-234
There is also a growing literature documenting the association of chronic hyperuricemia and gout with diabetes, chronic
kidney disease, and adverse cardiovascular
outcomes.8-11 Therefore, improving the
long-term management of gout may lead
to other important health benefits as well.
Guidelines for the treatment of acute
gout and the optimal management of
hyperuricemia have been evolving and
have been the subject of several recent reviews.12-14 These reviews highlight several
barriers to optimal gout management,
including poor patient adherence; the need
for better patient education; and a lack of
awareness of management guidelines, especially among primary care physicians. Notably, unlike other forms of inflammatory
arthritis (eg, rheumatoid arthritis), there
is a straightforward and easily monitored
outcome measure that correlates with optimal long-term outcomes in gout. Both the
European League Against Rheumatism15
and the American College of Rheumatology16 recommend that patients with
tophaceous or recurrent gout be treated
with urate-lowering therapy (ULT) to a
target sUA level below 6.0 mg/dL. Maintaining the sUA at that level eventually
leads to cessation of gout flares.17 This fact
is particularly notable given the burden of
gout in the US. One study found there
were 3.9 million outpatient visits for gout
in the US in 2002.18 Unfortunately, only
a minority of patients with gout receives
appropriate treatment, including doses of
ULT sufficient to achieve this target.11,19
Specifically, deficiencies in ULT management include a lack of appropriate monitoring, failure to treat-to-target, and fear
of ULT dose escalation in some patients,
particularly those with chronic kidney
disease.12,13 Thus, there is a need for new,
practical, and more effective approaches to
the management of gout.
To address the problem of inadequate
adherence to gout treatment guidelines,
we previously developed a management
model consisting of a telephone-based
“clinic” composed of a clinical pharmacist
under the supervision of a board-certified
Robert Goldfien, MD, is the Chair of the Chiefs of Rheumatology for The Permanente Medical Group in
Richmond, CA. E-mail: [email protected]. Alice Pressman, PhD, MS, is the Director of Analytics and
Evaluation in the Department of Research, Development, and Dissemination for Sutter Health in Walnut
Creek, CA. E-mail: [email protected]. Alice Jacobson, MS, is a Senior Statistical Analyst in the
Department of Research, Development, and Dissemination for Sutter Health in Walnut Creek, CA. E-mail:
[email protected]. Michele Ng, PharmD, is a Clinical Pharmacist in the Department of Outpatient
Pharmacy at the Oakland Medical Center in CA. E-mail: [email protected]. Andrew Avins, MD, MPH, is
a Research Scientist at the Division of Research in Oakland, CA. E-mail: [email protected].
18
The Permanente Journal/Perm J 2016 Summer;20(3):15-234
ORIGINAL RESEARCH & CONTRIBUTIONS
A Pharmacist-Staffed, Virtual Gout Management Clinic for Achieving Target Serum Uric Acid Levels: A Randomized Clinical Trial
rheumatologist. 20 In this model, the
pharmacist uses telephone encounters to
implement a simple protocol, initiating
and adjusting standard gout medications
in patients referred by their primary care
physicians for management of recurrent or
tophaceous gout. Patients are monitored
by the clinic until they have 2 consecutive target sUA results at least 3 months
apart; they are then discharged back to the
care of their primary physician. We previously reported a case series from this pilot
study, analyzing the outcomes of the first
100 patients referred to the program. The
results of this pilot were encouraging, and
the current study (Gout Uric Acid ReDuction, or GUARD trial) was conducted to
test whether this model would be more
effective than usual care in the context of
a randomized controlled trial.
The GUARD study was a randomized,
parallel-group, open-label clinical trial of a
pharmacist-staffed, structured gout management program compared with usual care.
the care of their primary care physician or
rheumatologist. If physician consent was
obtained, patients were contacted by letter
accompanied by a description of the study
and a written informed consent document.
The program pharmacist telephoned the
potential subject and described the study,
answered any questions, and then obtained
verbal consent. Each participant was provided written educational material on gout
at the time of program entry. Randomization was accomplished by assigning an
identification number using a balanced,
blocked randomization list with variable
block sizes (used to reduce the likelihood of
an unbalanced or biased randomization).
After randomization, a baseline laboratory assessment was required of all potential
participants to begin the trial. (The laboratory measurements were obtained after
randomization for practical implementation reasons.) This panel included sUA and
alanine aminotransferase values, estimated
glomerular filtration rate, and complete
blood cell count. The trial protocol was approved by the Kaiser Foundation Research
Institute’s institutional review board.
Patient Selection
Group Assignments
METHODS
Design
The study sample was recruited from the
Kaiser Permanente Northern California
(KPNC) patient population. Inclusion
criteria included at least 2 consecutive
years of Health Plan membership, an established diagnosis of gout (International
Classification of Diseases, Ninth Revision
Code 274.XX), and clear documentation
of at least 2 distinct episodes of acute gouty
arthritis in the preceding 12 months. To be
eligible for randomization, patients between
the ages of 21 and 80 years had either a
most recent sUA level above 7.0 mg/dL
or no measurement of sUA in the past year.
Patients were excluded if they had a current
cancer diagnosis with active treatment, were
believed to be terminally ill (as judged by
the Principal Investigator before randomization), were pregnant or lactating, or had
end-stage renal disease or dementia.
For each patient fulfilling the eligibility
criteria, an e-mail was sent to his/her primary care physician. This e-mail included
a brief description of the trial, including
the expectation that those assigned to
receive “usual care” would be instructed
to continue to manage their gout under
The Permanente Journal/Perm J 2016 Summer;20(3):15-234
Control subjects were asked to complete
baseline, 12-week, and 26-week laboratory
assessments. We defined measurement windows of between 10 weeks and 16 weeks for
the 12-week measurement of sUA in the
control group, and between 24 weeks and
30 weeks for the closeout measurement.
In the intervention group, the clinical
pharmacist, under a protocol approved by
the KPNC East Bay Pharmacy and Therapeutics Committee, was authorized to order relevant laboratory tests and to initiate
or to change orders for the medications
used for ULT and for flare prophylaxis.
In the event of acute flares or abnormal
laboratory results, the pharmacist consulted with the rheumatologist, who could
prescribe treatment or advice if outside the
scope of the pharmacy protocol. The ULT
was either initiated or adjusted if the sUA
level was above 6.0 mg/dL. Prophylaxis
of gout flares was prescribed in all cases
(see next paragraph). Subjects already receiving ULT treatment had their medications titrated but not changed. Subjects
not receiving ULT at the start of the trial
were started on a regimen of allopurinol,
100 mg/day (if the estimated glomerular
filtration rate was less than 30 mL/min,
the starting dose was 50 mg/day), unless there was a known allergy or other
contraindication to allopurinol. After any
change in ULT, subjects were instructed
to return for laboratory assessment (sUA,
alanine aminotransferase, complete blood
cell count, and estimated glomerular filtration rate) in 2 weeks to 3 weeks, and report
any adverse drug reactions or gout flares.
Dose titration was in increments of 100
mg/day. The titration process was continued in an iterative fashion until a target
sUA level was achieved and maintained,
or until the trial ended at 26 weeks. In all
cases, the primary outcome—sUA level at
or below 6.0 mg/dL—was determined by
either a second consecutive target result or
the most recent result at 26 weeks (with a
window of 24 weeks to 30 weeks).
Probenecid and febuxostat were secondline agents and used if allopurinol was not
tolerated. Flare prophylaxis in most cases
consisted of daily oral colchicine or any
nonsteroidal anti-inflammatory drug and
was continued throughout the study in the
intervention group. At the conclusion of
the trial, each subject’s primary physician
was informed whether or not the patient
achieved the target, and the most recent
sUA level. If the patient had achieved the
target, the physician was advised to continue the current medication and dose of
ULT. For patients not at target, the physician was reminded of the target level.
Outcome Variables
The primary outcome was achieving an
sUA level of 6.0 mg/dL or below at the 26week closeout visit. Secondary outcomes
included the absolute change in sUA level
from baseline to 26 weeks and achieving
at least a 2 mg/dL decrease in sUA level at
the closeout visit.
Statistical Analyses
All analyses of continuous variables
were conducted with the Student t-test.
Categorical variables were analyzed with
the Fisher exact test or its generalization
for more than 2 levels.21 Analyses were
conducted and are reported here both
under the principle of intention-to-treat,
with the last value carried forward (the
primary analysis), and as a per-protocol
19
ORIGINAL RESEARCH & CONTRIBUTIONS
A Pharmacist-Staffed, Virtual Gout Management Clinic for Achieving Target Serum Uric Acid Levels: A Randomized Clinical Trial
analysis, including only observed values.
All reported p values were 2-sided with
the experimental error rate set to α =
0.05, and no adjustments were made for
multiple testing. Analyses were performed
with SAS Version 9.3 (SAS Institute, Cary,
NC) and STATA 12 (StataCorp LP, College Station, TX).
RESULTS
Figure 1. Flow diagram of design of Gout Uric Acid ReDuction study.
sUA = serum uric acid level (mg/dL).
Table 1. Baseline demographic and clinical characteristics, overall and by study group
Characteristic
Demographic characteristic
Age (years), mean (SD)
Male sex, no. (%)
Race/ethnicity, no. (%)
Native American
Asian
African American
Pacific Islander
White
Hispanic
Unknown
Clinical characteristic
Hypertension, no. (%)
Chronic kidney disease, no. (%)
Diabetes mellitus, no. (%)
Serum uric acid (mg/dL), mean (SD)
Serum creatinine (mg/dL), mean (SD)
SD = standard deviation.
20
All participants
(N = 77)
Intervention group
(n = 37)
Control group
(n = 40)
59.4 (1.4)
68 (88)
60.9 (2.0)
36 (97)
58.0 (2.0)
32 (80)
1 (1)
9 (12)
12 (16)
17 (22)
23 (30)
14 (18)
1 (1)
1 (3)
7 (19)
5 (14)
7 (19)
9 (24)
7 (19)
1 (3)
0 (0)
2 (5)
7 (18)
10 (25)
14 (35)
7 (18)
0 (0)
49 (64)
23 (30)
19 (25)
8.3 (1.4)
1.2 (0.4)
25 (68)
13 (35)
9 (24)
8.5 (1.5)
1.3 (0.5)
24 (62)
10 (26)
10 (26)
8.2 (1.3)
1.1 (0.3)
The outcomes of the selection, consent,
randomization, and trial progress are
shown in Figure 1. We identified 1860
potentially eligible patients from KPNC
electronic health records. The records were
placed in random order, and charts were
then reviewed for eligibility by a boardcertified rheumatologist (RG) to validate
the inclusion and exclusion criteria. We
screened the charts of the first 749 patients
and identified 329 who were eligible for
inclusion in the study. Of the 418 who
were not eligible, the most common
reasons were insufficient documentation
of at least 2 gout flares in the prior year
(n = 226, 54%), a most recent sUA level
of 7.0 mg/dL or less (n = 93, 22%), and
excluded comorbidities (n = 15, 4%).
Ultimately, 104 patients consented to
participate and were randomly assigned
to receive either active intervention or
usual care. Three patients gave consent
and were randomized but, on baseline
laboratory evaluation, were found to have
sUA levels at or below 6.0 mg/dL. Of the
99 remaining subjects, 51 were randomly
assigned to the intervention group and 48
to the control group. Of these, 12 subjects
never completed the baseline sUA assessment (7 in the treatment group and 5
in the control group). A total of 22 participants dropped out of the study after
obtaining their baseline sUA measurements (8 in the control group and 14 in
the intervention group); all but 1 (whose
insurance lapsed) failed to obtain required
laboratory assessments despite repeated
attempts by the study pharmacist. Of
the 37 participants randomized to the
intervention group, 32 (86%) remained
in the trial at the 12-week time point and
29 (78%) at the 26-week closeout call; the
corresponding lab adherence numbers for
the control group were 36 (90%) of 40
participants at 12 weeks and 35 (88%) at
26 weeks. Table 1 shows the demographic
The Permanente Journal/Perm J 2016 Summer;20(3):15-234
ORIGINAL RESEARCH & CONTRIBUTIONS
A Pharmacist-Staffed, Virtual Gout Management Clinic for Achieving Target Serum Uric Acid Levels: A Randomized Clinical Trial
and baseline information for all subjects
entering the study (n = 77).
Table 2 reports the results of the primary
outcome measure. In the intention-to-treat
analysis using the method of last-valuecarried-forward, 13 (35%) of 37 subjects
in the intervention group (95% confidence
interval [CI] = 20% to 52%). However,
only 5 (13%) of 40 subjects (95% CI =
4% to 27%) in the control group achieved
an sUA level of 6.0 mg/dL or below at 26
weeks (Figure 2; risk ratio [RR] = 2.8,
95% CI = 1.1 to 7.1, p = 0.03). This difference was greater at the 12-week time
point with 15 participants (41%, 95% CI
= 25% to 58%) in the intervention group
and 3 participants (8%, 95% CI = 2% to
20%) in the control group achieving the
targeted study outcome of sUA levels of
6.0 or less (RR = 5.4, 95% CI = 1.7 to
17.2, p = 0.001).
The control group experienced a mean
increase in the sUA level at 26 weeks of
0.1 mg/dL (95% CI = -0.45 to 0.69),
whereas the sUA in the intervention group
decreased by an average of 1.5 mg/dL
(95% CI = -1.0 to -2.0). The intergroup
difference in sUA levels was -1.6 mg/dL
(95% CI = -0.9 to -2.4, p < .001). Results
Figure 2. Comparison of mean serum uric acid during study period. Values shown are at each study time
point, with error bars indicating 95% confidence intervals (intention-to-treat analysis).
were similar, although somewhat more
pronounced, for the less-conservative perprotocol analysis, which did not include
imputed data (Table 2).
Figure 2 shows the mean sUA levels at
baseline, 12 weeks, and 26 weeks for both
groups for the intention-to-treat analysis.
In the control group, there was no significant change in sUA levels at either time
point, whereas the intervention group
had significant reductions of sUA at both
time points.
To elucidate the range of outcomes
among subjects in the control and intervention groups, we plotted the individual
change in sUA levels at week 26 for all
participants completing the protocol
(Figure 3).
DISCUSSION
Our premise for this study was that an
important failure in the management of
chronic gout has been the lack of a systematic approach for identifying inadequately
Table 2. Primary and secondary outcome measures by study group
Intention-to-treat analysis
Intervention group
Control group
(n = 37)
(n = 40)
Outcome
sUA level ≤ 6 mg/dL, no. (%)
12 weeks
15 (41)
26 weeks
13 (35)
sUA level change from baseline (mg/dL), mean ± SE
12 weeks
-1.6 ± 0.2
26 weeks
-1.5 ± 0.3
Decrease in sUA level by ≥ 2 mg/dL, no. (%)
12 weeks
16 (43)
26 weeks
14 (38)
ALT level change from baseline (mg/dL), mean ± SE
12 weeks
8.4 ± 3.1
26 weeks (mg/dL) mean ± SE
8.1 ± 3.9
Creatinine level change from baseline (mg/dL), mean ± SE
12 weeks
0.01 ± 0.02
26 weeks
0.006 ± 0.03
p value
Per-protocol analysis
Intervention group
Control group
(n = 29)a
(n = 35)a
p value
3 (8)
5 (13)
0.001b
0.03d
15 (47)
13 (45)
3 (8)
3 (9)
0.001c
0.001e
0.2 ± 0.2
0.1 ± 0.3
< 0.001
< 0.001
-1.9 ± 0.2
-1.8 ± 0.3
0.3 ± 0.3
0.1 ± 0.3
< 0.001
< 0.001
4 (10)
5 (13)
0.001
0.02
16 (50)
14 (48)
4 (11)
3 (9)
0.001
< 0.001
-2.4 ± 1.5
-1.3 ± 1.8
0.002
0.03
8.6 ± 3.2
6.7 ± 4.8
-2.8 ± 1.7
-0.7 ± 1.9
0.003
0.13
-0.02 ± 0.02
0.005 ± 0.03
0.28
0.99
0.1 ± 0.02
-0.003 ± 0.03
-0.2 ± .02
0.2 ± .02
0.27
0.61
Numbers refer to participants assessed at the 26-week time point. For the 12-week time point, there were 32 evaluable participants in the intervention group and 36 participants in the
control group.
b
RR = 5.4 (95% CI = 1.7 to 17.2).
c
RR = 5.6 (95% CI = 1.8 to 17.7).
d
RR = 2.8 (95% CI = 1.1 to 7.1).
e
RR = 5.2 (95% CI = 1.6 to 16.6).
ALT = alanine aminotransferase; CI = confidence interval; RR = risk ratio; SE = standard error; sUA = serum uric acid.
a
The Permanente Journal/Perm J 2016 Summer;20(3):15-234
21
ORIGINAL RESEARCH & CONTRIBUTIONS
A Pharmacist-Staffed, Virtual Gout Management Clinic for Achieving Target Serum Uric Acid Levels: A Randomized Clinical Trial
Figure 3. Net change in serum uric acid among individual evaluable participants in the intervention and
usual care groups.
treated patients and then to treat and monitor them in a structured, target-driven
way. In our organization, the management
of other chronic diseases has improved
substantially by using such an approach.22
We previously published results of a pilot
program designed to assess the feasibility
of using a pharmacist to manage ULT in
patients with gout under the supervision
of a rheumatologist.20 The outcomes in this
single-cohort study were encouraging, but
it was an uncontrolled study. The present
study, which included a randomized usualcare control group, confirmed that a higher
percentage of patients randomly assigned
to a structured, goal-directed program did
… an important failure in the
management of chronic gout
has been the lack of a systematic
approach for identifying
inadequately treated patients and
then to treat and monitor them in
a structured, target-driven way.
indeed achieve and maintain a target sUA
level at or below 6.0 mg/dL. In addition,
we found a statistically significant greater
mean improvement in sUA level among
patients in the intervention group.
The percentage of subjects in the intervention group who achieved the primary
outcome (35% in the intention-to-treat
22
analysis, 45% in the per-protocol analysis)
was considerably lower than what we were
able to achieve in our pilot program (82%),
but much higher than the percentage seen
in the control group (8%). In our current
trial, the lower rate of success without the
intervention was notable but must be interpreted within the context of the study.
In particular, unlike the pilot program,
the study recruited patients not referred
by their primary physicians, which may
have resulted in a cohort of less-motivated
patients. Although greater in the intervention group, there was also a higher dropout rate compared with that seen in our
pilot program. It is also possible that the
lower success rate was partially caused by
limitations imposed by the study protocol.
Specifically, unlike the present trial, the
pilot study allowed the continuation of
the program beyond 26 weeks if the sUA
target was not maintained for at least 3
months. Because adherence to ULT is
known to be low compared with treatment
of other chronic conditions,23 the successful long-term management of gout must
eventually account for this by building in
a continued monitoring scheme that will
identify nonadherent patients and allow
further intervention. In the current study,
limited to 26 weeks, we were not able to
address this need. Nonetheless, initiating
and adequately titrating pharmacologic
treatment to lower sUA level is a necessary
step toward long-term control, and one
that is achieved in a relatively low percentage of patients with gout in the absence
of a structured program. We believe that
the results in the pilot study may well be a
better reflection of how well our program
would perform outside the constraints of
the study design and length.
Our study had several strengths, including a comparable randomized control
group; a clear, structured intervention
protocol; and objective outcome measurements. However, several limitations should
be noted. First, there was a relatively high
dropout rate from the program (22%),
which was higher in the intervention
group than the control group. This difference did not reach statistical significance, p = 0.232. Despite this difference,
both the per-protocol and intent-to-treat
analyses showed a statistically significant
improvement in attaining the primary
outcome in our intervention group.
Moreover, we were not able to use a control group that strictly reflected usual
care. This is because our primary outcome
measure required that every participant be
tested at least two times for sUA during
the study. Under true “usual care,” it was
unrealistic to expect that all the patients
with gout would have been tested, and
thus we would have been unable to assess
our primary outcome. Indeed, we have
reviewed KPNC data for sUA among
patients with a gout diagnosis and found
that 29% had no sUA level measured
in the 5-year period before their last
encounter for gout (unpublished data).
If anything, we believe this monitoring
requirement may have biased our results
against an intervention effect because the
lack of an sUA measurement during the
study would more likely lead to a lack of
initiation or titration of treatment.
CONCLUSION
The fact that we were able to demonstrate improved outcomes even with a
restrictive and time-limited intervention
suggests that an ongoing monitoring
program integrated within a primary
care-centered medical system could be
highly effective in achieving sustained
reduction of sUA levels in patients with
gout. Moreover, if managed efficiently
by a pharmacist or other physician extender, this approach could result in a
The Permanente Journal/Perm J 2016 Summer;20(3):15-234
ORIGINAL RESEARCH & CONTRIBUTIONS
A Pharmacist-Staffed, Virtual Gout Management Clinic for Achieving Target Serum Uric Acid Levels: A Randomized Clinical Trial
cost-effective program and, over time, in
a large reduction in health care utilization
and cost of caring for patients with gout,
with improved clinical outcomes. v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
Acknowledgments
This trial was registered at www.clinicaltrials.gov
(#NCT01568879). This work was supported
by a Community Benefit Grant from the Kaiser
Foundation Research Institute, Oakland, CA.
Kathleen Louden, ELS, of Louden Health
Communications provided editorial assistance.
How to Cite this Article
Goldfien R, Pressman A, Jacobson A, Ng M,
Avins A. A pharmacist-staffed, virtual gout
management clinic for achieving target serum
uric acid levels: a randomized clinical trial.
Perm J 2016 Summer;20(3):15-234. DOI:
http://dx.doi.org/10.7812/TPP/15-234.
5.
6.
7.
8.
9.
10.
11.
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Favoring Disease
Gout would thus appear at least partly to depend on a loss of power …
of the “uric-acid-exerting function” of the kidneys … . Any undue formation
of this compound would favour the occurrence of the disease; and hence
the connection between gout and uric acid, gravel and calculi ... and the
influence of high living, wine, porter, want of exercise, etc, in inducing it.
— Sir Alfred Baring Garrod, FRS, 1819-1907,
English physician credited with coining the term “rheumatoid arthritis”
The Permanente Journal/Perm J 2016 Summer;20(3):15-234
23
ORIGINAL RESEARCH & CONTRIBUTIONS
Exploring the Reality of Using Patient Experience Data
to Provide Resident Feedback: A Qualitative Study of Attending
Physician Perspectives
Steffanie Campbell, MD; Heather Honoré Goltz, PhD, LMSW, MEd; Sarah Njue, MPH; Bich Ngoc Dang, MD
E-Pub: 07/05/2016 ABSTRACT
Introduction: Little is known about the attitudes of faculty
and residents toward the use of patient experience data as a
tool for providing resident feedback. The purpose of this study
was to explore the attitudes of teaching faculty surrounding
patient experience data and how those attitudes may influence
the feedback given to trainees.
Methods: From July 2013 to August 2013, we conducted
in-depth, face-to-face, semistructured interviews with 9 attending physicians who precept residents in internal medicine at 2
continuity clinics (75% of eligible attendings). Interviews were
coded using conventional content analysis.
Results: Content analysis identified six potential barriers in
using patient experience survey data to provide feedback to residents: 1) perceived inability of residents to learn or to incorporate
feedback, 2) punitive nature of feedback, 3) lack of training in
the delivery of actionable feedback, 4) lack of timeliness in the
delivery of feedback, 5) unclear benefit of patient experience
survey data as a tool for providing resident feedback, and 6) lack
of individualized feedback.
Conclusion: Programs may want to conduct an internal review
on how patient experience data is incorporated into the resident
feedback process and how, if at all, their faculty are trained to
provide such feedback.
INTRODUCTION
Interpersonal and communication skills constitute one of
the Accreditation Council for Graduate Medical Education’s
(ACGME’s) 6 domains of clinical competencies for graduate
medical education in internal medicine. The ACGME supports
the use of patient experience data as an outcomes-based tool for
providing resident feedback on interpersonal and communication
skills.1 The American Board of Internal Medicine is exploring ways
to integrate this outcomes-based approach into their physician
certification activities.2 Patient experience data can serve as an
effective tool for providing residents with feedback. In a study by
Cope and colleagues,3 residents in an internal medicine training
program were randomized to receive a 30-minute structured feedback session in which they received mean scores on an experience
survey filled out by new patients. Residents in the intervention
Perm J 2016 Summer;20(3):15-154
http://dx.doi.org/10.7812/TPP/15-154
arm had a significant increase in mean scores on a subsequent survey of new patients compared with residents who did not receive
feedback. Patient experience data paired with actionable feedback
(ie, feedback that can change residents’ practice behavior) can be
highly effective when provided by trained individuals.4
Although data suggest actionable feedback has a positive impact
on residents’ practice behaviors, many graduate medical education programs have difficulties translating this knowledge into
real-world practice.5-12 Studies evaluating feedback-based interventions typically devote immense resources on the development
and training of personnel to deliver actionable feedback that is
typically neither feasible nor designed for implementation in general practice.13-20 As such, patient experience survey data are rarely
used effectively outside the research context to deliver resident
feedback, owing to lack of either training or time.6,11,12,21 In addition, little is known about the attitudes of faculty and residents
toward the use of patient experience data as a tool for providing
resident feedback.22 The purpose of this study was to explore how
attending physicians in a real-world academic setting incorporate
patient experience survey data into feedback practices, explore the
attitudes and beliefs surrounding the use of patient experience data
as a feedback tool, and identify potential areas for improvement.
Specifically, we were interested in exploring attendings’ attitudes
around giving feedback and understanding the process by which
attendings provide learners with actionable feedback.
METHODS
Participants
The study population was based on a nonrandomized convenience sample of attending physicians who precept residents
in internal medicine at two continuity clinics in Houston, TX
(clinics A and B). Eligibility criteria included 1) faculty with an
appointment in the Department of Internal Medicine and 2)
faculty with a role as a preceptor in the internal medicine resident
continuity clinic. This study was approved by the institutional
review board for our institution.
Data Collection
Participants were recruited by e-mail; attending physicians
received an e-mail from the Associate Program Director of the
Steffanie Campbell, MD, is an Assistant Professor of Medicine and an Associate Director of the Internal Medicine Residency Program
at Baylor College of Medicine in Houston, TX. E-mail: [email protected]. Heather Honoré Goltz, PhD, LMSW, MEd, is an
Assistant Professor at the University of Houston-Downtown and Adjunct Assistant Professor in the Section of Infectious Diseases at Baylor
College of Medicine in Houston, TX. E-mail: [email protected]. Sarah Njue, MPH, is a Research Coordinator in the Section of Infectious
Diseases at Baylor College of Medicine in Houston, TX. E-mail: [email protected]. Bich Ngoc Dang, MD, is an Assistant Professor of
Medicine in the Section of Infectious Diseases at Baylor College of Medicine and an Investigator at the Center for Innovations in Quality,
Effectiveness and Safety at the Michael E DeBakey VA Medical Center in Houston, TX. E-mail: [email protected].
24
The Permanente Journal/Perm J 2016 Summer;20(3):15-154
ORIGINAL RESEARCH & CONTRIBUTIONS
Exploring the Reality of Using Patient Experience Data to Provide Resident Feedback: A Qualitative Study of Attending Physician Perspectives
Internal Medicine Residency Program (SC) inviting them to take
part in the study. The e-mail informed potential participants of the
study and its purpose. Twelve attending physicians met eligibility
criteria and were recruited; 9 attending physicians participated.
Between July and August 2013, SC conducted in-depth, face-toface, semistructured interviews with attending physicians. She
conducted 4 individual interviews at clinic B and a focus group
interview involving 5 participants at clinic A. A focus group
Major Topics and Key Interview Questions
in Study of Resident Feedback
Impressions of patient experience survey
•Tell me about the satisfaction surveysa your patients fill out
on the residents.
•Tell me about how you use patient survey data in comparison to
the other information you use to provide feedback to a resident.
Training in the use of patient experience survey data
•Do you feel comfortable using patient satisfaction survey
data to provide feedback to the residents?
•How were you chosen to provide feedback to the residents?
•What was the time commitment required to learn how to use
patient satisfaction data in order to provide feedback?
•Think about your peers who provide feedback. Why do you
think they were chosen?
Process of feedback
•Context framing statement: Think about the first time you
used patient satisfaction survey data to provide a resident
with feedback.
•What happens during a typical feedback session?
•What parameters do you use to determine whether a feedback session was effective?
•Have you seen or been told by a colleague how they give
feedback?
•Have you received feedback on the process? We are all
[name of academic center] but our residents have continuity
clinics at two different sites. Do you think there is anything
specific to the culture of your location that impacts your
feedback process?
Attitudes/beliefs surrounding feedback
•Overall, how would you describe the interaction between
you and the resident when you use the patient survey data in
a resident feedback session?
•Think about the best feedback session you had where you used
patient satisfaction survey data. Could you describe this to me?
•Think about the worst feedback session you had where you
used patient satisfaction survey data. Could you describe this
to me?
Potential areas for improvement
•Is there anything the residency program can do to make the
feedback sessions based on patient satisfaction survey data
more effective?
•In an ideal situation, what would the process look like?
a
The term “satisfaction survey” was used instead of patient experience in the interview
guide because it was a term faculty were more familiar with.
The Permanente Journal/Perm J 2016 Summer;20(3):15-154
interview was conducted at clinic A per the request of the clinic
director, given the time constraints of the attending staff. Staff
members were willing to complete a group interview during their
lunch hour, but were unable to dedicate an hour individually for
interviews. Participants provided verbal but not written informed
consent to protect their identities. No compensation was provided
for participation. The individual interviews lasted 30 minutes to
60 minutes and the focus group lasted 60 minutes. Interviews were
audiotaped using an encrypted recorder and transcribed verbatim
by professional transcriptionists. The interviews were conducted
using an open-ended interview guide developed by the multidisciplinary team. The interview guide consisted of open-ended
questions to identify the process of feedback, the attitudes and
beliefs surrounding feedback, and the training given to attending physicians to use patient experience survey data in providing
resident feedback (see Sidebar: Major Topics and Key Interview
Questions in Study of Resident Feedback). Interviews took place
in conference rooms at the participants’ respective clinic sites.
Research Team and Reflexivity
The research team’s professional backgrounds and research interests informed development of the interview guide, interpretation of codes, and understanding of emergent themes within the
context of medical education and patient care. Our multidisciplinary team consisted of two physicians, a social work researcher,
and a research coordinator. SC, Associate Program Director of
the Internal Medicine Residency Program, ensures quality education and training for residents. BND is an Assistant Professor
of Medicine in the Section of Infectious Diseases. Her research
examines the use of patient experience metrics as a modifiable
focus for improving retention in care and adherence to medicines.
HHG, Assistant Professor in Social Work, is experienced in qualitative research methods; she is interested in patients’ access to and
quality of care. SN is a master’s-trained public health professional
with a background in health promotion and behavioral science.
Data Analysis
We did not use an a priori code list. Four researchers (SC,
HHG, SN, and BND) independently reviewed the transcripts
and coded the data, looking for examples of facilitators and barriers to actionable feedback. The full research team then came
together to compare codes and iteratively revise and refine codes
until 100% consensus was reached. This occurred during several
weekly team meetings. In the later stages of analysis, the team
examined recurrent themes across interviews and clinic sites.
RESULTS
Characteristics of Participants
The participation rate among eligible attending physicians was
75% (9/12). Nonparticipating physicians reported demanding
clinical duties and the lack of time as reasons for opting out.
Baseline characteristics are outlined in Table 1. Given the small
sample size, limited demographic characteristics are reported to
preserve confidentiality. Five were female and 4 reported their
race/ethnicity as Asian. Five participants precept residents at
clinic A and 4 at clinic B.
25
ORIGINAL RESEARCH & CONTRIBUTIONS
Exploring the Reality of Using Patient Experience Data to Provide Resident Feedback: A Qualitative Study of Attending Physician Perspectives
Barriers to Actionable Feedback
Table 1. Participant characteristics (N = 9)
Characteristic
Sex
Men
Women
Age, mean (± SD)
Race
Asian
Black or African American
White
Faculty facilitator experience, mean years
Location
Clinic A
Clinic B
no. (%)
a
4 (44)
5 (55)
47 (± 10.2)
4 (44)
3 (33)
2 (22)
9.7
5 (55)
4 (44)
Data are no. (%) except where indicated.
SD = standard deviation.
a
Description of Clinic, Patient Panel Assignment,
and Patient Experience Survey
Each clinic has a unique structure for assignment of a primary
care physician. Clinic A assigns patients to a staff physician as
their primary care physician. Residents are assigned to a specific
attending who then designates the resident as an associate physician for 75 to 90 of their patients. Attempts are made to schedule
follow-up appointments during the time the resident is present
to create continuity of care between residents and their patients.
At clinic B, patients are assigned a resident physician as their
primary care physician. All follow-up appointments are made on
the half-day the resident physicians are available to assure continuity of care. Resident physicians then discuss care plans with
the staff physician available during that half-day. A 9-item survey
adapted from resident evaluation tools, including those originating from Saint Mary’s Hospital and Maine Medical Center, is used
to measure patients’ experience with residents during a specific
encounter (see Sidebar: Patient Experience Survey Questions).23
These items reflect interpersonal and communication skills valued
as important on the basis of the program’s educational objectives
and the extant literature. Responses are kept anonymous and filed
under the resident’s name.
Patient Experience Survey Questions
1. Overall, I was satisfied with this visit
2. During this visit, my doctor treated me with respect
3. My doctor answered my medical questions
4. My doctor used terms I understood
5. My doctor involved me in making decisions about my care
6. I felt my doctor listened to my concerns
7. I felt my doctor spent enough time with me
8. I would recommend this doctor to a friend
9. I was seen by the doctor in a timely fashion
For each questions, patients were asked to choose: Strongly
disagree, Disagree, Neither disagree nor agree, Agree, Strongly
Agree, or Unsure.
26
Specific patterns of feedback varied by clinic site; however,
some core themes did emerge from the data. The research team
identified six themes corresponding to potential barriers in using
patient experience survey data to provide actionable feedback to
residents: 1) perceived inability of residents to learn or incorporate feedback, 2) punitive nature of feedback, 3) lack of training
in the use of patient-experience data to give feedback, 4) lack of
timeliness in providing feedback, 5) unclear benefit of patient
experience data as a tool to inform and frame actionable feedback,
and 6) lack of individualized feedback.
Perceived Inability of Residents to Learn or Incorporate Feedback
On occasion, attending physicians seemed resigned to the belief
that it is difficult to change residents’ practice behavior. They cited
difficulties in teaching adult learners and difficulties in teaching
“soft skills” (eg, personal attributes). Three attending physicians
specifically reported difficulty in teaching “professionalism.”
“It’s hard to change behavior for adults … . Just because they’re trainees, we should not forget the fact that they are adults and they’re supposed to be professionals, you know, so there’s only so much I can do …”
“But you can’t change personalities and habits of people [who are]
old. You can do your best, but professionalism is a very difficult thing
to teach, and it’s professionalism in not just how you look or how
you show up, but it’s also the amount of effort you put forth in what
your actual duties are, you know, and how much you can relate and
communicate to the patient. So it’s hard to teach soft skills. You can
do your best with a resident that you might have for three years, but
some personalities don’t change.”
—Attending physicians at clinics A and B
Punitive Nature of Feedback
Punitive feedback refers to any negative approach to providing
feedback. Three of four participants at clinic B reported that they
approached underperforming residents in a nonpunitive way to
address patient concerns or improve their clinical competence.
These attending physicians engaged the resident in coming up
with task-specific and actionable solutions.
“I talked to the resident about what she thought had happened,
… and then we kind of brainstormed kind of what we thought had
gone wrong between that. And she asked me was there anything I
thought uh could be done better in the- the situation, um and then
we kind of wrote back to the patient what had happened, which I
think was just a miscommunication thing.”
“So I learned that we have to be sensitive but at the same time
we have to get to the point because if you’re too sensitive you’re being
too nice. And if they don’t get the message then you’re not getting to
the feedback.”
—Attending physicians at clinic B
In contrast, attendings at clinic A reported using punitive
feedback in response to the residents’ actions, such as removing
patients from the residents’ panel.
“So that is why they [the patients] don’t want to write bad things,
but they will come and talk to us in person; especially because many
of them, if you’ve been seeing them for several years, they do understand that these people are in training, which is okay to some extent.
And some say, ‘No, I don’t want to see a resident; I want to see the
attending.’ Then we just change the patient back to us [attendings].”
The Permanente Journal/Perm J 2016 Summer;20(3):15-154
ORIGINAL RESEARCH & CONTRIBUTIONS
Exploring the Reality of Using Patient Experience Data to Provide Resident Feedback: A Qualitative Study of Attending Physician Perspectives
“But some of my patients I have actually removed from his panel
and either brought them back to me or put them with another person
that I know is better at listening and communication.”
“But it’s important for the resident that he at least gets a feel that
we are watching them and patients do have their opinions.”
—Attending physicians at clinic A
Lack of Training in the Use of Patient Experience Data
to Give Feedback
Participants were asked if they received specific training in using patient experience survey data to provide actionable feedback.
Two of the five participants at clinic A reported taking a threehour institutional workshop two years prior. Per their report, the
workshop explained how to provide feedback to residents, but
not specifically how to incorporate patient experience data into
feedback practices.
“There’s a course at [my institution] about how to evaluate residents
and other groups … . The one that we specifically had taken was how
to complete evaluations.”
—Attending physician at clinic A
However, three of the four participants at clinic B reported no
formal training in these areas.
“No, I mean, no formal training to start off with, except I meanI mean, we had, you know, teaching as residents and a lot of teaching
built into our primary care residency.”
—Attending physician at clinic B
Lack of Timeliness in Providing Feedback
Lack of timeliness refers to delays in providing feedback to the
residents. Branch and Paranjas24 suggest residents should receive
feedback at least every two to three months. In our analysis, two
attending physicians at clinic B reported completing evaluations
twice a year; they reported time constraints as a barrier to timely
feedback.
“It’s time consuming because I have 28 residents.”
“We just do it electronically so we don’t actually have that feedback like oral feedback session because they come at different times.”
—Attending physicians at clinic B
“I’d rather not deal with it than deal with that because then you’re
sending more work for me … . Every year, every year now, I have
one that is wasting my time.”
—Attending physician at clinic A
Unclear Benefit of Patient Experience Data as a Tool
to Inform and Frame Actionable Feedback
Benefit refers to the degree with which the attending physicians consider patient experience survey data as a beneficial
tool for providing actionable feedback. Only one of five participants at clinic B reported that the surveys were a suitable
tool for providing feedback to the residents. However, of the
nine participants overall, eight questioned the value of patient
experience survey data in providing resident feedback. These
attendings reported that the surveys were not beneficial; they
felt that the information obtained from the surveys was insufficient to address patient issues or give effective feedback
to the residents.
“I don’t see that they are a big help to the resident, nor to me, unless
the patient very specifically writes something, you know, out of the
ordinary that the resident did, whether it be egregious or something
The Permanente Journal/Perm J 2016 Summer;20(3):15-154
positive. Short of that, I don’t see that they are very helpful evaluations to me or the resident, in their current state.”
“Yeah, because I’m not getting that much useful information except uh “wonderful doctor,” “the best,”… but no really constructive
feedback … . We [are] doing it [patient experience surveys] just to
meet this [Accreditation Council for Graduate Medical Education]
requirement but yet they’re not learning … . There’s no feedback and
they’re not learning what they should do to improve themselves. There’s
no purpose of doing the evaluation … . So it’s a little more difficult
and there’s no details on those and so it’s a little harder to give feedback
… . I don’t see any comments … at all so it’s hard to give the feedback.”
“I don’t think the residents care too much. They get evaluated so
many ways and so many times a year.”
—Attending physicians at clinics A and B
Most attendings did not like the survey format. They preferred
open-ended questions where patients could provide specific examples and task-specific feedback.
Lack of Resident-Centered Feedback
Resident-centered feedback is feedback that engages the
resident in discussion and allows for shared goal setting.4 One
participant in clinic B reported delivering feedback by having a
face-to-face conversation. In contrast, the other three participants
in clinic B reported providing feedback electronically; they cited
lack of time and the high number of assigned residents as barriers
to resident-centered feedback.
“Unfortunately we don’t sit down … We don’t sit down with any
one of them except the ones who actually um have difficulty. Then
we meet, we talk to that person personally, but other than that we
just do it electronically so we don’t actually have that feedback-like
oral feedback session.”
—Attending physician at clinic B
“I mean, ideally, yes, it would be lovely to have them come, sit,
go through everything, see how you’re doing, whatever, but there’s so
many of them.”
—Attending physician at clinic B
These attendings acknowledge that use of an electronic medium
alone can create a barrier to resident-centered feedback because it
does not provide an opportunity for the resident to reflect, comment, or engage in the solution-making process.
DISCUSSION
This study provides insight into how attending physicians use
patient-reported experience measures to provide feedback for
residents in an internal medicine training program. We identified
six core themes influencing the use of patient experience data in
providing resident feedback: 1) perceived inability of residents to
learn or to incorporate feedback, 2) punitive nature of feedback,
3) lack of training in the delivery of actionable feedback, 4) lack
of timeliness in the delivery of feedback, 5) unclear benefit of
patient experience survey data as a tool for providing resident
feedback, and 6) lack of individualized feedback. In 2001, the
Institute of Medicine codified patient-centeredness as one of six
health care quality aims.25 Patient experience is a critical facet of
patient-centeredness. Moreover, studies have linked better patient
experiences to favorable health behaviors and outcomes.26-39 In
alignment with this aim, the Institute of Medicine advocates
27
ORIGINAL RESEARCH & CONTRIBUTIONS
Exploring the Reality of Using Patient Experience Data to Provide Resident Feedback: A Qualitative Study of Attending Physician Perspectives
Steps to Using Patient Experience Data to
Provide Residents with Actionable Feedback
1. Generate a feedback sheet for each resident, comparing
the individual scores with the scores for the entire group of
residents; see example in Table 2 (individualized).
2. Provide an in-depth feedback session with the resident; use
the feedback sheet to tailor feedback on the basis of areas
where the resident scored low compared to his/her peers.
3. Have the resident comment on his/her scores (residentcentered).
4. Collaboratively discuss different solutions for improving
areas with low scores (nonpunitive).
5. Have the resident set specific goals and solutions to improve
low-scoring areas.
6. Follow-up to determine if the resident has made progress in
achieving his/her goals.
the use of patient experience data as a patient-centered tool for
promoting quality care. Concrete patient experience data can
define key points of intervention for improving the care experience. These data argue for greater training on the use of patient
experience survey data to effect practice change and ultimately to
improve health behaviors and outcomes. Physicians in training
are an ideal population to intervene because they are at an early
stage in their career and may be more malleable.8,40-43 Thus, actionable feedback may have a greater effect on practice behaviors.
Implementation science dictates that a tool or system must
be accepted by the stakeholders for it to be successful.44 Low acceptability of patient experience data was noted in our study and
previously at other institutions.45 Thus, methods for increasing
attending buy-in on the merits of patient experience measures
as tools to inform actionable feedback need to be explored. Increased buy-in could be achieved by involving attending physicians in the implementation process. For example, participants
in our study suggested including open-ended questions and
comment areas to elicit more detailed patient experience data.
Previous studies suggest that medical education programs can
benefit from more intense support and from training on how to
interpret patient experience survey data and to deliver actionable
feedback.46,47 One potential method for incorporating patient
experience data into actionable feedback for the resident is the
use of a framework grounded in feedback-intervention theory.
Feedback should be individualized, and recommendations
should be solutions oriented (ie, task-specific and actionable).
The highest, most effective form of feedback de-emphasizes
hierarchy and embraces a supportive dialogue between the attending and resident. Beyond identifying competency gaps, it
requires the attending to understand the resident as a learner
(ie, understand the resident’s motivations and goal orientation).
The attending can then leverage this knowledge to engage and
motivate the resident to reflect on his/her performance, and to
set goals and develop an action plan to achieve those goals. To
close the feedback loop, the attending should follow-up to determine if the resident has made progress in achieving goals.48,49
The Sidebar: Steps to Using Patient Experience Data to Provide
Residents with Actionable Feedback details the steps to using
patient experience data to provide residents with actionable
feedback. These steps use an individualized, resident-centered,
and nonpunitive approach to providing feedback. A feedback
sheet (Table 2) provides the resident’s average score on each item
of a patient experience survey, and compares those scores with
a group of peers. Items where residents score below a certain
Feedback should be individualized, and
recommendations should be solutions oriented … The
highest, most effective form of feedback de-emphasizes
hierarchy and embraces a supportive dialogue between
the attending and resident. … it requires the attending
to understand the resident as a learner …
cut-off point (eg, the lowest quartile) can identify critical areas
where residents can improve. A plan to improve the identified
areas, in the context of specific goals, should be formulated.
For example, if “listening” is identified as an area of weakness,
specific goals may be 1) using more eye contact during the visit,
and 2) making reflective statements to summarize what the patient has said.50 By using this or other identified tools, one can
create a robust and effective feedback process.
Table 2. Sample feedback table providing performance data on the patient experience survey in comparison to peers1
Component experience
Shared decision making
1. Offer choices in your medical care
2. Discuss the pros and cons of each choice with you
3. Get you to state which option or choice you prefer
4. Take your preferences into account when making
treatment decisions
Scalea
Individual
Mean
SD
Mean
SD
Total (n = X)
25thb
50thb
75thb
1-5
1-5
1-5
1-5
1 = none of the time; 2 = a little of the time; 3 = some of the time; 4 = most of the time; 5 = all of the time.
percentile.
1
Cope DW, Linn LS, Leake BD, Barrett PA. Modification of residents’ behavior by preceptor feedback of patient satisfaction. J Gen Intern Med 1986 Nov-Dec;1(6):394-8. DOI:
http://dx.doi.org/10.1007/BF02596425.
SD = standard deviation. High SD indicates greater variability in patient responses (ie, responses vary a lot across patients)
a
b
28
The Permanente Journal/Perm J 2016 Summer;20(3):15-154
ORIGINAL RESEARCH & CONTRIBUTIONS
Exploring the Reality of Using Patient Experience Data to Provide Resident Feedback: A Qualitative Study of Attending Physician Perspectives
An important strength of our study is that we are one of the
first to explore how patient experience data is incorporated into
the resident feedback process. We identified six core themes that
residency programs can use in assessing and modifying their own
resident feedback process. On the basis of our findings, we believe
that patient experience data can be successfully used to augment
existing evaluation processes.
Limitations
The findings in our study should be interpreted with the following limitations in mind. Although our sample size is small, our
participation rate of 75% is acceptable for exploratory analyses.
In a qualitative study using 60 interviews, core themes were present as early as 6 interviews and data saturation was reached at 12
interviews.51 Although we collected data at 2 very different institutions, these institutions are affiliated with the same academic
center. Our findings may not be generalizable. We were forced to
use mixed methods by combining data from individual interviews
and focus groups. In a focus group there is the concern that 1
or 2 individuals can dominate the conversation. However, there
is also the opportunity for individuals to motivate each other to
express their thoughts. It has been noted that integration of these
2 study methods may provide data enrichment.52
CONCLUSION
Graduate Medical Education programs may want to conduct
their own internal assessment of the resident feedback process.
Such assessments should review how patient experience data is
incorporated into the resident feedback process and how, if at
all, their faculty are trained to provide such feedback. We believe
there is value in adhering to the ACGME guidelines in both spirit
and content so that residents emerge from training with greater
competency in interpreting and using patient experience data to
improve their interpersonal and communication behaviors. v
Disclosure Statement
This work was supported in part by the facilities and resources of the Center
for Innovations in Quality, Effectiveness and Safety at the Michael E DeBakey
VA Medical Center (#CIN 13-413), and the facilities and resources of Harris
Health System. The views expressed in this article are those of the authors and
do not necessarily represent the views of the Department of Veterans Affairs.
The author(s) have no other conflicts of interest to disclose.
Acknowledgments
We thank Aanand D Naik, MD, and Sylvia J Hysong, PhD, for their critical
review of an earlier draft of this manuscript.
Mary Corrado, ELS, provided editorial assistance.
How to Cite this Article
Campbell S, Goltz HH, Njue S, Dang BN. Exploring the reality of using patient
experience data to provide resident feedback: A qualitative study of attending
physician perspectives. Perm J 2016 Summer;20(3):15-154. DOI: http://dx.doi.
org/10.7812/TPP/15-154.
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Compassion
The greatest single quality which the intern should develop is
that of compassion for the sick, the afflicted and the suffering. …
No single attribute of medical practice is more demanding, more
difficult to acquire and more exacting to maintain than the
bond which exists between the patient and the doctor.
— The Internship. Roscoe L Pullen. Springfield, IL: Charles C Thomas; 1952
30
The Permanente Journal/Perm J 2016 Summer;20(3):15-154
ORIGINAL RESEARCH & CONTRIBUTIONS
Physicians Experiencing Intense Emotions
While Seeing Their Patients: What Happens?
Joana Vilela da Silva, MD; Irene Carvalho, PhD
Perm J 2016 Summer;20(3):15-229
E-pub: 07/29/2016
http://dx.doi.org/10.7812/TPP/15-229
ABSTRACT
Objectives: Physicians often deal with emotions arising
from both patients and themselves; however, management of
intense emotions when they arise in the presence of patients is
overlooked in research. The aim of this study is to inspect physicians’ intense emotions in this context, how these emotions are
displayed, coping strategies used, adjustment behaviors, and
the impact of the emotional reactions on the physician-patient
relationship.
Methods: A total of 127 physicians completed a self-report
survey, built from a literature review. Participants were recruited
in 3 different ways: through a snowball sampling procedure, via
institutional e-mails, and in person during service meetings.
Results: Fifty-two physicians (43.0%) reported experiencing
intense emotions frequently. Although most physicians (88.6%)
tried to control their reactions, several reported not controlling
themselves. Coping strategies to deal with the emotion at the
moment included behavioral and cognitive approaches. Only
the type of reaction (but not the emotion’s valence, duration,
relative control, or coping strategies used) seemed to affect the
physician-patient relationship. Choking-up/crying, touching,
smiling, and providing support were significantly associated
with an immediate positive impact. Withdrawing from the situation, imposing, and defending oneself were associated with a
negative impact. Some reactions also had an extended impact
into future interactions.
Conclusion: Experiencing intense emotions in the presence
of patients was frequent among physicians, and the type of reaction affected the clinical relationship. Because many physicians
reported experiencing long-lasting emotions, these may have
important clinical implications for patients visiting physicians
while these emotions last. Further studies are needed to clarify
these results.
INTRODUCTION
Emotions play a significant role in human interactions, yielding communicative intentions, modeling behavior, promoting
attachment, influencing information processing, and even determining choices.1,2 Physicians’ emotions in professional settings,
traditionally considered to be unprofessional and a taboo, have
increasingly been addressed in medical education as a result of the
recognition that physicians often deal with emotions arising from
both the patient and themselves.3,4 Even if feelings of moderate
intensity are manageable or unnoticeable in medical encounters,
physicians’ intense emotions constitute particular challenges
that are more difficult to ignore and possibly to manage at the
moment. The way physicians react and manage these emotions
can affect both the physician and the patient1,4 and shape the
clinical relationship in fundamental ways. What happens when
physicians experience strong emotions in the presence of their
patients? Although numerous studies have focused on patients’
emotions and on how physicians deal with them,5,6 physicians’
own emotions arising when they are seeing their patients have
received less attention.
Research on physicians’ emotions highlights the importance
of physicians’ awareness of their emotional states during the
medical encounter. Unrecognized emotions may impede the
use of patient-centered skills and may be associated with harmful behaviors, such as inappropriately interrupting the patient,
changing the subject, avoiding patients’ psychological issues,
avoiding bonding with patients to prevent suffering, avoiding
conducting certain medical procedures again, or avoiding patients altogether.7-10 One study showed that physicians themselves perceive their emotional states as influencing medical
acts such as prescribing, talking to patients, and referring.11 In
addition, lack of recognition of one’s emotions and low-level
choices, more than clinical knowledge or medical skills, have
been proposed to be associated with medical error.7,8 Along with
the effects of emotional unawareness on patient care, research
has also examined the impact of physicians’ emotions on their
own well-being. Unexplored feelings may be associated with distress, poor judgment, loss of privileges, social isolation, increased
workload, risk of litigation, burnout, reduced work satisfaction,
and an increase in alcohol and other substance use.12-16
This research is informative of important systematic and lasting
effects of emotions experienced by physicians after the encounter
with patients. However, it does not address how physicians manage their intense emotions when these arise in the presence of their
patients. How these emotions are displayed to the patient and
their impact on the relationship are overlooked. Most previous
studies that focus on physicians’ emotions deal with the extreme
contexts of dying patients, medical errors, safety-related events,
and treatment complications.17-20 Emotions in these contexts
include hurt feelings, anger, frustration, remorse, sadness, guilt,
and unhappiness,21 and disturbing emotions can last for years.19
Coping strategies used in these contexts include obtaining emotional support from others, trying to have a positive perspective
over the situation, getting back to work to clear the mind,22 talking
Joana Vilela da Silva, MD, is an Intern Physician of Otorhinolaryngology Head and Neck Surgery in Vila Nova de
Gaia/Espinho Hospital Center, Portugal. E-mail: [email protected]. Irene Carvalho, PhD, is a Professor of
Clinical Neurosciences and Mental Health at Oporto University in Portugal. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-229
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ORIGINAL RESEARCH & CONTRIBUTIONS
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to other physicians or family members, doing physical exercise,20
doing nothing, and talking to the patient.21
However, these situations are limited to a few extreme scenarios
associated with negative emotions (one study did identify positive
daily emotions, including gratitude, happiness, compassion, pride,
and relief, but these emerged among medical trainees and were
associated with connecting with patients and with colleagues, receiving recognition for one’s work, learning, being part of modern
medicine, and receiving emotional support).23 Intense emotions
during interactions with patients in less extreme scenarios may
present a bigger challenge for physicians. They may impair an
ongoing clinical interaction, lessen empathy, or jeopardize the
physician-patient relationship. Physicians must make decisions
while experiencing powerful feelings, and they need to manage
these emotions in front of their patients. The aim of this study is
to explore intense emotions physicians experience in their daily
practice while with patients, how these emotions are displayed
to the patients, the strategies used to manage these emotions at
that moment, and the impact the emotional reactions have on
the physician-patient relationship.
METHODS
Procedures
In this cross-sectional, retrospective study, participants were recruited through 1) a snowball sampling procedure, 2) institutional
e-mails (from the School of Medicine of Oporto University, the
Portuguese League against Cancer, and the Oporto Health Campus
Ministry), and 3) in-person contact during service meetings at the
major central hospital in Oporto and in several primary care centers
in that geographic area. Data were collected between June 2012
and February 2013. Physicians were informed about the aim of the
study, as well as the confidential, anonymous, and voluntary nature
of their participation. Agreement to participate served as informed
consent. The hospital ethics committee approved the study.
Instrument
A questionnaire on physicians’ emotional experiences was developed for this study after a literature review. The Geneva Appraisal
Questionnaire24 assesses individual appraisal processes in the case
of an emotional episode and was close to the goals of this study.
Several items from its version 3 were translated and used in their
original form or in a modified version. Three additional items
were included in the questionnaire to address specific issues in
this study (eg, strategies used to control the emotional expression).
The questionnaire was then applied to a sample of physicians
and medical students who were not participating in the study
to check for meaning, accuracy, and completeness. Ambiguous/
incomplete items were modified, and the survey was again tested
with a different sample of physicians and medical students. This
procedure was repeated until the final version of the survey was
approved. The final 21-item version combines open-ended and
multiple-choice questions (presenting either 4, 5, or 6 options,
plus an additional option that can be either “I don’t know” or
“other—specify”).
The questionnaire starts with the following instruction: “In
this questionnaire, we ask you to recall moments [in your clinical
32
life] when you experienced an intense emotion, either positive or
negative. The events might have been brought about by you, [by a
patient], by someone else, or by [other] causes.” Next, physicians
were asked to recall and briefly describe a situation of their daily
clinical practice in which they experienced an intense emotion
while they were seeing their patients; to name the emotion experienced; to indicate how long ago they experienced the emotion,
how long the emotion lasted, where it took place, and the attitude they had at that moment (options ranging from complete
control of the emotion to uncontrolled emotional reaction); to
describe the actual reaction (if they had one); to indicate what
they did after realizing they reacted openly (eg, returned to their
previous posture, apologized); to describe the strategies used to
control the emotion; and to describe how the emotional reaction
affected their relationship with the patient at that moment and
in future encounters. Two final questions were added for a better
understanding of the occurrence of strong emotional experiences
Table 1. Sample characteristics of physician survey
respondents
Respondent characteristics (N = 124)
Age (years), mean (SD; range)
Professional experience (years), mean (SD; range)
Sex (n = 122)
Women
Men
Professional level (n = 121)
Attending
Resident
Currently practicing
Geographic work location (n = 123)
Urban
Nonurban
Northern country
South (Madeira Island)
Medical specialty (n = 119)
General practice
Internal medicine
Ophthalmology
Psychiatry
Infectious diseases
Nephrology
Legal medicine
Endocrinology
Cardiology
Pediatrics
Neurology
Gynecology
Pathology
General surgery
Pulmonology
N/A (1st-year interns)
Valuea
37.8 (12.8; 25-66)
12.0 (12.3; < 1-40)
75 (61.5)
47 (38.5)
56 (46.3)
65 (53.7)
124 (100)
115 (93.5)
8 (6.5)
118 (95.9)
5 (4.1)
46 (38.7)
13 (10.9)
11 (9.2)
6 (5.0)
5 (4.2)
5 (4.2)
4 (3.4)
4 (3.4)
3 (2.5)
3 (2.5)
2 (1.7)
2 (1.7)
2 (1.7)
1 (0.8)
1 (0.8)
11 (9.2)
Data are no. (%) of physician survey respondents unless otherwise indicated.
SD = standard deviation.
a
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Physicians Experiencing Intense Emotions While Seeing Their Patients: What Happens?
in clinical practice throughout physicians’ careers: to indicate (as
many as applicable) intense emotions experienced when seeing
patients in situations other than the one already described (the
list included 24 emotional reactions; eg, deep sadness, depression,
enthusiasm, intense fear, total relief, intense joy, and deep shock);
and to indicate how frequently intense emotions were experienced
in the presence of patients. Participants additionally answered
questions on demographic and professional characteristics (eg,
sex, birth date, level of medical training, medical specialty, years
of medical experience, and current professional status, whether
practicing or not).
Participants
A total of 127 participants completed the questionnaire. Three
were excluded (2 men who reported never experiencing intense
emotions while interacting with patients and 1 woman who described a situation outside of the study’s goals). The final sample
(depicted in Table 1) comprised 124 actively practicing physicians
working mostly in the north of the country (95.9%) and in urban
areas (93.5%). Because of missing values and nonapplicability
of some items to subgroups of respondents, the total number of
participants included in each analysis varied between 53 and 124.
Analyses
A content analysis was applied to the description of the episode,
with both authors independently coding the situations. Observations were compared, with Cohen’s K = 1 in 12 categories, plus
K = 0.91, K = 0.92, and K = 0.96 in the 3 remaining categories,
respectively. The shorter-answer, open-ended questions were
also independently coded, with final categories reached through
Table 2. Fifteen types of situations eliciting intense emotions in daily practice from 122 physician survey respondentsa
Categories of situations
Health deterioration/death
n (%)
35 (28.7)
Physical or psychosocial suffering
14 (11.5)
End-of-life patients
13 (10.7)
Aggressive patients
11 (9.0)
Communicating bad news
Solving the patient’s problem
11 (9.0)
8 (6.6)
Patients’ rudeness
Unexpected disabling condition
7 (5.7)
7 (5.7)
Accusations of malpractice
7 (5.7)
Disagreeing about the proposed
treatment
Patient telling disturbing information
Making harmful decisions
4 (3.3)
Stress at work
Demanding patients
1 (0.8)
1 (0.8)
Patients’ gratitude
1 (0.8)
1 (0.8)
1 (0.8)
Indicators
I watched a patient die before the medical team’s powerlessness and anguish. The patient was conscious
and we could tell by his facial expression that he could understand what was going on. He tried to tell us
something but it was not perceptible.
I followed-up with a patient in the intensive care unit. She was young and suffered from severe systemic
lupus. She had a tracheostomy and was ventilated but conscious. In one of the medical visits she asked
me for a paper and wrote, “Help me.” She was in very bad shape and eventually died.
She was a terminal patient receiving comfort measures in the intensive care unit. For four years I could
never get her to accept her illness and start treatment. I felt frustrated watching her die and could not do
anything. Then, she grabbed my hand and looked at me in a way I will never forget, and smiled. I felt that
her look meant, “It was my fault, you did everything you could. I am in peace.”
During a consultation a patient pointed a gun at himself.
In the ER the family of a patient invaded my office and threatened me because I was taking too long to
see her .… I felt very vulnerable around them all. They were threatening to destroy everything, using
inappropriate language, hitting the wall, and dropping material that was over the desk.
Having to tell a young patient that her husband and children died.
The first time I alone diagnosed and successfully treated a patient in the ER.
A patient who was amazed about the surgery that restored his sight.
While I was with a patient, his wife spent the entire time reading the newspaper. I felt disrespected.
A young patient entered the emergency room in cardiac arrest. She was alone at that moment without
any family members who could provide any information. After two cycles of advanced life support, she
recovered. When we could collect a clinical history, we found out that she had terminal brain cancer.
During a consultation, a patient confronted me with the desire to have a routine examination check for
everything, and about my obligation to do it. He said, “I have paid taxes for many years and now I have
the right to have the exams I want. Nowadays, doctors study medicine for money. In the old days, we had
good doctors that did the exams we wanted.”
A family member of a patient I had seen the day before came to tell me that the patient died on her way
home. He criticized me for not sending her to the emergency room instead.
The team told a patient’s family that he would die and that the situation was inevitable. I believed that a
bigger effort on our part could still save him.
I felt repulsed after a patient mentioned that during an impulsive episode she killed her pets.
A patient asked me for a compulsory detention of her mother, who took care of a bedridden brother. This
brother would be abandoned for lack of social and family support.
Stress in the operating room.
Following-up a patient with a personality disorder. She questioned every medical intervention, saying
nothing was working. She had multiple complaints and was very demanding. Dealing with her husband’s
pressure (“You have to make her better”).
A patient’s widow offered me a reminder of her husband, who had died three months earlier. I never met
him, only supervised some aspects for his well-being during his palliative phase.
In this particular question only 122 physicians answered; 2 participants reported the emotion but not the situation that elicited it.
ER = emergency room.
a
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consensus. Chi-squared tests and independent-sample t-tests were
conducted in PASW, version 20 (IBM, Armonk, NY).
RESULTS
Physicians indicated experiencing many and varied strong emotions in the presence of their patients throughout their careers
(median = 6.00; interquartile range = 4; range, 1-16 emotions
per physician). The emotional spectrum includes both positive
and negative feelings, and though most emotions in the list we
provided were negative, several positive emotions appeared at the
top of the list as frequently experienced (enthusiasm was the most
signaled emotion in the list). Forty-eight participants (39.7% of
the 121 who answered this question) reported experiencing strong
emotions only a few times per year while interacting with patients.
But 18 (14.9%) mentioned monthly occurrences, and 34 (28.1%)
reported weekly and daily experiences of intense emotions in the
presence of patients. Frequency was independent from physicians’ gender and geographic work location. However, physicians
reporting frequent strong emotions had fewer years of medical
practice (mean ± standard deviation [SD], 8.40 ± 11.03) than
those reporting more sporadic experiences of strong emotional
reactions (mean ± SD, 15.43 ± 12.73), t(109) = 3.12, p = 0.002.
Regarding the specific emotional event described in the questionnaire, most physicians reported situations that occurred long
ago: years ago in 48 cases (38.7%) and months or weeks ago in
59 cases (47.6%) of all 124 physicians. Only 17 (13.7%) recalled an event that occurred days or hours ago. These situations
included several extreme events (the most frequently mentioned
was, “Dealing with patients’ health deterioration or death”), but
also less extreme scenarios (eg, “A patient did not want to greet
me with a handshake”). Additionally, some situations were positive experiences (“A patient was amazed about the surgery that
restored his sight”; Table 2).
Physicians’ emotions associated with these situations are depicted in Table 3 according to their positive, negative, or mixed
(comprising compassion and surprise) valence. Mostly, physicians
reported negative emotions (139 instances, or 85.8% of all 162
reported emotions). For 47 participants (39.8% of the 118 who
answered this question), these emotions lasted longer than a few
minutes or hours: more than 1 day for 34 physicians (28.8%)
and more than 1 week for 13 participants (11.0%), and 2 participants offered that the emotion is still retrieved upon recalling
the situation.
Most physicians (109 of the 123 who answered this question
[88.6%]) at least tried to control their emotions, and 33 (26.8%)
reported they completely controlled themselves. Only 14 participants (11.4%) reported they did not control their emotional
reaction. Only participants experiencing negative emotions
reported controlling them completely in the presence of their
patients (χ2(1) = 9.379, p = 0.001). The difference from physicians experiencing positive and mixed emotions was statistically
significant (χ2(1) = 9.379, p = 0.001), though some of the latter
also attempted to control themselves.
Table 4 depicts physicians’ actual reactions. Physicians were
more likely to touch the patient when experiencing positive emotions than when experiencing negative emotions (χ2(1) = 6.563,
34
p = 0.022), and only smiled when experiencing positive emotions
(χ2(1) = 39.375, p < 0.001). All other reactions occurred only
during negative and mixed emotional experiences.
Several participants who reported not completely controlling their emotional reactions adjusted their behaviors after
they reacted (n = 58). Of these, 16 (27.6%) said they tried to
return to their previous posture, 3 (5.2%) apologized for their
reaction, 1 (1.7%) allowed room for the patient to apologize.
Thirty-eight (65.5%) felt that their reactions were expected and
that no further action was necessary. No significant differences
were observed between physicians who attempted to adjust their
behavior afterwards and physicians who did not, regarding the
different types of reactions.
To cope with their intense emotions at the moment, physicians
resorted to several types of strategies (Table 5). These strategies
were reported especially by physicians who considered they controlled or attempted to control their emotions (73 [96.1%] of
the 76 participants who reported using these strategies, χ2[1] =
10.900, p = 0.001). The difference from physicians who did not
control their emotions (n = 3 [3.95%)] was statistically significant
(χ2[1] = 10.900, p = 0.001). Though most physicians resorting to
coping strategies reported intense negative feelings (63 [84.00%],
comparing with 12 reporting positive and mixed feelings), using
coping strategies was not significantly associated with negative
emotions, and the same types of strategies were generally used
to deal with negative and with mixed emotions. Using coping
strategies was reported in association with positive emotions in
3 cases: breathing, refocusing attention, and a combination of
these 2 to deal, respectively, with intense relief (1 case) and with
happiness (2 cases).
Of the 89 physicians who considered that a relationship with
the patient existed, most (47 [52.8%]) considered that their
emotional reactions had no impact in the relationships with their
Table 3. Physician respondents’ intense emotions experienced
in the presence of patients
Emotions experienced
Negative
Sadness
Fear/anxiety (nervousness, fright, panic, apprehension)
Frustration (powerlessness, incapacity)
Anger (revolt, indignation)
Disappointment
Repulsion (contempt)
Guilt
Shame
Positive
Happiness (joy, self-fulfillment)
Relief
Mixed
Compassion (empathy, tenderness, solidarity)
Surprise/confusion
a
No. (%)a
41 (25.3)
34 (21.0)
32 (19.8)
24 (14.8)
3 (1.9)
2 (1.2)
2 (1.2)
1 (0.6)
7 (4.3)
2 (1.2)
12 (7.4)
2 (1.2)
N = 162 reported emotions. Some survey respondents reported more than one
emotion.
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patients; 33 (37.1%) considered a positive impact; and only a few
(9 [10.1%]) reported negative consequences at the moment. Additionally, 23 participants (43.4% of the 53 who answered this
question) reported that the impact of the episode in their relationship with the patient extended beyond the immediate moment
into future interactions. For 17 (73.9%) of these 23 participants,
the result was positive, whereas for 6 participants (26.1%), it was
negative. Positive consequences included sense of relief, ability to
clarify the situation, awareness of one’s fallibility, increased understanding of the patient’s reality, attitudes, increased admiration
and interest for the patient, increased attention to the patient’s
needs, increased empathy, increased relationship strength, closeness, mutual consideration and trust, and increased adequacy of
the patient’s behavior. Negative consequences included increased
defensiveness, avoidance of the patient, loss of empathy and of
trust in the patient, and relationship termination.
The (immediate or extended) impact of the emotional reaction on the physician-patient relationship was not significantly
associated with valence, duration, relative control of the emotion, or coping strategies used. However, specific reactions had a
significant impact in physician-patient relationships. Touching,
smiling, providing support, and choking up/crying did not yield a
negative impact in physician-patient relationships at the moment
(χ2(1) = 7.814, p = 0.009) or in future interactions (χ2(1) = 5.181,
p = 0.038). On the other hand, withdrawing from the situation,
imposing oneself and defending oneself were significantly associated with an immediate negative impact in the physician-patient
relation (χ2(1) = 16.774, p < 0.001). These reactions tended to
result in negative consequences for physicians who considered
that their reactions required no subsequent adjustment and in
positive consequences for physicians who tried to subsequently
adjust their behavior and repair the situation. These tendencies
were statistically nonsignificant, though. Withdrawing from the
situation, imposing oneself, and engaging in medical procedures
were further associated with a negative impact in future physicianpatient interactions (χ2(1) = 8.727, p = 0.009). Defending oneself
was associated with a positive impact in future interactions for the
1 physician who attempted to go back to his previous posture.
Additionally, the physician who withdrew from the situation but
allowed room for the patient to eventually apologize reported a
positive impact in future interactions with that patient. However,
these tendencies referred to small numbers of physicians and were
statistically nonsignificant.
The type of emotion and its relative control were not significantly associated with physicians’ gender or number of years of
medical experience. However, a greater percentage of physicians
Table 4. Physician respondents’ reactions while experiencing strong emotions in the presence of patients
Categories of reactions
Touching the patient
Performing medical procedures
Withdrawing from the situation
Providing support
Choking up/crying
Imposing oneself
Smiling
Defending oneself
Explaining
Expelling the patient
a
Indicators
Touching/holding the patient’s hand; hugging; shaking hands
Writing a prescription; starting life support
Leaving the room; avoiding the patient (eg, telling him to switch physicians, passing the telephone
to another physician); refusing to see the patient
Maintaining silence, respect, presence; comforting, attempting to understand or to communicate
empathically; offering material help (money, goods)
No. (%)a
13 (18.6)
10 (14.3)
9 (12.9)
Showing grief; feeling moved; unable to speak; crying
Speaking with authority; raising tone of voice; shouting; gesticulating; shaking one’s head; getting up;
walking back and forth
8 (11.4)
7 (10.0)
Explicitly legitimizing one’s perspective
Providing clarification, including one physician who looked at the patient’s eyes and assumed
responsibility for what happened
Standing up and ending the consultation, expelling the patient
8 (11.4)
5 (7.1)
4 (5.7)
4 (5.7)
2 (2.9)
N = 70 respondents reported reactions.
Table 5. Reported coping strategies to deal with emotional reactions in the presence of patients
Categories of coping strategies
Breathing
Keeping the emotion away/focusing on
something else
Talking/listening to the patient
Breaking eye contact
Reframing
Withholding the emotion
a
Indicators
Breathing; taking a deep breath; holding one’s breath
Ignoring; keeping emotional distance from the situation; continuing the encounter as if nothing was
happening; focusing on the (next) task, on the patient, on one’s posture; thinking as a professional;
thinking of a solution; mentally counting
Speaking calmly, gradually, with openness; maintaining silence; empathy; understanding; letting the
patient express himself; keeping eye contact
Gaining time; organizing thoughts
Thinking of/providing an optimistic, hopeful perspective; rationalizing; accepting
Blocking the feelings; not crying
No. (%)a
34 (44.7)
21 (27.6)
7 (9.2)
6 (7.9)
5 (6.6)
3 (3.9)
N = 76 strategies.
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working in rural areas (37.5%) reported compassion, compared
with physicians working in urban areas (8.1%, χ2[1] = 7.110,
p = 0.033), and physicians from the South (ie, Madeira Island)
reported controlling their reactions more than physicians from
the North part of Portugal (χ2[1] = 14.061, p = 0.001). However,
the interpretation of these results needs caution because very few
physicians in the study were from southern Portugal or from
nonurban centers. Physicians’ specific reactions were not significantly associated with number of years of medical experience or
geographic work location. But explaining the situation and expelling the patient were exclusive to male physicians in this sample
(χ2[1] = 9.488, p = 0.005). Physicians of both genders used the
various coping strategies described, but women tended to resort
to breathing more than men (χ2[1] = 5.250, p = 0.022). Breaking
eye contact was significantly associated with fewer years of medical
experience (t[22] = 2.115, p = 0.046). Finally, the duration of the
emotion, the type of behavioral adjustment attempted after the
emotional reaction, and the (immediate or extended) impact of
the emotional reaction on the physician-patient relationship were
statistically unrelated with gender, geographic work location, and
years of medical experience.
DISCUSSION
Results indicate that experiencing negative and positive intense
emotions in the presence of patients is frequent among physicians.
The fact that experiencing intense emotions was more frequent
among those with fewer years of clinical practice suggests that
repeated exposure to these situations or increased clinical experience may contribute to attenuating the emotional response, as
previous studies indicate.25
Previous research on physicians’ emotions has specifically
focused on extreme scenarios associated with negative strong
emotional reactions.18,19 Such scenarios and associated intense
negative feelings were frequent also in this study. However, other
contexts emerged as well, including less extreme scenarios (eg,
dealing with patients’ rudeness) and situations triggering intense
positive emotions (the most frequent being resolving the patient’s
problem). The fact that most situations described here elicited
negative feelings may suggest that negative emotions are more
strongly felt by physicians, or that these may be recalled more
easily than positive experiences.26 An interesting finding is that,
as in previous studies,19 many physicians reported experiencing
longlasting emotions. This may have important clinical implications for patients visiting physicians while these emotions last,
namely regarding decision processes.11
Most physicians in this study tried to control the emotion,
which may partly explain the lack of perceived impact of their
reaction on their relationship with patients. This attempted control suggests that physicians may consider displaying emotional
reactions to be inappropriate in the presence of patients, although
possibly less so if the emotion is positive. Smiling was associated
only with positive emotions, and physicians touched the patient
significantly more if they were experiencing positive feelings. On
the other hand, only participants experiencing negative emotions
reported controlling them completely, probably because they
36
felt that negative emotions were
less appropriate during clinical
interactions.
To deal with these emotions,
physicians used both cognitive
and behavioral coping strategies.
After-the-fact coping strategies
reported in previous research
appeared in our study as ways of
managing emotions at the moment (eg, changing perspectives,
keeping emotional distance, or
talking to the patient).10,21,22 In
our study, physicians additionally used other strategies in the moment, like breathing deeply,
focusing on their posture, thinking about the next action, being
empathic, listening to the patient more, and mentally counting.
Whether or not controlled, in most cases physicians’ emotional
reactions did not affect relationships with patients, at least from
physicians’ perspectives. The impact was also independent from
emotional valence (though no positive emotion had a negative
impact on the relationship) and duration, and from the coping
strategies used. Some specific reactions, however, did have an
impact. Choking up/crying, touching, smiling, and providing
support were significantly associated with an immediate positive
impact and with no impact. This impact also extended into future
interactions. Not surprisingly, withdrawing from the situation,
imposing, and defending oneself were associated with a negative
immediate impact. The former two reactions plus engaging in
medical procedures had a further extended negative impact in
future interactions. But the tendency for readjusting the behavior
after the reaction to be less associated with a negative impact than
when no readjustment existed, though not statistically significant,
suggests that the clinical relationship may be shaped by interactions beyond the display of strong negative reactions, and that the
reaction does not, per se, necessarily lead to a negative impact on
the relationship, as long as interveners have the ability to repair it.
This study took a first step in the inspection of what happens
when physicians experience strong emotions while seeing patients,
and further research is needed for a better understanding of the results. Specifically, better discrimination of the effects of particular
reactions on medical relationships is necessary. Also, the sampling
strategy in this study limited our goal of forming a representative
sample of physicians in the country, which restricts the generalizability of the results. It is possible that physicians who agreed to
participate were particularly interested in the theme, introducing
biases (eg, increasing the prevalence of intense emotions in clinical practice). Because we used a self-report, retrospective instrument, recall or report biases may also exist. Finally, the sample
size may prevent the analysis and the observation of effects that
could be visible with larger numbers of participants per group.
Future research needs to consider additional aspects that could
affect physician-patient relationships (eg, duration and kind of
relationship with the physician) on a larger sample. It is also
important to assess patients’ perceptions of physicians’ emotions
and of their impact on the clinical relationship, in addition to
… physicians
additionally used
other strategies in the
moment, like breathing
deeply, focusing on
their posture, thinking
about the next action,
being empathic,
listening to the patient
more, and mentally
counting.
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Physicians Experiencing Intense Emotions While Seeing Their Patients: What Happens?
assessing patients’ own reactions to the situations. The inclusion
of other clinical implications is also crucial, such as the effect of
physicians’ emotional state in appropriate medical management,
as suggested in previous studies.11
CONCLUSION
Although the display of emotions in medical encounters may be
considered unprofessional, the experience of intense emotions by
physicians in the presence of patients seems frequent. Physicians
control the display of intense negative emotions more than that of
positive reactions. However, relative control of the emotion, coping strategies used, the valence (positive, negative, or mixed), and
the duration of the emotion do not affect the clinical relationship.
Specific emotional reactions do. Choking up/crying, touching,
smiling, and providing support did not affect relationships in
negative ways, but leaving the patient, imposing, and defending
oneself did. The fact that the impact of these reactions could be
different according to physicians’ subsequent adjusted behavior
suggests that this impact may be modulated by the interlocutors’
following actions, namely attempts at repairing the situation.
Future studies are needed to clarify these results. v
Disclosure Statement
The author(s) have no conflicts of interest to disclose.
Acknowledgment
Mary Corrado, ELS, provided editorial assistance.
How to Cite this Article
da Silva JV, Carvalho I. Physicians experiencing intense emotions while
seeing their patients: What happens? Perm J 2016 Summer;20(3):15-229.
DOI: http://dx.doi.org/10.7812/TPP/15-229.
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What Counts
It is the human touch after all that counts for most
in our relation with our patients.
— Robert Tuttle Morris, 1857-1945, American surgeon and author
The Permanente Journal/Perm J 2016 Summer;20(3):15-229
37
ORIGINAL RESEARCH & CONTRIBUTIONS
Difference in Effectiveness of Medication
Adherence Intervention by Health Literacy Level
Ashli A Owen-Smith, PhD, SM; David H Smith, PhD, RPh; Cynthia S Rand, PhD; Jeffrey O Tom, MD, MS;
Reesa Laws; Amy Waterbury, MPH; Andrew Williams, PhD; William M Vollmer, PhD
Perm J 2016 Summer;20(3):15-200
E-Pub: 06/29/2016 http://dx.doi.org/10.7812/TPP/15-200
ABSTRACT
Context: There is little research investigating whether health information technologies, such as interactive voice recognition, are effective ways to deliver information to
individuals with lower health literacy.
Objective: Determine the extent to which the impact of an interactive voice
recognition-based intervention to improve medication adherence appeared to vary by
participants’ health literacy level.
Design: Promoting Adherence to Improve Effectiveness of Cardiovascular Disease
Therapies (PATIENT) was a randomized clinical trial designed to test the impact, compared
with usual care, of 2 technology-based interventions that leveraged interactive voice
recognition to promote medication adherence. A 14% subset of participants was sent a
survey that included questions on health literacy. This exploratory analysis was limited
to the 833 individuals who responded to the survey and provided data on health literacy.
Main Outcome Measures: Adherence to statins and/or angiotensin-converting enzyme
inhibitors and/or angiotensin II receptor blockers.
Results: Although intervention effects did not differ significantly by level of health
literacy, the data were suggestive of differential intervention effects by health literacy level.
Conclusions: The differences in intervention effects for high vs low health literacy in
this exploratory analysis are consistent with the hypothesis that individuals with lower
health literacy may derive greater benefit from this type of intervention compared with
individuals with higher health literacy. Additional studies are needed to further explore
this finding.
INTRODUCTION
Treatment nonadherence with cardiovascular disease (CVD) therapy has been
well documented1 and is a major contributor to increased cardiovascular risk
and morbidity.2 At the population level,
low adherence is often the broken link
between effective new therapies and improved health outcomes.3 Nonadherence
has also been identified as a key target for
reducing unnecessary health care costs.4,5
The most effective adherence interventions include both educational and behavioral strategies6; however, these strategies
are costly and require both staff time and
specialized counseling skills, which can
limit the likelihood for dissemination.
Furthermore, most interventions evaluated
thus far have enrolled highly select and
small patient populations, thus limiting
generalizability. More recently, research
has focused on using health information
technologies (HIT) to develop low-cost
interventions that can be delivered to
large populations to promote adherence
for patients with chronic illness.7-9 For
example, one recent study described an
intervention among 5216 adults who were
newly prescribed a statin but had failed to
fill the prescription.10 The intervention
group received automated telephone reminder calls followed by mailed letters.
The intervention improved initial fill rates
during the next 25 days by 16 percentage
points. These and other studies suggest that
HIT-based reminder interventions offer a
promising, “light-touch” option for promoting adherence in large populations.11-14
Although HIT-based interventions
may be more easily disseminated, reach
a greater number of people, and be lower
cost, they may exacerbate certain health
disparities, because more educated and
technologically advanced individuals
will benefit disproportionately from
such advances. 15,16 Patients with low
health literacy—individuals who face
challenges with respect to their capacity
to obtain, process, and understand basic
health information and services needed
to make appropriate health decisions17—
are likely to be particularly vulnerable in
this regard.18 Individuals with low health
literacy, for example, are much less likely
to use computers, mobile applications,
and other consumer and patient medical
devices. 19,20 Consequently, it has been
argued that interactive voice recognition (IVR) is one type of HIT that may
be particularly well suited for delivering
interventions to low-literacy individuals
because it 1) delivers information via
speech instead of text and 2) uses the
telephone so that computer access and
computer literacy are not required.19,21,22
An Institute of Medicine report23 in
2004 called for studies that establish effective approaches to reduce the negative
Ashli A Owen-Smith, PhD, SM, is an Assistant Professor of Health Management and Policy at the Georgia State University
School of Public Health in Atlanta. E-mail: [email protected]. David H Smith, PhD, RPh, is a Senior Investigator at The
Kaiser Permanente Center for Health Research in Portland, OR. E-mail: [email protected]. Cynthia S Rand, PhD,
is a Professor of Medicine in the Department of Medicine at the Johns Hopkins School of Medicine in Baltimore, MD.
E-mail: [email protected]. Jeffrey O Tom, MD, MS, is an Assistant Clinical Professor in the Department of Pediatrics at the
University of Hawaii John A Burns School of Medicine in Honolulu. E-mail: [email protected]. Reesa Laws is the Research
and Data Analytics Center Manager and Technical Research Program Manager at The Kaiser Permanente Center for Health
Research in Portland, OR. E-mail: [email protected]. Amy Waterbury, MPH, is a Research Program Manager at The
Kaiser Permanente Center for Health Research in Portland, OR. E-mail: [email protected]. Andrew Williams, PhD,
is a Faculty Scientist in the Center for Outcomes Research and Evaluation at the Maine Medical Center Research Institute
in Scarborough. E-mail: [email protected]. William M Vollmer, PhD, is a Senior Investigator at The Kaiser Permanente
Center for Health Research in Portland, OR. E-mail: [email protected].
38
The Permanente Journal/Perm J 2016 Summer;20(3):15-200
ORIGINAL RESEARCH & CONTRIBUTIONS
Difference in Effectiveness of Medication Adherence Intervention by Health Literacy Level
effects of limited health literacy. However,
there is still little research to date investigating whether IVR systems are, in fact,
effective ways to deliver health information
to lower health literacy individuals with
chronic disease.
The purpose of the present exploratory
analysis was to explore whether an IVRbased intervention to improve medication
adherence among individuals with CVD
or diabetes mellitus would yield differences
in outcomes according to participants’
health literacy level.
METHODS
Study Design
The Promoting Adherence to Improve
Effectiveness of Cardiovascular Disease
Therapies (PATIENT) study was a randomized pragmatic clinical trial in which
21,752 adults were randomly assigned to
receive either usual care or 1 of 2 HITbased interventions designed to increase
adherence to statins, angiotensin-converting enzyme inhibitors (ACEIs), and angiotensin II receptor blockers (ARBs). Before
randomization at baseline, a subgroup of
potentially eligible individuals (n = 2965)
were recruited to participate in an interviewer-administered survey via telephone
in English, which was conducted centrally
by a team of experienced interviewers. The
baseline survey was administered from
September through December 2011 and
had a completion rate of 57% (n = 1678).
Among those who completed the survey,
833 respondents ultimately were randomly
assigned to participate in the intervention.
Data for the present study were based on
this subgroup of individuals.
Research Setting
Participants were members of 1 of 3 Regions of Kaiser Permanente (KP), a health
maintenance organization providing
comprehensive, prepaid health care to its
members. The three Regions, Northwest
(KPNW), Hawaii (KPHI), and Georgia
(KPGA), collectively serve a population
of about 944,000 individuals. The institutional review boards at all 3 study sites
approved the study. An external data and
safety monitoring board and local clinician
advisory boards at each site approved the
study protocol and monitored the study
for safety and data quality.
The Permanente Journal/Perm J 2016 Summer;20(3):15-200
The PATIENT Study
We have previously described the
PATIENT study in detail.24 Using each Region’s electronic medical records (EMRs),
we identified participants aged 40 years
and older with diabetes mellitus and/or
CVD, with suboptimal (< 90%) adherence to a statin or ACEI/ARB during the
previous 12 months, and who were due or
overdue for a refill. Individuals with medical conditions that might contraindicate
the use of these medications (eg, allergic
to the medication, liver failure, cirrhosis,
rhabdomyolysis, end-stage renal disease,
chronic kidney disease) and those on KP’s
“do not contact” list were excluded. In each
Region, we randomly assigned a sample
of eligible members to the 3 study arms
(usual care and 2 intervention arms) in a
1:1:1 ratio at the study outset and repeated
this process for newly eligible members
for each of the following 5 months. Study
enrollment began in December 2011 and
continued through May 2012. Intervention and outcome assessment continued
through November 2012.
In the first intervention arm, IVR, participants received automated phone calls
when they were due or overdue for a refill
of their ACE/ARB and/or statin. Patients
were offered a transfer to KP’s automated
pharmacy refill line. In the second intervention arm, enhanced IVR, participants
received the same calls as in the IVR arm
but also received a personalized reminder
letter if they were 60 to 90 days overdue
and a live outreach call if they were 90 days
or more overdue, as well as EMR-based
feedback to their primary care clinicians.
Participants in the enhanced IVR arm
received additional written and graphic
materials, including a personalized health
report with their most recent blood pressure and cholesterol levels, a pill organizer,
and bimonthly mailings to answer common questions. The IVR call scripts, letters, and other mailings were written at a
sixth-grade reading level.
Study Measurements
Electronic Medical Record Data
We used a modified version of the Proportion of Days Covered for our primary
measure of medication adherence.25 Because
we were measuring long-term medications
that the patients were known to be taking
Health Literacy Questions
1. How often do you need to have
someone help you when you read
instructions, pamphlets, or other
written materials from your doctor
or pharmacy?
2. How confident are you filling out
medical forms by yourself?
3. How would you rate your ability
to read?
at the time of randomization, we modified
the Proportion of Days Covered to include
the whole follow-up period as the denominator timeframe rather than time from first
dispensing.26 We also accounted for medication on hand at randomization and ignored
any medication remaining at the end of
follow-up. We computed the modified
Proportion of Days Covered separately for
statins and ACEI/ARBs. To simplify enrollment logistics, we defined study eligibility
at baseline using the simpler Medication
Possession Ratio, which we computed by
dividing total days’ dispensed supply by
365 and capping at 1.
We used the EMR to capture age, race,
sex, physical and mental health comorbidities, smoking status, body mass index, number of medications dispensed, health care
utilization, hospital and Emergency Department visits, and blood pressure and lipid levels. We defined baseline systolic and diastolic
blood pressure levels as the mean of the 6
most recent measurements taken during the
12 months before randomization. Follow-up
blood pressure was defined as the mean of the
6 most recent measurements taken before the
end of the study period, which ranged from
6 to 12 months of follow-up depending on
when randomization occurred. We defined
blood pressure control as blood pressure
below 140/90 mmHg and lipid control as
a low-density-lipoprotein cholesterol level
below 100 mg/dL.
Survey Data
Participants were asked three singleitem health literacy questions (see Sidebar: Health Literacy Questions). The first
question, used previously by Williams and
colleagues,27 aimed to assess participants’
use of a surrogate reader: “How often do
you need to have someone help you when
you read instructions, pamphlets, or other
written materials from your doctor or
39
ORIGINAL RESEARCH & CONTRIBUTIONS
Difference in Effectiveness of Medication Adherence Intervention by Health Literacy Level
Table 1. Characteristics of study population, total and by health literacy level
Characteristic
Age, years (mean ± SD )
Sex, %
Women
Men
Race/ethnicity, %
Asian
Black/African American
Native Hawaiian/Pacific Islander
White
Other
Hispanic
Highest level of education, %
High school or less
Some college/college degree
Some graduate school/graduate degree
Household income, %
< $25,000
$25,000-$49,000
$50,000-$74,999
≥ $75,000
Marital status, %
Single
Married/partnered
Separated/divorced/widowed
Health history
Uncontrolled blood pressure,%
Uncontrolled LDL cholesterol, %
Baseline statin adherence among users, mean ± SD
Baseline ACEI/ARB adherence among users, mean ± SD
No. of medications dispensed, %
1-5
6-12
≥ 13
ED visit in last 6 months, %
Hospitalization in last 6 months, %
Health care utilization in last 6 months, mean
HUI2, mean ± SD
HUI3, mean ± SD
Satisfied with care, %
Depression diagnosis, %
BMI,e %
18.5-24.9
25.0-29.9
30.0-39.9
≥ 40
Smoker, %
a
b
Total
(N = 833)
65.2 ± 11.6
Health literacy level
Low
High
(n = 148)
(n = 685)
69.5 ± 13.2
64.3 ± 11.0
Significancea
t = -5.01, p = < 0.001
51.0
49.0
51.3
48.7
50.9
49.1
χ2 = 0.008, p = 0.93
12.9
17.0
6.1
57.7
6.3
2.7b
19.1
12.9
5.4
53.1
9.5
1.0c
11.6
17.9
6.2
58.7
5.6
3.06d
χ2 = 10.70, p = 0.03
34.3
53.9
11.9
60.8
33.8
5.4
28.5
58.2
13.3
χ2 = 34.82, p = < 0.001
20.6
35.5
20.5
23.4
36.9
43.4
10.7
9.0
17.3
33.8
22.5
26.4
χ2 = 39.21, p = < 0.001
13.3
62.8
23.8
10.8
58.1
31.1
13.9
63.9
22.2
χ2 = 5.48, p = 0.07
14.7
30.2
0.59 ± 0.27
0.65 ± 0.30
19.3
27.3
0.60 ± 0.25
0.62 ± 0.32
13.7
30.8
0.59 ± 0.27
0.66 ± 0.29
χ2 = 3.03, p = 0.08
χ2 = 0.59, p = 0.44
t = -0.11, p = 0.91
t = 1.11, p = 0.27
39.1
39.1
21.7
10.6
4.2
6.5 ± 6.8
0.84 ± 0.17
0.77 ± 0.28
93.0
3.4
41.9
32.4
25.7
13.5
3.4
7.8 ± 8.3
0.79 ± 0.20
0.60 ± 0.35
92.6
6.1
38.5
40.6
20.9
9.9
4.4
6.2 ± 6.3
0.85 ± 0.17
0.80 ± 0.25
93.1
2.8
χ2 = 0.17, p = 0.68
11.8
29.7
47.2
11.3
10.1
14.9
39.2
35.1
10.8
11.2
11.1
27.8
49.7
11.4
9.9
χ2 = 1.31, p = 0.25
χ2 = 1.66, p = 0.20
χ2 = 0.30, p = 0.58
t = −2.64, p = 0.01
t = 3.06, p = 0.00
t = 7.43, p = < 0.001
χ2 = 0.06, p = 0.81
χ2 = 4.10, p = 0.04
χ2 = 3.30, p = 0.07
χ2 = 0.23, p = 0.23
Two-sided p values based on F test for continuous variables, Pearson χ test for unordered categorical data, and Mantel-Haenszel χ test for ordered categorical data;
N = 589. c n = 1. d n = 15. e kg/m2.
2
2
ACEI/ARB = angiotensin-converting enzyme inhibitor/angiotensin II receptor blocker; BMI = body mass index; ED = Emergency Department; HUI = Health Utilities Index mark;
LDL = low-density lipoprotein; SD = standard deviation.
40
The Permanente Journal/Perm J 2016 Summer;20(3):15-200
ORIGINAL RESEARCH & CONTRIBUTIONS
Difference in Effectiveness of Medication Adherence Intervention by Health Literacy Level
pharmacy?” Participants responded using a
five-item Likert scale ranging from “never”
to “always.” We considered participants
who indicated that they “always” or “often”
needed help as having low health literacy
for this question. The second question,
used by Chew and colleagues,28,29 aimed
to assess participants’ confidence with
medical forms: “How confident are you
filling out medical forms by yourself?”
Participants responded using a five-item
Likert scale ranging from “not at all” to
“extremely.” We considered participants
who indicated that they were “not at all”
or “a little bit” confident as having low
health literacy for this question. The third
question, also used by Williams and colleagues,27 aimed to assess participants’
self-rated reading ability: “How would
you rate your ability to read?” Participants
responded using a six-item Likert scale
ranging from “very poor” to “excellent.”
We considered participants who indicated
that their reading ability was “very poor” or
“poor” as having low health literacy for this
question. For the purposes of this study,
we assigned individuals to the low health
literacy group if their responses met those
criteria on any of the three questions.
Participants were asked about their current health status and health-related quality
of life using the Health Utilities Index. Both
the Mark 2 and Mark 3 Health Utilities
Index instruments were used to provide a
comprehensive health status classification
based on the domains of health and levels of
functional ability/disability in each domain.
These domains included vision, hearing,
speech, ambulation, dexterity, cognition,
pain, self-care, and emotion.30
Participants were asked whether they
were satisfied with the care they received
from their clinicians and whether they
could indicate that they were “very satisfied,” “satisfied,” “uncertain,” “unsatisfied,”
or “very unsatisfied.” Individuals were
categorized as satisfied with their health
care if they endorsed that they were either
“very satisfied” or “satisfied” in response
to this question.
Finally, participants were asked about
their highest level of schooling completed,
total household income, and marital status.
Statistical Analysis
Among those who participated in the
baseline survey (N = 1678), complete
health literacy and intervention outcome
data were available for only 833 of these
individuals. The other 845 individuals who
completed the survey were not randomly
assigned to participate in the intervention.
Therefore, our analyses are restricted to this
subset of 833 participants. For bivariate
analyses, we used t-tests for comparisons
of means of continuous variables, Pearson
χ2 tests for comparing unordered categorical data, and Mantel-Haenszel χ2 tests
for comparing ordered categorical data.
Separate analyses were conducted for users
of statins and users of ACEI/ARBs. We assessed whether intervention effects differed
by health literacy level in general linear
models with main effects for treatment
arm, health literacy, and their interaction.
Main effect estimates were adjusted for
site and sex. We assessed follow-up from
randomization until the end of the study
or loss of Health Plan coverage, whichever
came first.
Because the study was not designed to
examine whether the intervention effects
differed by health literacy level, these post
hoc analyses are inevitably exploratory in
nature, and we made no adjustment for
multiple comparisons or to conduct retrospective power calculations. Statistical
software (SAS v9.2, SAS Institute, Cary,
NC) was used for statistical analyses.
RESULTS
The study population was approximately
65 years of age on average, equally men
and women, predominantly white (approximately 58%), had some college or a
college degree (approximately 54%), were
middle income, and were currently married
or with a partner (approximately 63%). Approximately 18% of participants had low
health literacy (n = 148). Participants who
had low health literacy were more likely to
be older, have a lower level of education,
report a lower total household income, use
health care services more frequently, report
poorer health status, and have a depression
diagnosis compared with participants who
had higher health literacy (Table 1).
Although both the IVR and enhanced
IVR interventions increased adherence to
statins and ACEIs/ARBs compared with
usual care in the full trial analysis, in this
much smaller sample we did not observe
statistically significant differences between
either IVR or enhanced IVR and usual care
in subgroups defined by health literacy
status (Table 2). Of more immediate relevance to the focus of this exploratory analysis, however, the data were suggestive of
differential intervention effects for low and
high health literacy. Among participants
Table 2. Analysis of adherence by health literacy level
Follow-up
adherence by
health literacy level
Enhanced
interactive voice
recognition
Interactive
voice
recognition
Adherence to statins (interaction p = 0.202)
Low
0.61 ± 0.034c
0.56 ± 0.36
High
0.58 ± 0.34
0.58 ± 0.29
Adherence to ACEI/ARBs (interaction p = 0.116)
Low
0.70 ± 0.32
0.62 ± 0.37
High
0.58 ± 0.37
0.62 ± 0.31
Usual
care
Enhanced interactive voice
recognition vs usual care
Δa
Significanceb
Interactive voice
recognition vs usual care
Δa
Significanceb
0.52 ± 0.32
0.59 ± 0.32
0.105 (-0.035, 0.246)
-0.026 (-0.094, 0.042)
0.143
0.460
0.09 (-0.061, 0.241)
-0.032 (-0.101, 0.036)
0.244
0.359
0.52 ± 0.33
0.62 ± 0.31
0.146 (-0.023, 0.316)
-0.053 (-0.133, 0.027)
0.091
0.196
0.075 (-0.091, 0.241)
-0.011 (-0.089, 0.067)
0.375
0.780
Net intervention effect, expressed as mean (and 95% confidence interval).
Two-tailed significance level based on linear regression analysis adjusting for site and sex as fixed main effects. Health literacy subgroup analyses also include the corresponding
treatment by subgroup interaction.
c
Raw, unadjusted adherence, expressed as mean ± standard deviation.
a
b
ACEI/ARB = angiotensin-converting enzyme inhibitor/angiotensin II receptor blocker.
The Permanente Journal/Perm J 2016 Summer;20(3):15-200
41
ORIGINAL RESEARCH & CONTRIBUTIONS
Difference in Effectiveness of Medication Adherence Intervention by Health Literacy Level
with low health literacy, for example, the
IVR and enhanced IVR interventions were
associated with statin adherence that was
9% to 10.5% higher than for usual care.
By contrast, among participants with high
health literacy, statin adherence in the IVR
and enhanced IVR groups was 2.6% to
3.2% lower than for usual care.
We observed a similar pattern for ACEI/
ARB adherence. Participants with low
health literacy in either IVR group (IVR
or enhanced IVR) had ACEI/ARB adherence that was 7.5 percentage points to 14.6
percentage points higher than for usual
care, whereas among participants with high
health literacy the IVR and enhanced IVR
interventions were associated with ACEI/
ARB adherence that was 1.1 percentage
points to 5.3 percentage points lower
than for usual care. However, although
consistent with an interaction effect, none
of the tests of health literacy by treatment
interactions was statistically significant.
DISCUSSION
Although not statistically significant, the
differences in observed intervention effects
for high vs low health literacy in the study
sample are certainly consistent with the hypothesis that individuals with lower health
literacy may derive greater benefit from
this type of intervention compared with
individuals with higher health literacy. In
a review of promising HIT interventions
for diabetes, Boren21 identified telephone
interventions for education, counseling,
and reminding as an appropriate method
for individuals with limited health literacy.
Our results provide some preliminary support for this notion.
Approximately 18% of the study
population in the present study had low
health literacy; this estimate is generally
consistent with prior studies. Depending
on the study population and health literacy measure employed, the prevalence
of low health literacy ranges from 11% to
44%.31-35 Also consistent with the prior
literature, we found that individuals with
lower health literacy are more likely to be
of lower socioeconomic status compared
with higher health literacy individuals.
For example, other studies have similarly
reported that years of school completed31-34,36-39 and income32-34,38,39 are significantly associated with health literacy level.
42
… lower health literacy
populations may be more
responsive to this type
of interactive voice recognitionbased intervention compared
with higher health literacy
populations, a finding that
may lead to even more efficient
patient outreach.
Individuals with low health literacy in
the present study were more likely to have
poorer health-related quality of life and a
depression diagnosis compared with those
with high health literacy. Prior studies have
consistently reported that lower health
literacy populations frequently experience
poorer health status as indicated by 1)
specific biochemical and biometric health
outcomes such as higher blood pressure37,40
and poor control of Type 2 diabetes,32,41,42
2) disease prevalence and incidence such as
higher rates of depression,43-46 and 3) global
health status.31,33,38,47-49 In contrast to previous studies, individuals with low health
literacy in this study were not more likely
to have Emergency Department visits or
hospitalizations in the previous six months
compared with individuals with higher
health literacy.50-53 They were, however,
more likely to use other health services
such as regular office visits compared with
individuals with higher health literacy.
Interestingly, individuals with low
health literacy did not differ from individuals with high health literacy with
respect to baseline statin or ACEI/ARB
adherence. Although one study found a
positive association between poor health
literacy and low adherence to cardiovascular medications,54 a recent systematic
review examining this phenomenon concluded that the current evidence does not
show a consistent relationship between
health literacy and medication adherence
in adults with CVD or diabetes.55
The present study has several limitations. First, the small intervention effect
seen in the parent trial, combined with
the much smaller sample size for this
analysis, greatly limits our power to detect
significant interactions. Second, although
the survey completion rate was satisfactory (approximately 57%), individuals
who decided to participate in the survey
may differ from those who declined to
participate. For example, previous studies suggest that certain subgroups may
be less likely to participate in telephone
surveys, including men, those with less
education, and individuals in poorer
health.56-58 Third, because the survey was
administered only in English, individuals
for whom English was a second language
and/or who were uncomfortable or unable
to complete the survey in English were not
included; therefore, our findings cannot be
generalized to these populations. Fourth,
although we used 3 well-validated, reliable,
single-item measures for identifying poor
health literacy,59 our summed health literacy
score based on these 3 items has not been
compared against one of the gold standard
instruments, such as the Rapid Estimate
of Adult Literacy in Medicine60 or the Test
of Functional Health Literacy in Adults.61
However, Hardie and colleagues51 similarly provided a summed health literacy
score based on participants’ responses to
3 single-item questions and reported that
these questions correctly identified individuals with inadequate health literacy
90% to 95% of the time. Therefore, we
feel confident that we have accurately
categorized the individuals who have low
health literacy in our population. Another
benefit of using these 3 items includes a
shorter time burden for patients, as they
take only a few minutes to complete (in
contrast to the Test of Functional Health
Literacy in Adults, which can take up to
30 minutes). In addition, these questions
pose less risk of embarrassment to patients
in contrast to the Rapid Estimate of Adult
Literacy in Medicine, which asks patients
to read aloud medical terms such as herpes,
testicle, and hemorrhoids.
CONCLUSIONS
Attractive features of health interventions include both effectiveness and cost
savings. With use of HIT and automation
of the delivery of such health education
messaging, there are possible cost savings
associated with reduced personnel time.62
Furthermore, our findings suggest that
lower health literacy populations may
be more responsive to this type of IVRbased intervention compared with higher
health literacy populations, a finding that
The Permanente Journal/Perm J 2016 Summer;20(3):15-200
ORIGINAL RESEARCH & CONTRIBUTIONS
Difference in Effectiveness of Medication Adherence Intervention by Health Literacy Level
may lead to even more efficient patient
outreach. By allowing the health system
to better tailor intervention activities to
specific patient characteristics, limited
financial resources can be allocated where
there is the potential for the greatest impact. Future studies are needed to explore
the most effective and efficient methods
for identifying and reaching individuals
with lower health literacy. v
10.
11.
12.
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
Acknowledgment
Kathleen Louden, ELS, of Louden Health
Communications provided editorial assistance.
How to Cite this Article
Owen-Smith AA, Smith DH, Rand CS, et al.
Difference in effectiveness of medication adherence
intervention by health literacy level. Perm J 2016
Summer;20(3):15-200. DOI: http://dx.doi.org/
10.7812/TPP/15-200.
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People Are Not Like This
Nowadays people are not like this [ie, temperate in eating and
drinking]; they use wine as beverage and they adopt reckless
behavior … . Their passions exhaust their vital forces; their cravings
dissipate their true [essence]; they do not know how to find
contentment within themselves; they are not skilled in the control of
their spirits. They devote all their attention to the amusement of their
minds, thus cutting themselves off from the joys of long [life]. Their
rising and retiring is without regularity. For these reasons they reach
only one half of the hundred years and then they degenerate.
— The Yellow Emperor’s Classic of Internal Medicine, Huangdi, c 2704 BC - 2598 BC,
known as the Yellow Emperor, a legendary Chinese sovereign and culture hero
44
The Permanente Journal/Perm J 2016 Summer;20(3):15-200
ORIGINAL RESEARCH & CONTRIBUTIONS
Lifestyle and Self-Management by Those Who Live It:
Patients Engaging Patients in a Chronic Disease Model
Michelle T Jesse, PhD; Elizabeth Rubinstein; Anne Eshelman, PhD, ABPP; Corinne Wee;
Mrunalini Tankasala; Jia Li, PhD; Marwan Abouljoud, MD, CPE, MMM, FACS
E-pub: 07/13/2016 Perm J 2016 Summer;20(3):15-207
http://dx.doi.org/10.7812/TPP/15-207
ABSTRACT
Background: Patients pursuing organ transplantation have complex medical needs,
undergo comprehensive evaluation for possible listing, and require extensive education.
However, transplant patients and their supports frequently report the need for more
lifestyle and self-management strategies for living with organ transplantation.
Objectives: First, to explore feasibility of a successful, patient-run transplant lifestyle
educational group (Transplant Living Community), designed to complement medical
care and integrated into the clinical setting; and second, to report the major themes
of patients’ and supports’ qualitative and quantitative feedback regarding the group.
Methods: Informal programmatic review and patient satisfaction surveys.
Results: A total of 1862 patient satisfaction surveys were disseminated and 823 were
returned (response rate, 44.2%). Patients and their supports reported positive feedback
regarding the group, including appreciation that the volunteer was a transplant recipient
and gratitude for the lifestyle information. Five areas were associated with the success
of Transplant Living Community: 1) a “champion” dedicated to the program and its successful integration into a multidisciplinary team; 2) a health care environment receptive
to integration of a patient-led group with ongoing community development; 3) a high
level of visibility to physicians and staff, patients, and supports; 4) a clearly presented
and manageable lifestyle plan (“Play Your ACES”a [Attitude, Compliance, Exercise, and
Support]), and 5) a strong volunteer structure with thoughtful training with the ultimate
objective of volunteers taking ownership of the program.
Conclusion: It is feasible to integrate a sustainable patient-led lifestyle and selfmanagement educational group into a busy tertiary care clinic for patients with complex
chronic illnesses.
INTRODUCTION
Patients with end-stage organ disease
referred for possible organ transplantation are a highly complex, multimorbidity
population. Given the medical and psychosocial complexities, including potential patient impairments (eg, cognitive or
physical disability) and provision of care
through multidisciplinary teams, these
patients require a great deal of education
on the transplant process and ongoing support.1 Nurses, social workers, physicians,
and surgeons are the most frequent providers of education to end-stage organ disease
patients who are pursuing transplant.2-4
Disease management programs are considered an important component of care for
patients living with a transplanted organ5,6
and have been associated with positive
outcomes such as improved patient satisfaction and adherence.7,8
Patients with end-stage organ disease
have increased risks for cognitive impairments secondary to their illnesses.9-17 Educational programs must take into account
the patient’s ability to process and recall
educational information provided. 18-20
Involvement of family members in the
care of patients with chronic diseases
significantly increases patient physical
and mental health.21 Additionally, the
positive effects of educational interventions are sustained longer with support
involvement.21 Both transplant patients
and their supports report the need for
more comprehensive education and, in
particular, lifestyle and long-term selfmanagement, because this is frequently
not addressed or not adequately addressed
by hospital staff.5,22-25 However, there are
gaps in available evidence on the education of support systems in the context of
organ transplantation.
The provision of patient-centered care
with efficient use of resources has become
the quality standard in today’s health
care environment.26,27 Integration of the
posttransplant patient into the plan of
care provides an alternative way to meet a
quality standard that has been successful
with other patient populations.28 However,
strategies to address lifestyle and self-management in organ transplant patients have
been limited to information gathering (eg,
patient focus groups), nurse-led education
groups, or other multidisciplinary teamprotocol refinements.3,29-31 Although these
are important first steps, their findings support the need for integration of transplant
patients in the refinement of resources and
education on successful lifestyle and selfmanagement strategies.
The purpose of this study was 2-fold:
1) to explore the feasibility of a successful,
patient-run transplant lifestyle educational
group designed to complement medical
care and integrated into the clinical setting,
and 2) to report patients’ and supports’
qualitative and quantitative feedback regarding the group.
Michelle T Jesse, PhD, is a Bioscientist for the Transplant Institute and Senior Staff Psychologist in the Behavioral Health Department at the
Henry Ford Health System in Detroit, MI. E-mail: [email protected]. Elizabeth Rubinstein is a Patient Advocate for the Transplant Institute at the
Henry Ford Health System in Detroit, MI. E-mail: [email protected]. Anne Eshelman, PhD, ABPP, is a Senior Staff Psychologist for the Transplant
Institute at the Henry Ford Health System in Detroit, MI. E-mail: [email protected]. Corinne Wee is a Research Assistant for the Transplant
Institute at the Henry Ford Health System in Detroit, MI. E-mail: [email protected]. Mrunalini Tankasala is a Research Assistant for
the Transplant Institute at the Henry Ford Health System in Detroit, MI. E-mail: [email protected]. Jia Li, PhD, is an Assistant Scientist in
Public Health Sciences at the Henry Ford Health System in Detroit, MI. E-mail: [email protected]. Marwan Abouljoud, MD, CPE, MMM, FACS, is the
Director of the Transplant Institute and Hepatobiliary Surgery for the Henry Ford Health System in Detroit, MI. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-207
45
ORIGINAL RESEARCH & CONTRIBUTIONS
Lifestyle and Self-Management by Those Who Live It: Patients Engaging Patients in a Chronic Disease Model
Transplant Living Community:
Program Success and Feasibility
The Henry Ford Health System Transplant Living Community (TLC) was established in 2008 via a collective patient
initiative. TLC is a patient-to-patient organ transplant education program aimed
at increasing patient and family awareness
of necessary lifestyle changes throughout
the transplant process. The framework for
the program incorporates foundational
principles of successful hospice, geriatric,
pediatric, and cancer patient advocacy. The
program is subject to institutional oversight and exists as an “ambassador” (volunteer) program to support patients, living
donors, supports, and families throughout
the transplant process. Transplant recipients are welcome to volunteer (beginning
the service no sooner than 10 months after
the transplant) and undergo an extensive
training curriculum that covers empathic
listening skills, appropriate medical referral
to physicians, Health Insurance Portability and Accountability Act regulations,
TLC platform materials, and continued
mentoring. Training occurs during 2 full
days (16 hours) followed by several weeks
of supervised in-clinic training with established ambassadors. All ambassador volunteers are transplant recipients, representing
heart, lung, kidney, pancreas, liver, multivisceral, and bone marrow transplants.
However, ambassadors and patients are
not matched based upon organ received.
Ambassador volunteers provide interactive,
onsite support within clinic and inpatient
floors daily Monday through Friday. Since
2008, there have been more than 40 active
ambassadors.
The primary goal of TLC is expressed
to patients as “Play Your ACES!”a (Attitude, Compliance, Exercise, and Support),
which highlight important areas of selfmanagement skills necessary for successful
transplant, with an easy-to-understand,
patient-centered approach. The elements
of “Play Your ACES!”a are not unitary constructs but represent an adaptive lifestyle
approach while living with chronic illness.
Attitude refers to more than positivity; it
means having a “fighting attitude,” which
is a more active coping strategy to manage
the instability of living with chronic illness
and embracing the new normal of living
with an organ transplant. Compliance
46
focuses on the lifestyle elements of adhering to a complicated treatment regimen
amid real-life circumstances, which could
create obstacles or challenges to taking optimal care of oneself—for example, exploring and strategizing on environmental or
social barriers that may hinder the patient’s
ability to adhere. Exercise includes redefining exercise to make it attainable with small
incremental increases in activity (eg, walking 25 steps today, 35 steps tomorrow) and
using charting tools to track progress. This
allows for small successes to be recognized
and reinforces physical activity. Lastly, sup-
of the education on self-management
skills and posttransplant lifestyle changes.
Within the TLC education, both patients
and supports are addressed as a team unit
where specific conceptualized home support team assignments are identified to
include all family members, other supports, and extended support structures.
For patients who undergo transplantation, a TLC ambassador visits the patient
before discharge and provides him or her
with a TLC Toolkit complementing prior
pretransplant TLC education. The TLC
Toolkit contains personal health recording
The primary goal of TLC is expressed to patients as “Play Your ACES!”a
(Attitude, Compliance, Exercise, and Support) … are not unitary constructs
but represent an adaptive lifestyle approach while living with chronic illness.
port is a multimember team for long-term
support. TLC defines the duties of each
person with a conceptualized approach.
Some of the support roles include CEO
or primary care manager, assistant CEO,
drivers, medication manager, comedian,
exercise buddy, spiritual caretaker, and
other tangible support (eg, mowing the
lawn, making meals, babysitting). All
education and materials are presented in
the patient voice (avoiding medical jargon)
from a patient perspective and address
only lifestyle components. All medical
aspects of transplant are referred directly
to medical staff and remain in the medical
domain. TLC provides organizational tools
and education to help patients navigate
their medical care on a daily basis. TLC
addresses caregivers as team members and
provides a stylized support team approach
involving the entire family in a positive,
cooperative manner throughout the continuum of care.
What is truly unique about TLC, besides being entirely patient run, is its successful integration into routine clinical
care. Within the waiting room of the main
clinic there is an information table, staffed
by an ambassador volunteer during normal
clinic hours, dedicated to providing TLC
educational and related materials. Medical
personnel can also “refer” patients to TLC.
When patients and supports return for
the routine educational meeting (“family
meeting”), required for listing for transplantation, TLC provides a component
tools with a tabbed notebook for Medications, Lab Tests, To Do Lists, Medical
Records, and General Information. Other
materials consist of support team contact
and assigned duty outline, medical team
contact card sleeve, calendar, medication
charting tools, medication box, pill cutter, medication travel bag, thermometer,
pedometer, emergency medication key
fob, surgical masks, TLC button for social
experiment, hand sanitizer, “Play Your
ACES”a support materials, food safety
guide, transplant lifestyle information,
organ donation (Gift of Life) and registry
information, donor contact guidelines, and
tote bag. The TLC ambassador volunteer
reviews educational resources within the
toolkit in addition to answering or referring any questions of concern.
METHODS
Informal Program Evaluation
TLC has undergone continuous informal programmatic evaluation since its
inception in 2008. First, as part of the
kits provided to patients, there is a feedback form for suggestions to improve any
resources or processes. Second, as part of
a Patient Family Advisory Council, which
involves physicians, staff representation
from each hospital unit, and TLC ambassadors, all participating members provide
feedback and recommendations. For the
purposes of this article, the contributing
authors identified and reviewed the elements of TLC that were thought to have
The Permanente Journal/Perm J 2016 Summer;20(3):15-207
ORIGINAL RESEARCH & CONTRIBUTIONS
Lifestyle and Self-Management by Those Who Live It: Patients Engaging Patients in a Chronic Disease Model
a high level of impact on the feasibility and
sustainability of the group. The results of
the programmatic evaluation are in the
discussion section.
Patient and Support Feedback Evaluation
All data were collected with full institutional research and administrative approval. A patient and support satisfaction
survey was developed for the purposes of
this study to assess patient and support
satisfaction with TLC-related education.
The surveys were disseminated (via passive
consent; the cover letter that explained
completion of survey indicated consent)
before the TLC component of the routine educational meeting for listing for
transplant and were entirely anonymous
to maximize response rates. Respondents
were invited to return surveys either directly to staff or in a locked box located
within the clinic. Data collected in the
survey included basic demographic characteristics (sex, race/ethnicity), organ needing transplant, and whether the respondent
was the patient, primary caregiver, or other
support person. Respondents were then
asked to rate the TLC educational program
on length, helpfulness, understandability,
whether it met expectations for education, and confidence that the information
provided would help them navigate the
transplant process. They were assessed
for recall of basic information presented
in the TLC portion of the presentation
(eg, “What does ACES stand for?” and
asked to write in a response). Lastly, they
were given the opportunity to provide
Table 1. Characteristics of 823 respondents in study of Transplant Living Communitya
Characteristic
Sex
Men
Women
Hispanic/Latino
Yes
No
Prefer not to respond
Middle Eastern
Yes
No
Prefer not to respond
Race
American Indian or Alaskan Native
Black or African American
Other Pacific Islander
Asian
White
Other
Prefer not to respond
Multi-ethnic
Organ
Liver
Heart
Kidney
Pancreas
Lung
Liver/kidney
Kidney/pancreas
Other
Patients
(n = 217)
Primary caregivers
(n = 255)
Other supports
(n = 351)
130 (59.9)
72 (33.2)
56 (22.0)
188 (73.7)
140 (39.9)
201 (57.3)
9 (4.1)
176 (81.1)
5 (2.3)
10 (3.9)
209 (82.0)
5 (2.0)
11 (3.1)
305 (86.9)
2 (0.6)
5 (2.3)
172 (79.3)
4 (1.8)
4 (1.6)
209 (82.0)
5 (2.0)
2 (0.6)
310 (88.3)
3 (0.9)
2 (0.9)
70 (32.3)
1 (0.5)
2 (0.9)
127 (58.5)
5 (2.3)
1 (0.5)
5 (2.3)
—
57 (22.4)
1 (0.4)
4 (1.6)
174 (68.2)
2 (0.8)
2 (0.8)
8 (3.1)
5 (1.4)
64 (18.2)
1 (0.3)
1 (0.3)
256 (72.9)
6 (1.7)
8 (2.3)
4 (1.1)
112 (51.6)
—
94 (43.3)
2 (0.9)
1 (0.5)
3 (1.4)
2 (0.9)
2 (0.9)
171 (67.1)
1 (0.4)
66 (25.9)
1 (0.4)
1 (0.4)
3 (1.2)
2 (0.8)
1 (0.4)
285 (81.2)
—
52 (14.8)
—
—
4 (1.1)
1 (0.3)
—
Data are presented as number (% of category) unless otherwise noted. Within categories, columns do not consistently
add up to the total because of missing data.
— = no affirmative responses.
a
The Permanente Journal/Perm J 2016 Summer;20(3):15-207
qualitative feedback on what they liked the
best and least about the TLC portion of
the informational session. The assessment
is available online at: www.thepermanentejournal.org/files/15-207Appx1.pdf.
Analyses
Participant’s responses were compared
between groups by χ2 test for categorical variables and Kruskal-Wallis H test
for continuous variables. For qualitative
responses, 3 of the authors (ER, CW, and
MT) individually classified the responses
on the basis of content and assigned numerical labels to the comments (dummy
coding) corresponding to thematic content. Following dummy coding, all numerics were sent to another author (MJ), who
reviewed the data and selected scoring on
the basis of a majority of responses. For example, if 2 coders reported a statement was
a “2” but a third coder reported the statement was a “3,” the statement was coded
as a “2.” Frequencies of all codes were then
analyzed for frequency of content.
RESULTS
Patient Evaluation and Feedback
Surveys were collected from January
through November 2013. Of the 1862
surveys disseminated, 823 surveys were
returned (response rate, 44.2%). The mean
(standard deviation) age of patients was
54.1 (11.5) years, of primary supports was
51.97 (14.24) years, and of other supports
was 46.48 (16.22) years. Additional demographic and respondent characteristics are
presented in Table 1.
Table 2 provides the frequency of correct responses on defining compliance and
ACES. There was no significant difference
between respondent groups in defining
ACES but there was a significant difference in defining compliance, with patients
having the highest frequency of incorrect
responses.
A Kruskal-Wallis H test was run to
compare patients, primary supports, and
other supports on satisfaction with the
TLC presentation. There was a statistically significant difference on how confident respondents reported feeling after
meeting with the TLC ambassador (p =
0.002), with secondary supports reporting the highest confidence followed by
primary support and lastly patients. There
47
ORIGINAL RESEARCH & CONTRIBUTIONS
Lifestyle and Self-Management by Those Who Live It: Patients Engaging Patients in a Chronic Disease Model
were no significant differences between
respondent groups on expectations being
met (p = 0.699), information being easy
to follow and understand (p = 0.241),
whether the information presented will
help navigate the transplant process (p =
0.174), or length of the session (p = 0.364);
see Table 3.
For qualitative data, as scored above,
633 of the respondents (76.9%) wrote
in a reply for what they liked the most
about the TLC portion of the educational
session. Several respondents received
more than 1 code if the content of their
response addressed more than 1 thematic
area. Aspects of the program that generated the most frequent positive responses
are included in Table 4 (percentages are
out of those who provided qualitative
feedback). When asked what they liked
the least about the TLC portion of the educational session, 199 of the respondents
Table 2. Responses to survey about Attitude, Compliance, Exercise, and Support
in study of Transplant Living Communitya
Survey responses
What does compliance mean?
Responded correctly
Responded incorrectly
Did not respond
Attitudeb
Answered correctly
Answered incorrectly
Did not respond
Complianceb
Answered correctly
Answered incorrectly
Did not respond
Exerciseb
Answered correctly
Answered incorrectly
Did not respond
Supportb
Answered correctly
Answered incorrectly
Did not respond
a
b
Patients
(n = 217)
Primary caregivers
(n = 255)
Other supports
(n = 351)
171 (78.8)
39 (18.0)
7 (3.2)
219 (85.9)
32 (12.5)
4 (1.6)
308 (87.8)
32 (9.1)
11 (3.1)
0.008
173 (79.7)
3 (1.4)
41 (18.9)
188 (73.7)
9 (3.5)
58 (22.7)
266 (75.8)
11 (3.1)
74 (21.1)
0.462
171 (78.8)
4 (1.8)
42 (19.4)
191 (74.9)
6 (2.4)
58 (22.7)
271 (77.2)
10 (2.8)
70 (19.9)
0.820
172 (79.3)
1 (0.5)
44 (20.3)
189 (74.1)
5 (0.2)
61 (23.9)
272 (77.5)
4 (1.1)
75 (21.4)
0.500
169 (77.9)
3 (1.4)
45 (20.7)
183 (71.8)
4 (1.6)
68 (26.7)
256 (72.9)
13 (3.7)
82 (24.2)
0.163
p value
Data are presented as number (% of category). Percentages may not total 100 because of rounding.
Responses to the questions: What does ACES stand for?
Table 3. Respondent satisfaction with Transplant Living Communitya
Respondent satisfaction metrics
Adequate or not enough time in the TLC
information session
The information presented was helpful or very
helpful in managing the transplant process
The information presented was understandable
or very understandable and easy to follow
The TLC program met or exceeded expectations
Respondents were mostly or completely
confident they could navigate the transplant
process with the information provided by the
TLC ambassador
Patients
(n = 217)
201 (92.6)
Primary support
(n = 255)
235 (92.2)
Other supports
(n = 351)
332 (94.6)
204 (94.0)
240 (94.1)
323 (92.0)
211 (97.2)
243 (95.3)
335 (95.4%)
203 (93.5)
191 (88.0)
237 (92.9)
211 (82.7)
322 (91.7)
284 (80.9)
Data represent affirmative responses. Data are presented as number (% of category).
TLC = Transplant Living Community.
a
48
(24.2%) responded. Themes identified (in
order of frequency of occurrence) are also
reported in Table 4.
DISCUSSION
TLC is a unique, sustainable, patient-led
lifestyle and self-management educational
program providing a valuable resource for
organ transplantation patients and their
caregivers. Prior research has shown that
transplant patients report a lack of caregiver education and acknowledge the need
for distributed educational opportunities
during the course of transplant.5 The Institute of Medicine’s 2000 report32 called
for engaging and empowering patients
in health care. Since this seminal report,
patients are becoming more proactive consumers, actively participating in their care.
However, as others have outlined, practical
guidance on how to engage patients has
been limited.33-35 For patient engagement
to be successful, patient education must
address lifestyle skills. This education will
need to come from the patient’s perspective, complement medical care, and involve patients, caregivers, and extended
social support members. An example of
this approach, in which lifestyle methods
are applicable across many chronic disease
populations, is the TLC. Patients and supports reported high levels of satisfaction
with the lifestyle and self-management
skills presented by the TLC. Respondents
also frequently indicated appreciation
for having an actual transplant recipient
providing the information as they felt this
made the information more accessible and
gave them hope for the future. When asked
about possible improvements, most of the
responses indicated nothing, or provided
suggestions that were logistical or unrelated to TLC (eg, protocol requirements
for transplant).
An interesting finding was that patients
were significantly less likely to correctly
identify the components of compliance
than were primary or other supports. As
outlined in the introduction, end-stage
organ disease has a well-documented association with the development of cognitive
impairments.9-17 This underlines the importance of providing relatable lifestyle and
self-management education not only to the
patient but also to primary and secondary
supports throughout the care continuum.
The Permanente Journal/Perm J 2016 Summer;20(3):15-207
ORIGINAL RESEARCH & CONTRIBUTIONS
Lifestyle and Self-Management by Those Who Live It: Patients Engaging Patients in a Chronic Disease Model
Also interesting was that secondary supports reported the greatest confidence in
being able to manage the transplant process following the TLC education class.
For supports other than the patient’s primary support, the TLC lifestyle and selfmanagement education is often their first
exposure to the seriousness and extensive
nature of care for organ transplants. “Other
supports” often come in knowing only that
their relative or friend needs a transplant
and may have had minimal tangible support requirements placed on them. The
potential of secondary supports to be considered as integral support team members
to assist the primary support role has not
been explored and could be considered for
further research to determine the accuracy
of this interpretation.
There are a number of factors unique
to the TLC and considered integral to its
sustainability that would be useful in integrating a similar program. First, a “champion” or at least one person should be
dedicated to the program and its successful
integration into a multidisciplinary team.
Table 4. Frequency of qualitative
(themes) responses to “liked most” or
“liked least” about Transplant Living
Communitya
Theme for “liked most”
The volunteer/that the volunteer
was a transplant recipient
Information provided
Overall positive experience with
the program
Quality of the presentation
Have a reference for lifestylerelated questions
Theme for “liked least”
Disliked nothing
Aspects other than the TLC
presentation (eg, interruptions)
Inadequate time with TLC
Desired more information
Disliked the group format (would
have preferred individual)
Disliked requirements or
compliance factors related to
transplant
Disliked the individual presenting
359 (56.7)
195 (30.8)
69 (10.9)
66 (10.4)
21 (3.3)
136 (68.7)
23 (11.5)
12 (6.0)
10 (5.0)
9 (3.9)
8 (4.0)
5 (2.5)
Data are presented as number (% of those who
provided qualitative feedback for that theme).
TLC = Transplant Living Community.
a
The Permanente Journal/Perm J 2016 Summer;20(3):15-207
Transplant recipients have recognized the
value of patient-to-patient interaction.23
Secondly, a health care environment must
be receptive to integration of a patient-led
group with ongoing community development. Internally, a representative of
TLC attends the selection committee to
advocate for patients. TLC ambassadors
have been instrumental within the Patient Family Advisory Council, driving
the patient and family needs agenda with
staff in a structured fashion. Medical staff
trust has been developed and maintained
through continual dialogue, the provision
of a consistent curriculum, field mentoring of ambassadors, standardization of
lifestyle resources and related tools, and
routine practice of referring medical questions back to medical staff. Anecdotally,
TLC involvement has fostered positive
outcomes that reinforce ongoing trust
from medical staff. At our center, there
are several examples of patients who were
determined not to be transplant candidates
but, through interactions with TLC and its
tenants, were able to meet eligibility for
listing for organ transplantation. Third,
the program must be accessible and visible to patients, supports, and staff. TLC
has a centralized presence on the clinic
floor via an educational table full of resources manned by a TLC ambassador
in addition to TLC dedicated e-mail
and voicemail access. Fourth, a clearly
presented and manageable lifestyle plan
(“Play Your ACES”a) is needed. Related
information and resources are presented
in a clear and useful format accessible to
most patients. Resources (eg, informational packet, brochures) are routinely
evaluated and updated or improved to
maximize utility and accuracy. Lastly, a
strong volunteer structure with thoughtful
training/orientation contains the ultimate
objective of volunteers taking ownership
of the program. Transplant recipients are
invited to become ambassador volunteers
only after a minimum of ten months after
the transplant to ensure adequate physical and psychological recovery, wellness,
and stability.
This study has several limitations. First,
the assessment of the satisfaction of patients and supports was at a single time
point and therefore the level of satisfaction and information retained may be
different following repeated exposure (as
that is the TLC model) or the overall experience with the program. Second, there
is the potential for response bias. Patients
and their supports were asked to complete
the survey after an approximately threehour educational session, which owing to
patient fatigue or other factors may have
reduced our response size. Lastly, given
that TLC is a well-established community
of ambassadors integrated into the clinic
with patients routinely exposed to the
TLC group, whether TLC has a significant
impact on patient outcomes at this time
could not be determined. To ascertain
whether this is the case, randomized controlled trials would need to be performed.
Future research should attempt to parse
the effects of similar interventions on
patient-related outcomes. However, one
of the true strengths of this group is its
visibility and accessibility, suggesting a
multisite study with similar patient sociodemographic characteristics would be
an optimal strategy.
CONCLUSION
It is entirely feasible and sustainable to
integrate a patient-led lifestyle and selfmanagement educational group into a
busy tertiary care clinic for patients with
complex chronic illnesses. This requires
a receptive and supportive health care
environment, a coordinated and cohesive
patient volunteer structure, and continued
improvement. Furthermore, overwhelmingly positive feedback from patients and
their supports regarding such a group
suggest that these groups could provide
substantial benefits in the care of complex
illnesses. v
a
“Play Your ACES” is service marked. For those interested
in more information, please contact Elizabeth Rubinstein
at [email protected].
Disclosure Statements
The author(s) have no conflicts of interest to
disclose.
Acknowledgments
We thank the volunteers of Transplant Living
Community, the patients and supports who
completed the survey, the entire Transplant Institute
staff for their ongoing and exemplary care of
patients, and the Gift of Life Foundation and the
Benson Ford Endowment.
Mary Corrado, ELS, provided editorial assistance.
49
ORIGINAL RESEARCH & CONTRIBUTIONS
Lifestyle and Self-Management by Those Who Live It: Patients Engaging Patients in a Chronic Disease Model
Role of the Funding Source
Funding for the Transplant Living Community is
from a grant from the Gift of Life Foundation and
the Benson Ford Endowment for Transplantation.
There was no funding for the collection or analysis
of these data or the development of this article.
How to Cite this Article
Jesse MT, Rubinstein E, Eshelman A, et al. Lifestyle
and self-management by those who live it: Patients
engaging patients in a chronic disease model.
Perm J 2016 Summer;20(3):15-207. DOI:
http://dx.doi.org/10.7812/TPP/15-207.
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DOI: http://dx.doi.org/10.1371/journal.pone.0028313.
14. Parekh PI, Blumenthal JA, Babyak MA, et al;
INSPIRE Investigators. Gas exchange and exercise
capacity affect neurocognitive performance in
patients with lung disease. Psychosom Med
2005 May-Jun;67(3):425-32. DOI: http://dx.doi.
org/10.1097/01.psy.0000160479.99765.18.
15. Pegum N, Connor JP, Feeney GF, Young RM.
Neuropsychological functioning in patients with
alcohol-related liver disease before and after
liver transplantation. Transplantation 2011 Dec
27;92(12):1371-7. DOI: http://dx.doi.org/10.1097/
tp.0b013e3182375881.
16. Putzke JD, Williams MA, Rayburn BK, Kirklin JK,
Boll TJ. The relationship between cardiac
function and neuropsychological status among
heart transplant candidates. J Card Fail 1998
Dec;4(4):295-303. DOI: http://dx.doi.org/10.1016/
s1071-9164(98)90235-4.
17. Sauvé MJ, Lewis WR, Blankenbiller M,
Rickabaugh B, Pressler SJ. Cognitive impairments
in chronic heart failure: a case controlled study.
J Card Fail 2009 Feb;15(1):1-10. DOI: http://dx.doi.
org/10.1016/j.cardfail.2008.08.007.
18. Wilson EA, Wolf MS. Working memory and
the design of health materials: a cognitive
factors perspective. Patient Educ Couns 2009
Mar;74(3):318-22. DOI: http://dx.doi.org/10.1016/j.
pec.2008.11.005.
19. Wilson EA, Wolf MS, Curtis LM, et al. Literacy,
cognitive ability, and the retention of health-related
information about colorectal cancer screening. J
Health Commun 2010;15 Suppl 2:116-25. DOI: http://
dx.doi.org/10.1080/10810730.2010.499984.
20. Wolf MS, Curtis LM, Wilson EA, et al. Literacy,
cognitive function, and health: results of the LitCog
study. J Gen Intern Med 2012 Oct;27(10):1300-7.
DOI: http://dx.doi.org/10.1007/s11606-012-2079-4.
21. Hartmann M, Bäzner E, Wild B, Eisler I, Herzog W.
Effects of interventions involving the family
in the treatment of adult patients with chronic
physical diseases: a meta-analysis. Psychother
Psychosom 2010;79(3):136-48. DOI: http://dx.doi.
org/10.1159/000286958.
22. Haspeslagh A, De Bondt K, Kuypers D, Naesens M,
Breunig C, Dobbels F. Completeness and satisfaction
23.
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35.
with the education and information received by
patients immediately after kidney transplant: a mixedmodels study. Prog Transplant 2013 Mar;23(1):12-22.
DOI: http://dx.doi.org/10.7182/pit2013249.
Moloney S, Cicutto L, Hutcheon M, Singer L.
Deciding about lung transplantation: informational
needs of patients and support persons. Prog
Transplant 2007 Sep;17(3):183-92. DOI: http://dx.doi.
org/10.7182/prtr.17.3.k4x28156403g6735.
Myers J, Pellino TA. Developing new ways to
address learning needs of adult abdominal organ
transplant recipients. Prog Transplant 2009
Jun;19(2):160-6. DOI: http://dx.doi.org/10.7182/
prtr.19.2.2084g543676202j6.
Schmid-Mohler G, Schäfer-Keller P, Frei A, Fehr T,
Spirig R. A mixed-method study to explore patients’
perspective of self-management tasks in the early
phase after kidney transplant. Prog Transplant 2014
Mar;24(1):8-18. DOI: http://dx.doi.org/10.7182/
pit2014728.
Davis K, Schoen C, Schoenbaum SC. A 2020 vision
for American health care. Arch Intern Med 2000
Dec 11-25;160(22):3357-62. DOI: http://dx.doi.
org/10.1001/archinte.160.22.3357.
Davis K, Schoenbaum SC, Audet AM. A 2020 vision
of patient-centered primary care. J Gen Intern
Med 2005 Oct;20(10):953-7. DOI: http://dx.doi.
org/10.1111/j.1525-1497.2005.0178.x.
Funnell MM. Peer-based behavioural strategies
to improve chronic disease self-management and
clinical outcomes: evidence, logistics, evaluation
considerations and needs for future research. Fam
Prac 2010 Jun;27 Suppl 1:i17-22. DOI: http://dx.doi.
org/10.1093/fampra/cmp027.
Ashcroft P. Adapting patient education for potential
liver transplant recipients in a climate of chronic
donor organ shortfall. Prog Transplant 2009
Mar;19(1):59-63. DOI: http://dx.doi.org/10.7182/
prtr.19.1.k18316t43n071j31.
Armstrong N, Herbert G, Aveling EL, Dixon-Woods M,
Martin G. Optimizing patient involvement in quality
improvement. Health Expect 2013 Sep;16(3):e36-47.
DOI: http://dx.doi.org/10.1111/hex.12039.
Baldoni L, De Simone P, Paganelli R, et al. The “You
Are Not Alone” care program for liver transplantation.
Transplant Proc 2008 Jul-Aug;40(6):1983-5. DOI:
http://dx.doi.org/10.1016/j.transproceed.2008.05.066.
Institute of Medicine: Committee on Quality Health
Care in America. Crossing the quality chasm: a new
health system for the 21st century. Washington, DC:
National Academies Press; 2001 Mar 1.
Clancy CM. Paitient engagement in health care.
Health Serv Res 2011 Apr;46(2):389-93. DOI: http://
dx.doi.org/10.1111/j.1475-6773.2011.01254.x.
Coulter A. Patient engagement—what works? J
Ambul Care Manage 2012 Apr-Jun;35(2):80-9. DOI:
http://dx.doi.org/10.1097/jac.0b013e318249e0fd.
Gruman J, Rovner MH, French ME, et al. From
patient education to patient engagement: implications
for the field of patient education. Patient Educ
Couns 2010 Mar;78(3):250-6. DOI: http://dx.doi.
org/10.1016/j.pec.2010.02.002.
To Interact
It is our duty to remember at all times and anew that medicine is not only a science,
but also the art of letting our own individuality interact with the individuality of the patient.
— Albert Schweitzer, 1875-1965, French-German theologian, organist, philosopher, and physician
50
The Permanente Journal/Perm J 2016 Summer;20(3):15-207
credits available for this article — see page 112.
ORIGINAL RESEARCH & CONTRIBUTIONS
Special Report
Improving Care in Older Patients with Diabetes:
A Focus on Glycemic Control
Eric A Lee, MD; Nancy E Gibbs, MD; John Martin, MD; Fred Ziel, MD;
Jennifer K Polzin, PharmD; Darryl Palmer-Toy, MD, PhD
E-pub: 06/29/2016
Perm J 2016 Summer;20(3):15-080
http://dx.doi.org/10.7812/TPP/15-080
ABSTRACT
Diabetes affects more than 25% of Americans older than age
65 years. The medical care of older patients must differ from the
care of their younger counterparts. Older patients are at high
risk of drug toxicity. A hemoglobin A1c (HbA1c) level less than
7.0% has historically been the goal of all patients with diabetes,
regardless of age. Recent research has demonstrated that using
medications to achieve such tight glycemic control is not necessary and is often not safe.
This article discusses the seminal research findings that
strongly suggest that HbA1c goals should be relaxed in older
patients. The authors then recommend an age-specific and functionally appropriate HbA1c reference range for patients receiving
medications to improve glycemic control. Other interventions
are suggested that should make diabetes care safer in older
patients receiving hypoglycemic medications.
INTRODUCTION
Care of Older Adult Patients
The medical care of older patients must differ from the care
of their younger counterparts. Complications from “standard”
medical care are much more common in the geriatric population because of reduced reserve physiologic capacity, leading to
functional decline. For example, among the sickest patients—
hospitalized older patients—lasting disability is more common
compared with hospitalized younger patients because of at least
three mechanisms:
1.Incomplete recovery from a classic medical diagnosis (eg, oxygen dependence after pneumonia or chronic dyspnea after a
myocardial infarction)
2.Exacerbation of a preexisting geriatric syndrome (eg, heightened fear of falls caused by hospital-related deconditioning
with leg weakness or worsening dizziness caused by additional
polypharmacy from new medications)
3.Iatrogenic complications during a hospitalization (eg, nosocomial
Clostridium difficile colitis leading to nursing home placement
or hospital-acquired incident delirium leading to dementia).
Older patients are at high risk of drug toxicity. Because they
are more likely than younger patients to have multiple medical
problems, older patients take more medications, which often
leads to incorrect and unnecessary administration of prescribed
medications. Additionally, the metabolism of drugs is reduced
in older patients because of decreased lean body mass with increased body fat and a higher likelihood of having renal, hepatic,
and/or cardiac insufficiency. Finally, drug-drug and drug-disease
interactions make older patients at high risk of iatrogenic complications of drug toxicity.
“Overuse” of medications has been categorized as when the
benefits of the additional medication are negligible (eg, antibiotics for a sore throat), when the risks outweigh the benefits
(eg, muscle relaxant for neck pain), or use of a medication that
a competent patient would have otherwise declined after shared
decision making (eg, morphine for mild knee pain).1,2 Use of
hypoglycemic medications for the treatment of diabetes in older
patients using standard guidelines often fit all three categories
of “overuse.” The clinical benefits of additional hypoglycemic
medications are often minimal, the harms are common and
lasting, and the patient often lacks understanding of the time
needed to accrue benefits from hypoglycemic medications. Hypoglycemia occurs frequently in older patients with diabetes,
more often contributing to functional decline and lasting disability compared with their younger counterparts. The goals of
glycemic control and the treatment using hypoglycemic diabetic
medications in patients with diabetes must differ depending on
age and functional status.
Diabetes Care in Older Adult Patients
Since 2003, there has been general acceptance by geriatricfocused physicians that glycemic control should be tempered
by a sense of life expectancy, goals of care, cognitive status, and
physical functional status.3 The one-size-fits-all model is not appropriate in frail older patients receiving hypoglycemic medications, for whom the risks of these medications often outweigh
their benefits. Rather, shared decision making is necessary.
Eric A Lee, MD, is the Assistant Chief of Internal Medicine at the West Los Angeles Medical Center and Co-Chair of the Southern California
Permanente Medical Group High Risk Drugs in the Elderly Committee in Pasadena. E-mail: [email protected]. Nancy E Gibbs, MD, is the
former Regional Coordinating Chair for Geriatrics and Continuing Care for Kaiser Permanente Southern California and Co-Chair of the
Southern California Permanente Medical Group High Risk Drugs in the Elderly Committee in Pasadena. E-mail: [email protected].
John Martin, MD, is an Internist at the Los Angeles Medical Center and Co-Director of the Southern California Permanente Medical Group
Diabetes Complete Care Program in Pasadena. E-mail: [email protected]. Fred Ziel, MD, is the Physician-in-Charge of Endocrinology at
the Woodland Hills Medical Center in CA and the Regional Coordinating Chair for Endocrinology for Kaiser Permanente Southern California.
E-mail: [email protected]. Jennifer K Polzin, PharmD, is the former Clinical Operations Senior Pharmacy Consultant for Medication
Management and Safety for the Southern California Permanente Medical Group in Pasadena. Darryl Palmer-Toy, MD, PhD, is the Medical
Director of the Regional Reference Laboratories and the Regional Assistant Medical Director of Laboratory Services for the Southern
California Permanente Medical Group in Pasadena. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-080
51
ORIGINAL RESEARCH & CONTRIBUTIONS
Improving Care in Older Patients with Diabetes: A Focus on Glycemic Control
Historically, glycemic goals target a hemoglobin A1c (HbA1c)
level below 7.0% without differentiation by age. The 2013
American Association of Clinical Endocrinologists (AACE) executive summary for diabetes management states that the HbA1c
goal is 6.5% or lower for healthy patients without concurrent
illness and who are at low hypoglycemic risk.4 The AACE states
that the goal should be individualized to an HbA1c measurement
above 6.5% for patients with concurrent illness and who are
at risk of hypoglycemia.4 Although this AACE position states
that the goals should be individualized on the basis of age and
comorbidity, guidance on comorbidity criteria is absent. We
believe that the lack of clarity in the AACE’s statement perpetuates the “lower-is-better” myth and encourages the overuse of
potentially dangerous hypoglycemic medications.
The American Diabetes Association’s (ADA’s) 9-page executive
summary of its 67-page position statement, “Standards of Medical Care in Diabetes 2014,” states that an HbA1c under 7.0% is
“a reasonable goal” for many nonpregnant patients.5 Also, the
ADA recommends that “older adults who are functional, cognitively intact, and have significant life expectancy should receive
diabetes care with goals similar to those developed for younger
adults” and that “glycemic goals for some older adults might
reasonably be relaxed, using individual criteria, but hyperglycemia leading to symptoms or acute hyperglycemic complications
should be avoided … .”5 Like the 2013 AACE executive summary, the 2014 ADA executive summary possibly lacks proper
guidance for clinicians on when HbA1c goals should be relaxed.
However, in the text of the ADA’s 2014 position statement,
HbA1c goals of below 7.5%, below 8.0%, and below 8.5% are
recommended for older patients who have, respectively, good
health, complex/intermediate health, and very complex/poor
health.6 This recommendation is more aligned with the position
of the American Geriatrics Society (AGS), in which the target
goal is set for an HbA1c between 7.5% and 8.0% in most older
patients, and higher HbA1c targets between 8.0% and 9.0%
are recommended with multiple comorbidities, poor health,
and limited life expectancy. 7 These recommendations from
the AGS have been adopted and publicized by the “Choosing
Wisely” campaign sponsored by the American Board of Internal Medicine (ABIM) Foundation.8 On the basis of results of
pivotal historical trials, we strongly agree with the glycemic goal
of having HbA1c below 7.0% in most patients under 65 years
of age. In this article, we discuss the scientific foundation for
treating hyperglycemia to the historic goal of less than 7.0% in
patients older than age 65 years (still generally considered the
threshold for proper glycemic control in patients with diabetes
of all ages), and why we believe that these goals should be relaxed
to the standards set by the AGS.
Historical Context for Lower Glycemic Targets
The Diabetes Control and Complications Trial (DCCT) was
the first trial to establish that microvascular and macrovascular
complications of hyperglycemia could be delayed with tighter
glycemic control. In this seminal work published in 1993, a total
of 1441 patients with Type 1 diabetes (mean age = 27 years),
with and without microvascular complications, were randomly
52
assigned to receive either standard control of blood glucose or intensive control (intervention). After an average follow-up of 6.5
years, the DCCT (conducted from 1983 to 1993) demonstrated
that patients with tight glycemic control had a delay in onset
(primary prevention) or progression (secondary prevention) of
nephropathy, neuropathy, and retinopathy.9 The intervention
group had a mean HbA1c of 7.4%; the conventional treatment
group had a mean HbA1c of 9.1%. The 11-year, postintervention follow-up published in 2005 showed a 42% reduction in
any cardiovascular disease event.10 (In 2004, the mean HbA1c
in the intervention group was 7.9% compared with 7.8% in
the control group.10) Notably, the widespread applicability of
the DCCT investigators’ conclusions to most patients with diabetes was properly questioned.11 Less than 10% of all patients
with diabetes have Type 1 diabetes, and the pathophysiology
of Type 1 diabetes (formerly called juvenile diabetes) is markedly
different from that in most patients with Type 2 (formerly called
adult-onset) diabetes, particularly those older than 65 years.
The UK Prospective Diabetes Study (UKPDS), whose results
were published in 1998, attempted to mitigate these concerns
and validate the importance of tight glycemic control in patients
with Type 2 diabetes.12 In this study, 3867 patients with newly
diagnosed Type 2 diabetes (mean age = 54 years) were randomly
given intensive therapy or conventional treatment. Patients
older than age 65 years were excluded from enrollment in the
UKPDS.12 After 10 years of follow-up, the intensive therapy
group (mean HbA1c = 7.0%) had delays in microvascular complications, with less retinopathy and nephropathy compared
with those who received conventional treatment (mean HbA1c
= 7.9%).12 Macrovascular complications were not shown to be
prevented or delayed during the initial publication in 1998.
After the end of the randomization of the 2 groups, shortly
after the 1998 publication, the glycemic control equalized in both
study groups. The 10-year postsurveillance results of the UKPDS,
published in 2008, suggested there was a “legacy effect,” or longdelayed benefit, in preventing myocardial infarctions and death
in the intensive therapy group compared with the conventional
group.13 Earlier intensive glycemic control during the first 10
years after the diagnosis of diabetes could reduce macrovascular events 10 to 19 years later, the study found. The UKPDS
influenced the adoption of HbA1c goals below 7.0% in adult
patients with Type 2 diabetes.
Fallacy of Applying these Studies to Older Adult Patients
In 2014, Selvin et al14 published data from the National
Health and Nutrition Examination Survey (NHANES, conducted by the Centers for Disease Control and Prevention).
The authors labeled patients with diabetes of all ages who received hypoglycemic medications and had an HbA1c of 7.0%
or greater as being suboptimally controlled.14 We think that an
HbA1c below 7.0% should not necessarily be the goal in older
patients with diabetes receiving hypoglycemic medications, and
conclusions from influential articles such as NHANES mislead
both clinicians and older patients with diabetes, potentially leading to harm. In NHANES, 40% of the patients with diabetes
were older than age 65 years. We know that up to 57% of older
The Permanente Journal/Perm J 2016 Summer;20(3):15-080
ORIGINAL RESEARCH & CONTRIBUTIONS
Improving Care in Older Patients with Diabetes: A Focus on Glycemic Control
patients with diabetes have substantial comorbidities and geriatric syndromes, which often leads these patients to change their
goals of medical care.15 Given the known reduced life expectancy
in older patients, particularly in frail older patients, we believe
that the age-neutral historic target of an HbA1c below 7.0% is
fallacious. This target is based on results of studies (UKPDS
and DCCT) that did not allow for enrollment of patients aged
65 years or older, and hence these glycemic goals should not
translate to older patients.
The microscopic complications related to higher HbA1c concentrations may not be clinically relevant in older patients with
new-onset diabetes. In a theoretical construct model comparing
an HbA1c of 8.0% vs 7.0% in patients with the onset of diabetes
at age 65 years, the additional lifetime risk of blindness caused
by retinopathy was reduced by 0.2% (number needed to treat
= 500) and the additional lifetime risk of end-stage renal disease was reduced by 0.2% (number needed to treat = 500).16
Therefore, the clinical significance of preventing microvascular
disease is questionable. Later, the UKPDS showed that tight
glycemic control might reduce the development of macrovascular disease by 10 to 19 years, but in a patient with limited
life expectancy or onset of diabetes after the age of 65 years,
the relevance of aggressive lowering of glucose levels becomes
less clear. Furthermore, if microalbuminuria portends future
macrovascular complications, the control of hypertension and
hyperlipidemia with the appropriate use of cardioprotective
medications (aspirin, angiotensin-converting enzyme inhibitors,
and statins) plays an equal if not a more important role in the
prevention of cardiovascular complications.
For older adult patients with long-standing diabetes and
multiple medical problems, at least 3 randomized trials have
demonstrated that an HbA1c of about 7.5% is appropriate and
safe and that an HbA1c below 6.5% might be dangerous. The
Action to Control Cardiovascular Risk in Diabetes (ACCORD)
trial published in 2008 assessed 10,251 patients (mean age =
62 years; average duration of diabetes = 10 years) with multiple
comorbidities who received intensive treatment (mean HbA1c
= 6.4%) or conventional therapy (mean HbA1c = 7.5%).17 The
study was halted prematurely after 3.5 years because it showed
that there was one additional death in the intervention group
for every 95 patients over 3.5 years. In addition, 10% of the
intervention group had hypoglycemic events that required
medical assistance vs 3% for the control group, and 28% of the
intervention group had more than 10-kg weight gain compared
with 14% in the control group.17
Also in 2008, the Action in Diabetes and Vascular Disease:
Preterax and Diamicron Modified Release Controlled Evaluation
(ADVANCE) trial took place in 11,140 older patients (mean
age = 66 years; average duration of diabetes = 8 years) with severe cardiovascular disease or cardiovascular disease risk factors or
preexisting microvascular complications.18 The ADVANCE trial
found no macrovascular benefit or increased rate of death in the
intense treatment group (mean HbA1c = 6.5%) vs conventional
therapy (mean HbA1c = 7.3%) after 5 years. Severe hypoglycemia was significantly more common in the intervention group
(2.7% vs 1.5% in the control group), which contributed to the
The Permanente Journal/Perm J 2016 Summer;20(3):15-080
significantly increased rate of hospitalization in the intervention
group. The only microvascular benefit with intense treatment was
a statistically significant reduction in albuminuria.18 In 2014, the
follow-up study in ADVANCE demonstrated no reduction in
macrovascular disease after the 6-year, postsurveillance followup. The legacy effect in preventing macrovascular disease seen
in the UKPDS was not seen in ADVANCE.19
In 2009, the Veterans Affairs Diabetes Trial assessed 1791
military veterans with suboptimally controlled Type 2 diabetes
(mean age = 60 years; mean duration of diabetes mellitus = 11.5
years; 40% with vascular disease).20 The goal in the intervention group receiving intensive glucose control was to reduce
the HbA1c by 1.5%. After 6 years, there were significantly
more serious events in the intervention group (mean HbA1c =
6.9%), including hypoglycemia, vs the controls (mean HbA1c
= 8.4%), which received standard glucose control. There were
no statistically significant changes in composite microvascular
outcomes, although a statistically significant reduction did occur in the progression of proteinuria. No statistical differences
existed in the number of eye surgical procedures, but there was
a trend for reduced retinopathy. There also were no significant
reductions in macrovascular events (stroke, cardiac events and
procedures) or amputations in the intervention group compared
with the control group.20
… the age-neutral historic target of an HbA1c below
7.0% is fallacious [and] based on results of studies
… that did not allow for enrollment of patients
aged 65 years or older, and hence these glycemic
goals should not translate to older patients.
Complications of Hypoglycemia
In 2011, the second most likely medication leading an older
patient to be hospitalized through the Emergency Department
because of an adverse drug event was insulin, and the fourth most
likely medication was an oral hypoglycemic agent, according to
authors from the Centers for Disease Control and Prevention.21
This group estimated that the numbers of hospitalizations in older
patients occurring annually in the US because of insulin and oral
hypoglycemic agents were 13,854 and 10,656 respectively. More
than 94% of these hospitalizations were caused by complications
of hypoglycemia, clearly demonstrating the potential dangers
of these endocrine agents. This same group later published that
patients older than age 80 years who were receiving insulin were
twice as likely to go to the Emergency Department and 5 times as
likely to be hospitalized because of insulin-related hypoglycemia
and errors compared with 45- to 64-year-old patients, suggesting
the need for looser glycemic targets based on age.22
Kaiser Permanente Northern California (KPNC) data showed
that hypoglycemia was the second most common nonfatal diabetic
complication (after cardiovascular complications) in patients age
70 to 79 years with a duration of diabetes for more than 10 years
and the third most common cause of nonfatal complications in
patients with diabetes for less than 10 years (after cardiovascular
53
ORIGINAL RESEARCH & CONTRIBUTIONS
Improving Care in Older Patients with Diabetes: A Focus on Glycemic Control
complications and eye disease).23 Additionally, among patients age
70 to 79 years, the incidence of hypoglycemia was 6 times more
likely than acute hyperglycemic events in those who had diabetes
for less than 10 years, and 19 times more likely in patients with
diabetes for greater than 10 years.23
As noted earlier, whether macrovascular disease can be prevented with tight glycemic control among older patients with a longstanding history of diabetes is questionable. Hypoglycemia might
also increase the risk of dementia later in life.24 In a KPNC diabetic
registry from 1980 to 2007, of 16,667 patients with a mean age
of 65 years, 1465 patients had at least 1 visit to the Emergency
Department or hospital for a hypoglycemic event. The absolute
risk in these patients of dementia developing per year of followup was 2.3%.25 Other KPNC data showed that hypoglycemia
Table 1. Kaiser Permanente Southern California’s electronic
medical record flag for elevated hemoglobin A1c in patients
with diabetes, used through December 2015a
Age
All agesb
High flag
(HbA1c, %)
≥ 7.0
Comments
Actual blood glucose measurements may differ
from the estimated average glucose because
of differences in test timing, stability of glycemic
control, and RBC lifespan
As of October 12, 2012, a separate test was created in Kaiser Permanente Southern
California for screening patients who did not have a diagnosis of diabetes. The
reference range for that test is 4.8% to 5.6%.
b
Patients of all ages were flagged as having elevated blood glucose levels if HbA1c
measurement was ≥ 7.0%.
HbA1c = hemoglobin A1c; RBC = red blood cell.
a
Table 2. Kaiser Permanente Southern California’s updated
hemoglobin A1c reference range for different age bandsa
Age,
years
≤ 17
High flag
(HbA1c, %)
≥ 7.5
18-64
≥ 7.0
65-75
≥ 7.5
≥ 76
≥ 8.0
Comments
Actual blood glucose measurements may differ
from the estimated average glucose because
of differences in test timing, stability of glycemic
control, and RBC lifespan
A less stringent HbA1c goal of < 8.0% may
be appropriate for an individual patient with
a history of severe hypoglycemia, limited
life expectancy, advanced microvascular or
macrovascular complications, or extensive
comorbid conditions
A less stringent HbA1c goal of < 9.0% may be
appropriate for an individual elderly patient with
a history of severe hypoglycemia, advanced
microvascular or macrovascular complications,
or extensive comorbid conditions
Convened by the manuscript’s authors, multiple relevant Kaiser Permanente Southern
California committees assisted in updating the HbA1c (diabetic monitoring) reference
range. The consensus reference range is shown here. In use since January 2016, this
updated reference range has been flagged as abnormal at an HbA1c level of ≥ 7.5%
in patients with diabetes between 65 and 75 years of age and has been flagged
as abnormal at an HbA1c ≥ 8.0 in patients with diabetes ≥ 76 years of age. The
corresponding comments will allow clinicians to choose a more tailored HbA1c goal on
the basis of the patient’s function and comorbidities.
HbA1c = hemoglobin A1c; RBC = red blood cell.
a
54
(as well as geriatric syndromes) more negatively affects an older
patient’s quality of life than do other diabetic complications (eg,
neuropathy, blindness, and end-stage renal disease).26
Hypoglycemia Continues in Older Patients
As already discussed, the literature shows that an unexpected
higher death rate was found in the intervention group of the
ACCORD study and that hypoglycemic agents often lead to
emergent hospitalizations in older patients, with hospitalizations
frequently leading to lasting disability. Other research showed
that older patients with multiple comorbid conditions and longstanding diabetes with an HbA1c between 6.4% and 6.9% did
not have improved macrovascular outcomes or clinically significant improved microvascular outcomes compared with those
with an HbA1c of 7.3% to 8.1%. Given this body of evidence,
the physician mantra of “do no harm” would suggest that only
a small percentage of patients older than 65 years would have an
HbA1c below 7.0% and be receiving hypoglycemic medications.
Yet, in published KPNC data, of 9786 patients between age 70
and 79 years with a duration of diabetes mellitus for longer than
10 years, 41% had an HbA1c below 7.0%.23 Although only 7%
of these patients were not receiving any hypoglycemic medication, 61% of these patients were on a regimen of a sulfonylurea
and 39% were receiving insulin.23
In a Veterans Affairs study in 2009 of 205,857 patients at
high risk of hypoglycemia because of age older than 74 years,
a creatinine level above 2.0 mg/dL, or presence of cognitive
impairment while receiving a sulfonylurea and/or insulin, 50%
of patients had a level of HbA1c under 7.0%, 27% had HbA1c
below 6.5%, and 11% had HbA1c less than 6.0%.27 These findings suggest overtreatment with hypoglycemic medications.
DISCUSSION
Many hypoglycemic episodes are avoidable. Many patients
may not know to take less hypoglycemic medication when their
oral intake is reduced (because of, for example, poor access to
food caused by an acute medical event such as an upper respiratory tract infection with consequent anorexia). All clinicians,
while educating older adult patients with diabetes, should instruct them to reduce their hypoglycemic agents during times
of poor nutritional intake and to carry candy and a glucagon
injection with them in the event of a hypoglycemic episode. The
first-line treatment of most diseases should be education and
other nonpharmaceutical interventions. In Kaiser Permanente
Southern California (KPSC), patients with diabetes mellitus
have better glycemic control if they have taken health education classes at KPSC (personal communication; Ray Nanda,
MD; 2016 Feb 22).a
There may be financial ramifications to overtreatment with
hypoglycemic agents. Medicare has been reducing reimbursements for care because of events thought to be avoidable (“never
events” during a hospitalization or readmission). In 2012, it was
estimated that in the US there was $213 billion of avoidable
health care costs, of which $20 billion in costs were caused by
medication errors and $1.3 billion was caused by mismatched
polypharmacy in elderly individuals.28 Given the alarming rate
The Permanente Journal/Perm J 2016 Summer;20(3):15-080
ORIGINAL RESEARCH & CONTRIBUTIONS
Improving Care in Older Patients with Diabetes: A Focus on Glycemic Control
of possible overtreatment with hypoglycemic agents in older
patients, the US Department of Health and Human Services
is developing a National Action Plan for Adverse Drug Event
Prevention that focuses on 3 classes of medications: opiates,
warfarin, and hypoglycemic agents.29
We believe that the excessive burdens such as hypoglycemic
episodes and other adverse medication reactions can be reduced
through the following multi-interventional approach:
1.Establish a new reference range for HbA1c levels in older
patients with diabetes that synthesize the recommendations
from the ADA, Choosing Wisely (sponsored by the ABIM
Foundation), and the AGS.
2.Educate and encourage clinicians to reduce hypoglycemic
medications in older patients at risk of functional loss or with
multiple medical problems when their HbA1c level is below
7.0%. Accounting for risks of polypharmacy and the goals of
care, for a healthy older patient with diabetes and an HbA1c
level below 7.0%, prescribing metformin as the only agent
may be appropriate. There is importance in using antidiabetes
medications to reduce glucose burden because hyperglycemia
can also cause substantial morbidity. Our (KPSC) updated
reference range can guide physicians to prescribe on the basis
of function and morbidity (Tables 1 and 2).
3.Prescribe metformin as the first-line agent when a physician
initiates therapy with a hypoglycemic medication because of
its low risk for hypoglycemia and its safety profile.
4.Use the electronic medical record to identify patients receiving
hypoglycemic agents who have an HbA1c level below 7.0%
and who are older than 80 years old or who have dementia
or chronic kidney disease stage 4 or greater.
5.Educate patients and caretakers, as well as provide written
instruction after the office visit, to decrease the dosing of
hypoglycemic medications when the patient’s oral intake is
reduced because of illness or poor access to food.
6.Prescribe glucagon for older patients with diabetes receiving
hypoglycemic medications, which can be used emergently
during symptoms of hypoglycemia.
7.Encourage older patients with diabetes who are receiving
hypoglycemic medications to always carry glucose tablets
or glucose-rich foods with them and to monitor their blood
glucose level before driving.
8.Use the electronic medical record to identify older patients receiving hypoglycemic medications who have 2 consecutive HbA1c
measurements below 6.5% in a period longer than 1 month.
By implementing the proposed interventions to reduce hypoglycemia, we can keep older patients with diabetes safer and
more functional, without having any clinically significant health
consequences from less intensive glycemic control. v
a
Chair of Health Education and Promotion, Kaiser Permanente Southern California,
Pasadena, CA.
Disclosure Statement
The author(s) have no conflicts of interest to disclose.
The Permanente Journal/Perm J 2016 Summer;20(3):15-080
Acknowledgments
The authors would like to thanks the following Kaiser Permanente (KP)
Southern California (KPSC) physicians: Jeffrey Brettler, MD (Assistant Area
Medical Director, KP West Los Angeles [LA]); Richard Chen, MD (Physican
Lead, Health Connect Clinical Content Lead and Decision Support, KPSC);
Howard Fullman, MD (Area Medical Director, KP West LA); Timothy Ho, MD
(Regional Assistant Medical Director, Quality and Clinical Analysis, KPSC);
Kisung Steve Hong, MD (Regional Coordinating Chair of General Internal
Medicine, KPSC); Michael Kanter, MD (Regional Medical Director of Quality
& Clinical Analysis, KPSC); Gregorio Saccone, MD (Regional Physician
Director, Health Connect Communications, KPSC); Steve Steinberg, MD
(Regional Coordinating Chair for Family Medicine, KPSC) for their lively
discussion and integral involvement in re-evaluating the glycemic goals of
older adults with diabetes. Without their support, the KPSC updated agebanded HbA1c reference range would not have been released.
Kathleen Louden, ELS, of Louden Health Communications provided editorial
assistance.
How to Cite this Article
Lee EA, Gibbs NE, Martin J, Ziel F, Polzin JK, Palmer-Toy D. Improving care
in older patients with diabetes: a focus on glycemic control. Perm J 2016
Summer;20(3):15-080. DOI: http://dx.doi.org/10.7812/TPP/15-080.
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Duckworth W, Abraira C, Moritz T, et al; VADT Investigators. Glucose control and
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Budnitz DS, Lovegrove MC, Shehab N, Richards CL. Emergency hospitalizations for
adverse drug events in older Americans. N Engl J Med 2011 Nov 24;365(21):200212. DOI: http://dx.doi.org/10.1056/nejmsa1103053.
22. Geller AI, Shehab N, Lovegrove MC, et al. National estimates of insulinrelated hypoglycemia and errors leading to emergency department visits and
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org/10.1001/jamainternmed.2014.136.
23. Huang ES, Laiteerapong N, Liu JY, John PM, Moffett HH, Karter AJ. Rates of
complications and mortality in older patients with diabetes mellitus: the diabetes
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org/10.1001/jamainternmed.2013.12956.
24. Yaffe K, Falvey CM, Hamilton N, et al; Health ABC Study. Association between
hypoglycemia and dementia in a biracial cohort of older adults with diabetes mellitus.
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jamainternmed.2013.6176.
25. Whitmer RA, Karter AJ, Yaffe K, Quesenberry CP Jr, Selby JV. Hypoglycemic
episodes and risk of dementia in older patients with type 2 diabetes mellitus. JAMA
2009 Apr 15;301(15):1565-72. DOI: http://dx.doi.org/10.1001/jama.2009.460.
26. Laiteerapong N, Karter AJ, Liu JY, et al. Correlates of quality of life in older adults with
diabetes: the diabetes & aging study. Diabetes Care 2011 Aug;34(8):1749-53. DOI:
http://dx.doi.org/10.2337/dc10-2424.
27. Tseng CL, Soroka O, Maney M, Aron DC, Pogach LM. Assessing potential glycemic
overtreatment in persons at hypoglycemic risk. JAMA Intern Med 2014 Feb
1;174(2):259-68. DOI: http://dx.doi.org/10.1001/jamainternmed.2013.12963.
28. Aitken M. Avoidable costs in US healthcare: the $200 billion opportunity from using
medicines more responsibly [Internet]. Danbury, CT: IMS Health Incorporated; c2016
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ADE-Action-Plan-508c.pdf.
Attending to Old People
Not only physicians, but everybody else attending old people,
being accustomed to their constant complaints, and knowing
their ill-tempered and difficult manners, realize how noble
and important, how serious and difficult, how useful and
even indispensable is that part of practical Medicine, called
Gerocomica, which deals with the conservation of old people
and the healing of their diseases.
—François Ranchin, MD, 1564-1641, French physician and professor
and chancellor of the Université de Médecin, Montpelier, France
56
The Permanente Journal/Perm J 2016 Summer;20(3):15-080
credits available for this article — see page 112.
ORIGINAL RESEARCH & CONTRIBUTIONS
Special Report
Evidence-Based Workflows for Thyroid and Parathyroid Surgery
Charles Meltzer, MD; Amer Budayr, MD; Annette Chavez, MD; Richard Dlott, MD; William Greif, MD;
Deepak Gurushanthaiah, MD; Andrew Klonecke, MD; Matthew Lando, MD; Joyce Leary, MD;
Sundeep Nayak, MD; Ryan Niederkohr, MD; Judith Park, MD; Alison Savitz, MBA, MD; Henry Schwartz, MD
E-pub: 07/29/2016 Perm J 2016 Summer:20(3):16-035
http://dx.doi.org/10.7812/TPP/16-035
ABSTRACT
A need exists to reduce care variations by standardizing the
practice of thyroid and parathyroid surgery. During the course of
a year, a task force developed algorithms representing decision
points and workflows based on American Thyroid Association
guidelines and three internal studies of surgical practices in the
Northern and Southern California Regions of Kaiser Permanente
conducted in collaboration with Health Information Technology
Transformation & Analytics (HITTA).
INTRODUCTION
In keeping with a movement toward specialty redesign based
on standardization and subspecialization, workflows were
developed between March 2015 and March 2016 to guide
evidence-based best practices and reduce disparities in care.
The evidence base for thyroid and parathyroid workup and
surgical procedures includes American Thyroid Association
(ATA) guidelines1 and three studies2-3 of surgical practices in
Kaiser Permanente (KP) Northern California and KP Southern
California conducted in collaboration with Health Information
Technology Transformation & Analytics (HITTA).
The first study used a robust set of variables and propensity
score methods to match 2362 patients undergoing hemithyroidectomy, total thyroidectomy, or parathyroidectomy as
outpatients (discharge within 8 hours of completion) to 2362
patients undergoing the same procedures as inpatients.2 Outcomes assessed were 30-day rates of complications, Emergency
Department visits, all-cause hospital readmissions, and mortality. No statistically significant differences between inpatients and
outpatients were found for complication rates or postdischarge
utilization, and we concluded that outpatient surgery should
be used for all patients for whom it is appropriate.2
The second study used similarly robust variables and propensity score methods to match 3135 patients who underwent
hemithyroidectomy and total thyroidectomy, or parathyroidectomy performed by a high-volume surgeon (> 40 cases per
year) to 3135 patients with the same procedure performed by
a low-volume surgeon (≤ 20 cases per year).3 Rates of all-cause
30-day complications, mortality, readmission, and Emergency
Department visits; proportion of outpatient procedures; incision-to-closure (“cut-to-close”) time; and length of stay were
assessed. For hemithyroidectomies, high-volume surgeons had
fewer readmitted patients, more outpatient procedures, shorter
lengths of stay, and shorter cut-to-close times. For total thyroidectomies, high-volume surgeons had lower rates of all surgeryrelated complications and of the individual complications of
hypocalcemia and surgical site infections, more outpatient
procedures, and shorter lengths of stay and cut-to-close times.
We concluded that high-volume surgeons improve patient safety
and have the potential to contribute to organizational efficiency
that may be underutilized in some settings.
The third study used decision-tree analysis to identify patientlevel characteristics associated with 30-day complications after
thyroid and parathyroid surgery.4 Among patients undergoing
thyroidectomies, the most important predictor of risk was thyroid cancer. For patients with thyroid cancer, additional risk
predictors included coronary artery disease and central neck
dissection. For patients without thyroid cancer, additional risk
predictors included coronary artery disease, dyspnea, complete
thyroidectomy, and lobe size. Among patients undergoing
parathyroidectomies, the most important risk predictor was
coronary artery disease, followed by cerebrovascular disease and
chronic kidney disease.3
Summaries of the evidence-based workflows are presented here.
THYROID NODULE: WORKUP
Figure 1 diagrams the workup of the patient with thyroid
nodules. Thyroid nodules are evaluated to rule out cancer and
rarely to address local symptoms. Palpable thyroid nodules are
uncommon. Nonpalpable nodules are identified frequently on
imaging studies. Thyroid nodule evaluation requires a dedicated
ultrasound examination of the thyroid and adjacent lymph
nodes. Whereas most nodules are benign, clinically significant
thyroid cancer is seen in a small minority of patients, and surgical treatment may be necessary. Nearly all thyroid cancers are
differentiated (papillary, follicular, or mixed).
Charles Meltzer, MD, is the Regional Chair of Chiefs of Head and Neck Surgery for The Permanente Medical Group in Oakland, CA.
E-mail: [email protected]. Amer Budayr, MD, is an Endocrinologist at the Oakland Medical Center in CA. E-mail: [email protected].
Annette Chavez, MD, is a General Surgeon at the Santa Clara Medical Center in CA. E-mail: [email protected]. Richard Dlott, MD, is an
Endocrinologist at the Walnut Creek Medical Center in CA. E-mail: [email protected]. William Greif, MD, is a General Surgeon at the Walnut Creek
Medical Center in CA. E-mail: [email protected]. Deepak Gurushanthaiah, MD, is an Otolaryngologist at the Oakland Medical Center in CA.
E-mail: [email protected]. Andrew Klonecke, MD, is a Nuclear Medicine Specialist at the Sacramento Medical Center in CA.
E-mail: [email protected]. Matthew Lando, MD, is an Otolaryngologist at the Union City Medical Center in CA. E-mail: [email protected].
Joyce Leary, MD, is an Endocrinologist at the Sacramento Medical Center in CA. E-mail: [email protected]. Sundeep Nayak, MD, is a Diagnostic
Radiologist and Nuclear Medicine Physician at the San Leandro Medical Center in CA. E-mail: [email protected]. Ryan Niederkohr, MD, is the
Chief of Nuclear Medicine at the Santa Clara Medical Center in CA. E-mail: [email protected]. Judith Park, MD, is a General Surgeon at the
Richmond Medical Center in CA. E-mail: [email protected]. Alison Savitz, MBA, MD, is a General Surgeon at the Walnut Creek Medical Center in
CA. E-mail: [email protected]. Henry Schwartz, MD, is an Endocrinologist at the Santa Rosa Medical Center in CA. E-mail: [email protected]
The Permanente Journal/Perm J 2016 Summer:20(3):16-035
57
ORIGINAL RESEARCH & CONTRIBUTIONS
Evidence-Based Workflows for Thyroid and Parathyroid Surgery
Figure 1. Thyroid nodule: Workup (full-size, color version available at: www.thepermanentejournal.org/files/Summer2016/16035-1.pdf).
Consider observation alone depending on patient characteristics, comorbidities, and imaging features.
Bethesda System for Reporting Thyroid Cytopathology categories: I = nondiagnostic or unsatisfactory; II = benign; III = atypia of unknown significance;
IV = follicular neoplasm or suspicious; V = suspicious for malignancy; VI = malignant.
AUS = atypia of unknown significance; CT = computed tomography; FNA = fine-needle aspiration; I = iodine; MRI = magnetic resonance imaging;
Tg = thyroglobulin; T4 = thyroxine; TSH = thyroid-stimulating hormone; US = ultrasound; X 2 = twice.
a
b
58
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ORIGINAL RESEARCH & CONTRIBUTIONS
Evidence-Based Workflows for Thyroid and Parathyroid Surgery
The Permanente Journal/Perm J 2016 Summer:20(3):16-035
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ORIGINAL RESEARCH & CONTRIBUTIONS
Evidence-Based Workflows for Thyroid and Parathyroid Surgery
Serum thyroid-stimulating hormone (TSH, thyrotropin)
levels should be measured as part of the initial evaluation of
a thyroid nodule. If serum TSH level is suppressed, further
workup for hyperthyroidism is warranted by confirming suppressed TSH level and checking the serum thyroxine (T4) level.
If the TSH level remains suppressed, the patient should undergo
a radioiodine thyroid uptake and scan. The workup and management of hyperthyroidism is beyond the scope of this summary.
Observation is recommended for nodules that are predominantly cystic or spongiform, for nodules smaller than 1.5 cm and
in the absence of sonographic high-risk features, and for nodules
smaller than 1 cm and suspicious but with no high-risk factors.
Diagnostic fine-needle aspiration (FNA) is recommended for
cytologic evaluation of nodules greater than 1 cm with a highsuspicion sonographic pattern. FNA is recommended for most
nodules 1.5 cm or larger. In addition to size criteria, high-risk
factors, including family history or other clinical features, may
influence the decision to perform an FNA of a smaller thyroid
nodule.
Ultrasound-guided FNA is the procedure of choice in the
evaluation of thyroid nodules. In the case of an incidentally
noted thyroid nodule in a patient with clinically significant morbidities or a limitation in functional status, pursuing a diagnostic
workup of the nodule may not be relevant. The most common
practice is to acquire two to three cytologic aspirates from each
nodule. If multiple nodules are found, the clinician should evaluate each on the basis of size criteria and sonographic findings.
Medical therapy with levothyroxine is not indicated for the
management of benign thyroid nodules.
For indeterminate cytologic findings, such as the Bethesda
System for Reporting Thyroid Cytopathology5 categories “atypia
of undetermined significance or follicular lesion of undetermined significance” or “follicular neoplasm or suspicious for
a follicular neoplasm,” molecular testing may be considered.
Results of molecular testing may suggest the need for either
observation or total thyroidectomy. In the absence of molecular
testing, diagnostic lobectomy remains the recommended initial
surgical procedure because malignancy may be present in up to
15% of these cases.
If abnormal results of cytologic evaluation are found and
surgery is advised, it is important to have a detailed evaluation
of cervical lymph nodes to assist in surgical planning. If it has
not been done already, the clinician should refer the patient for
diagnostic imaging for a nodal compartment neck sonogram to
be available at the time of surgical consultation. Sonographically abnormal lymph nodes warrant added diagnostic workup
by the endocrinologist or interventional radiologist, who will
perform nodal FNA for cytologic analysis or thyroglobulin
washout or both.
Primary hyperparathyroidism is uncommon but represents
an important potential comorbidity for patients undergoing
thyroid surgery. We recommend there be evidence of a serum
calcium level at least one year in advance of surgery to screen
for hypercalcemia.
A single benign FNA cytologic result does not guarantee
nodule benignity. The false-negative rate is 1% to 3%. Repeated
60
FNA or ultrasound monitoring at 6 to 12 months is recommended for low-risk nodules. If the repeated FNA is negative,
no further sonography is recommended. For high-risk nodules,
repeated sonography and/or FNA in 6 to 12 months is recommended. If the repeated FNA is also benign, repeated sonography is recommended in 2 or 3 years.
The endocrinologist should discuss the indication for and
extent of thyroid surgery with the patient. All patients with a
diagnosis of thyroid cancer or a suspected thyroid cancer should
be referred for surgery. It is advisable to refer patients to a highvolume surgeon with expertise in thyroid and parathyroid surgery.
THYROID NODULE:
PERIOPERATIVE MANAGEMENT
Figure 2 displays the evidence-based recommendations for
perioperative management of thyroid nodules. Our KP study
demonstrated increased efficiency and decreased complications
when management included a consultation with a highvolume thyroid surgeon (defined as having completed more
than 40 cases per calendar year as the primary surgeon). 3
Further analysis will inform our goal of directing care to
higher-volume surgeons who perform at least 20 cases of
thyroid and parathyroid surgeries per year. Surgical risks and
potential postoperative complications should be carefully
reviewed with the patient using a standardized procedurespecific consent form. Patients with clinically significant
substernal extension should be referred to a center with
thoracic surgery backup.
Preoperative documentation of the patient’s voice is recommended. Documentation can be accomplished by using
a patient-reported outcome tool, such as the Voice Handicap
Index, or by examination. Direct laryngeal evaluation should
be performed in patients with previous neck or thoracic surgery, abnormal voice, or known thyroid cancer. Intraoperative
monitoring of the recurrent laryngeal nerve is optional, but
identification and preservation of the nerves is recommended.
Steps also should be taken to preserve the external branch of
the superior laryngeal nerve.
The parathyroid glands should be preserved. Perioperative
antibiotics are not routinely recommended unless the case is
longer than anticipated or includes possible entrance into the
upper aerodigestive tract or a sternotomy. Drains also are not
recommended unless there is a large residual space, lateral neck
dissection, or sternotomy.
Diagnostic lobectomy is typically appropriate for indeterminate lesions, atypia of undetermined significance lesions,
or suspicious for malignancy lesions smaller than 4 cm. Welldifferentiated thyroid cancer that presents in a low-risk patient
as a nodule between 1 cm and 4 cm without extracapsular
spread may be treated with thyroid lobectomy alone. Patients
with nodules exceeding 4 cm or with contralateral nodules
should be considered for total thyroidectomy. However, the
treatment team may recommend, or the patient may consider,
total thyroidectomy to avoid reoperation and/or to enable radioactive iodine (RAI) ablation therapy. Thyroidectomy without prophylactic central neck dissection may be appropriate for
The Permanente Journal/Perm J 2016 Summer:20(3):16-035
ORIGINAL RESEARCH & CONTRIBUTIONS
Evidence-Based Workflows for Thyroid and Parathyroid Surgery
small T1 or T2 noninvasive, clinically node-negative papillary
thyroid carcinomas (cN0) and for most follicular cancers.
Patients with T3, T4, or any TN(+) or M(+) disease should
undergo a near-total or total thyroidectomy, with therapeutic
central compartment (Level VI) neck dissection in the presence
of clinically involved nodes. Prophylactic central neck dissection
(ipsilateral or bilateral) should be considered in patients with
advanced primary well-differentiated tumors with clinically involved lateral neck lymph nodes or clinically uninvolved central
neck lymph nodes (cN0) if the information will be used to plan
further steps in therapy. Therapeutic lymph node dissection of
the lateral neck compartment should be performed for patients
with biopsy-proven metastatic lateral cervical lymphadenopathy.
Postsurgical management of patients who undergo complete
thyroidectomy includes levothyroxine supplementation with a
recommended standard dose of 1.5 µg/kg and adjustment to
1.0 µg/kg to 1.4 µg/kg for older patients or those with comorbidities, such as cardiac disease.
Hypocalcemia management may be achieved with empirical
therapy or by obtaining intraoperative parathyroid hormone
(PTH) levels, which can be drawn at the time the incision is
closed. If the intraoperative PTH level exceeds 20 pg/mL, no supplementation is recommended. For an intraoperative PTH level
of 10 pg/mL to 20 pg/mL, we recommend prescribing calcium
supplementation at discharge; if the level is less than 10 pg/mL, the
clinician should recommend calcium supplements and prescribe
calcitriol. If the intraoperative PTH level is less than 6 pg/mL
or the patient is at high risk of postsurgical hypocalcemia and is
receiving empirical therapy or is symptomatic, one should consider checking a serum calcium level by the third postsurgical day.
Six to eight weeks postoperatively, the patient should undergo
a voice assessment via a telephone appointment visit and/or using the Voice Handicap Index. If abnormal voice quality is noted
by the surgeon or by the patient, the clinician should conduct a
laryngeal evaluation with early referral to speech therapy if dysfunction is present or suspected.
The endocrinologist is responsible for requesting postoperative thyroid hormone replacement therapy and obtaining TSH
and thyroglobulin measurements six to eight weeks after surgery.
THYROID CANCER:
POSTOPERATIVE INITIAL THERAPY
The goal is to standardize initial postoperative treatment on
the basis of postoperative ATA risk group determination and the
patient’s early response to treatment (Figure 3). Using these individualized dynamic risk assessment tools, TSH treatment goals
and early decisions about RAI therapy can be made.
The clinician should obtain TSH, thyroglobulin, and thyroglobulin antibody (TgAb) levels six to eight weeks after surgery.
Appropriate treatment planning is guided by correct cancer staging. Staging should be updated as additional clinical information
becomes available.
Using both the MACIS (metastasis, age at presentation, completeness of excision, invasion, size) scoring system (Figure 4) and
the ATA guidelines will help clarify the patient’s risk. Although
MACIS may be a better predictor of future survival/mortality,
ATA risk stratification may be more predictive of local recurrence. When using the MACIS calculator (available on the
Internet at www.thyroid.org/thyroid-cancer-staging-calculator
or on KP HealthConnect in Northern California), one should
assume no distant metastases to calculate the score unless distant metastases are known. The endocrinologist should note the
stage, MACIS score, ATA risk group, initial and current TSH
goal, appropriate tumor marker, use of RAI, and posttreatment
whole-body scan results as well as planned or last postoperative
thyroid ultrasonography.
MODIFIED 2009 ATA RISK STRATIFICATION (2015)
LOW RISK
• No local or distant metastases
• Clinically N0 or N1 micrometastases
(< 5 involved nodes with lesions < 2 mm)
• All macroscopic tumor resected
• No local invasion (no extrathyroidal
extension)
• No vascular invasion
• If Iodine-131 given, no uptake except
in the thyroid bed
• No aggressive history
• Intrathyroidal encapsulated follicular
variant papillary thyroid cancer
• Intrathyroidal well-differentiated follicular with only capsular invasion
• Intrathyroidal well-differentiated
follicular with ≤ 4 foci of vascular
invasion
• Intrathyroidal papillary microcarcinoma, unifocal or multifocal, including
V600 BRAF mutated (if known)
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INTERMEDIATE RISK
• Microscopic invasion of tumor into
the perithyroidal soft tissues
• Clinical N1 or > 5 pathologic N1
with all involved lymph nodes
< 3 cm in largest dimension
• Radioactive iodine avid metastatic
foci in the neck on the first posttreatment whole body radioactive iodine
scan
• Aggressive histology (eg, Tall cell,
hobnail variant, columnar cell carcinoma)
• Papillary thyroid cancer with > 4 foci
of vascular invasion
• Intrathyroidal, papillary thyroid
cancer, primary tumor 1 cm - 4 cm,
V600E BRAF mutated (if known)
• Multifocal papillary microcarcinoma
with extrathyroidal extension and
V600E BRAF mutated (if known)
HIGH RISK
• Macroscopic invasion of tumor
into the perithyroidal soft tissues
(gross extrathyroidal extension)
• Incomplete tumor resection
• Distant metastases
• Pathologic N1 with any metastatic
LN ≥ 3 cm in largest dimension
• Postoperative serum thyroglobulin
suggestive of distant metastases
• Follicular thyroid cancer with
extensive vascular invasion
(> 4 foci of vascular invasion)
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Figure 2. Thyroid nodule: Perioperative management (full-size, color version available at: www.thepermanentejournal.org/files/Summer2016/16035-2.pdf).
AUS = atypia of unknown significance; FN = follicular neoplasm; ioPTH = intraoperative parathyroid hormone (pg/mL); RLN = recurrent laryngeal nerve;
T4 = thyroxine; TAV = telephone appointment “visit”; Tg = thyroglobulin; TID = three times a day; TSH = thyroid-stimulating hormone; X 2 = twice.
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Figure 3. Thyroid cancer: Postoperative initial therapy (full-size, color version available at: www.thepermanentejournal.org/files/Summer2016/16035-3.pdf).
Calculate MACIS (metastasis, age at presentation, completeness of excision, invasion, size) score as if there are no distant metastases, unless known. If Tg level is out of
proportion to presumed burden of disease and MACIS score is borderline for therapy, proceed with radioactive iodine therapy.
See Sidebar: Modified 2009 ATA Risk Stratification (2015).
ATA = American Thyroid Association; I = iodine; MACIS = metastasis, age at presentation, completeness of excision, invasion, size; RAI = radioactive iodine; rhTSH = recombinant
human TSH; Tg = thyroglobulin; TgAb = thyroglobulin antibody; TSH = thyroid-stimulating hormone, mIU/L; THW = thyroid hormone withdrawal; USC = University of Southern
California Endocrine Laboratories.
a
b
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A postoperative thyroglobulin level below 10 ng/mL suggests
a low likelihood of clinically significant persistent disease. However, a thyroglobulin level exceeding 10 ng/mL does not always
indicate clinically significant residual disease, and confirmation
by a posttherapy scan is recommended. Initial thyroglobulin
testing should be done using an assay sensitive for thyroglobulin
antibodies, given that the presence of antibodies can reduce the
validity of thyroglobulin measurements.
On the basis of ATA risk group and response to therapy,
patients with low-risk disease should be assessed for possible
thyroid remnant ablation therapy with RAI. RAI remnant
ablation is an early option for patients who do not appear to
be heading for an excellent response to therapy. For most cases
of remnant ablation, stimulation with recombinant human
TSH is recommended. Unifocal micropapillary disease is usually treated only when the postoperative thyroglobulin level is
higher than expected.
Some patients with intermediate-risk disease and almost all
patients with high-risk disease benefit from RAI treatment. Thyroglobulin and TgAb levels six to eight weeks after surgery aid
in deciding which intermediate-risk patients might benefit from
RAI. For the treatment of high-risk patients with known or suspected metastatic disease, thyroid hormone withdrawal therapy
is recommended, often with pretherapy diagnostic scanning.
High-risk patients should be treated with recombinant human TSH stimulation only if thyroid hormone withdrawal is
medically contraindicated. Typical RAI doses are 125 mCi for
Figure 4. Screenshot of thyroid cancer staging: MACIS (metastasis, age
at presentation, completeness of excision, invasion, size) score calculator
(full-size, color version available at: www.thepermanentejournal.org/files/Summer2016/16035-4.pdf).1
Final prognostic score was defined as MACIS = 3.1 (if age ≤ 39 years) or 0.08 × age (if
age ≥ 40 years), + 0.3 × tumor size (in centimeters), + 1 (if incompletely resected), + 1
(if locally invasive), + 3 (if distant metastases are present).
b
Twenty-year cause-specific survival rates are as follows for each MACIS score: MACIS
< 6 = 99%; MACIS 6-6.99 = 89%; MACIS 7-7.99 = 56%; MACIS ≥ 8 = 24%.
1
Hay ID, Bergstralh EJ, Goellner JR, Ebersold JR, Grant CS. Predicting outcome in
papillary thyroid carcinoma: development of a reliable prognostic scoring system in a
cohort of 1779 patients surgically treated at one institution during 1940 through 1989.
Surgery 1993 Dec;114(6):1050-7; discussion 1057-8.
a
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local disease, including lateral neck nodes, 150 mCi for pulmonary metastases, and 200 mCi for skeletal or other metastases.
Dosimetry can help avoid overtreatment in the case of comorbid renal failure or widespread pulmonary metastases. If
dosimetry in renal failure is not possible, the patient’s dialysis
schedule can guide empirical reduction of iodine(I)-131. If dialysis occurs the day after treatment, the clinician should give
40% of the dose calculated as if the patient had normal renal
function. If dialysis will occur 2 days later, 22% of the calculated
dose should be given.
The likelihood of sufficient iodine clearance after a contrast
computed tomography (CT) study at 4 months is approximately
95%. Patients may be treated after thyroid hormone withdrawal
or after recombinant human TSH stimulation depending on
risk stratification.
THYROID CANCER: SURVEILLANCE
Surveillance for differentiated thyroid cancer can be divided
into biochemical and anatomic components (Figure 5). Biochemical surveillance uses thyroglobulin and TgAb testing. Anatomic surveillance is primarily done with neck ultrasonography.
At 6 to 12 months postoperatively, thyroglobulin and TgAb
testing should be performed with an assay highly sensitive for
TgAb. If TgAb levels are detectable, this same highly sensitive
assay should be used for long-term surveillance of antibody levels.
If the TgAb level is undetectable, thyroglobulin levels can be
used reliably for biochemical surveillance in most patients. Use
of a thyroglobulin assay with detectability to below 0.2 ng/mL
allows confidence in determination of a biochemically complete
response to therapy and is preferred over less sensitive assays.
Thyroglobulin and TgAb levels should be obtained every 3 to
12 months, depending on the patient’s ATA risk category. If the
thyroglobulin or TgAb level increases 50% or more above the
baseline for a given patient and is well above the limit of detection, ultrasound evaluation should be obtained.
Alongside regular biochemical surveillance, imaging with
ultrasound is recommended 6 to 12 months after the initial
therapy and periodically thereafter even if thyroglobulin/TgAb
levels remain stable. Central lymph nodes less than 0.8 cm in the
anterior-posterior dimension and lateral lymph nodes less than
1 cm in the anterior-posterior dimension should be monitored
with serial imaging if thyroglobulin/TgAb markers are stable.
If lymph nodes exceed these dimensions, they should undergo
FNA biopsy with thyroglobulin washout. Patients with biopsyproven or thyroglobulin washout-proven metastatic disease
should be referred for additional surgery.
In the event that thyroglobulin/TgAb levels are rising but
enlarged lymph nodes are negative on FNA biopsy and thyroglobulin washout, additional imaging with CT or magnetic
resonance imaging (MRI) should be performed. Any findings
on additional imaging should be considered for biopsy or
surgery. However, if all imaging has normal findings in the
setting of rising thyroglobulin/TgAb levels, an I-123 wholebody scan is indicated. Disease identified on an I-123 scan
can be treated with I-131 up to 150 mCi. In patients with
thyroglobulin levels exceeding 10 ng/mL and no findings on
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Figure 5. Thyroid cancer: Surveillance (full-size, color version available at: www.thepermanentejournal.org/files/Summer2016/16035-5.pdf).
CT = computed tomography; EBRT = external beam radiation therapy; 18FDG = fludeoxyglucose F 18; FNA = fine-needle aspiration; I = iodine; IR = interventional radiology;
mets = metastases; MRI = magnetic resonance imaging; NED = no evidence of disease; path = pathology; PET = positron emission tomography; RAI = radioactive iodine;
T4 = thyroxine; Tg = thyroglobulin; TgAb = thyroglobulin antibody; TSH = thyroid-stimulating hormone, mIU/L; US = ultrasound; USC = University of Southern
California Endocrine Laboratories; uTG = ultrasensitive thyroglobulin; X 2 = twice.
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ultrasound, CT or MRI, and I-123 scan, the clinician should
consider positron emission tomography-CT and case discussion with his/her local tumor board.
External beam radiation therapy is recommended for RAIrefractory disease or for treatment of symptomatic metastatic
lesions. Tyrosine kinase inhibitors and clinical trials should be
considered for patients with progressive, RAI-refractory disease.
Patients who are candidates for tyrosine kinase inhibitors should
be thoroughly counseled on the potential risks and benefits of
this therapy as well as alternative therapeutic approaches, including supportive care.
To facilitate understanding of probable long-term outcomes
and thereby guide surveillance frequency, one should ensure
that responses to therapy follow ATA recommendations and be
documented as “excellent response,” “biochemically incomplete
response,” “structurally incomplete response,” or “indeterminate
response” (Table 1).
Patients with an “excellent response” to therapy have no
clinical, biochemical, or structural evidence of disease. For this
designation, thyroglobulin levels must be below 0.2 ng/mL in
the setting of negative TgAb levels, or the TgAb level must have
dropped 50% or more from baseline. The recurrence rate in this
group is believed to be 1% or 2%.
Patients with “biochemically incomplete responses” to therapy
have persistent thyroglobulin/TgAb levels in the absence of
localizable disease. Studies have shown no increase in diseasespecific mortality for this group. At 5 to 10 years, 56% to 68%
of these patients will move into the “excellent response” category,
Table 1. Relationship of response to therapy at 6 to 18 months
to initial risk stratification and outcomes at 5 to 15 years
Measure
Initial risk stratificationb
Low
Intermediate
High
Outcomes at 5 to 15 years
No evidence of disease (NED)c
Indeterminant response (IDR)d
Biologically incomplete response (BIR)e
Structurally incomplete response (SIR)f
Response to therapy at
6 to 18 months, %
NED
IDRa
BIRa
SIRa
86-91
57-63
14-16
12-29
8-23
0-4
97-99
80-87
56-86
29-51
11-19
21-22
16-18
2-6
19-28
67-75
1-3
13-20
19-27 8-17
Blank boxes indicate that the proportion of patients in the category is not reported in
the literature.
Modified 2009 American Thyroid Association Risk Stratification System (2015),
assessed 6 to 8 weeks postoperatively.
c
No clinical, biochemical, or structural evidence of disease (thyroglobulin antibody
[TgAb] negative: unstimulated thyroglobulin < 0.2 ng/mL; TgAb positive: > 50% drop in
TgAb from preoperative level and no structural or functional disease).
d
Nonspecific lesions and indeterminate thyroglobulin and TgAb values.
e
Persistent thyroglobulin or TgAb with no localizable disease; detectable nonstimulated
thyroglobulin or positive TgAb without structural disease; typically, nonstimulated
thyroglobulin level > 1 ng/mL and < 50% drop in TgAb.
f
Structural or functional (radioactive iodine, fludeoxyglucose F 18-positron emission
tomography) evidence of persistent or newly identified locoregional or distant
metastases. Of patients with structurally incomplete response, 29% to 51% move to
NED after follow-up surgery. The 15-year mortality for structurally incomplete response
is 11% for locoregional disease and 57% for structural distant metastases.
a
b
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19% to 27% will remain in this category, and 8% to 27% will
experience a recurrence.
Patients with “structurally incomplete responses” to therapy
have persistent or newly identified locoregional or distantly metastatic disease, either biopsy-proven or likely disease as determined
by imaging. In 5 to 10 years, 29% to 51% of these patients will
move into the “excellent response” category. Mortality rates for
this group are highest, with death occurring in 11% of those with
locoregional disease and 57% of those with distant metastases.
Finally, patients with “indeterminate responses” to therapy are
those with nonspecific lesions and thyroglobulin/TgAb levels
between 0.3 and 1 ng/mL. Most of these patients do well; at 5
to 10 years, 80% to 87% will move into the “excellent response”
group while 13% to 20% will move into the “biochemically”
or “structurally incomplete response” group.
All patients require TSH monitoring at least annually. Patients
who are determined to be biochemically and structurally free of
disease and those with indeterminate responses should have TSH
levels maintained at 0.4 mIU/L to 2.0 mIU/L. Patients with
biochemically or structurally incomplete responses to therapy
should have TSH levels maintained at below 0.1 mIU/L if reasonable in the context of coexisting conditions and patient age.
PRIMARY HYPERPARATHYROIDISM:
PREOPERATIVE PREPARATION
Overproduction of PTH resulting in abnormal calcium
homeostasis covers a wide spectrum of presentations, including
the following:
• hypercalcemia with elevated PTH level
• hypercalcemia with normal but inappropriate PTH level
• eucalcemia with elevated PTH level in the absence of secondary causes.
Symptoms may or may not be present and include but are not
limited to osteoporotic fractures, renal stones, constipation or
abdominal pain, peripheral neuropathy, headaches, or psychiatric symptoms. One should suspect primary hyperparathyroidism
(PHPT) in patients with hypercalcemia, inappropriately low
bone density for age, or family history (hyperparathyroidismjaw tumor syndrome, multiple endocrine neoplasia, and familial
isolated hyperparathyroidism).
Secondary hyperparathyroidism often results from prolonged renal disease, especially after kidney transplantation when prolonged
pretransplant parathyroid stimulation could result in autonomous
PTH production and hypercalcemia. Patients treated with lithium,
especially for prolonged periods, may present with secondary hyperparathyroidism; lithium alters calcium sensing, causing four-gland
hyperplasia. Some patients could harbor an unrelated underlying
adenoma, and PHPT is detected in associated monitoring.
The ideal workup includes a simultaneous fasting serum calcium
test and PTH measurement (Figure 6). When in doubt, one should
repeat the PTH estimation. The most common causes of hypercalcemia other than PHPT are thiazide diuretics (through decreased resorption of calcium in the kidney) and malignancy (through a variety
of mechanisms). Rarely, excess calcium ingestion or granulomatous
processes (including but not limited to tuberculosis and sarcoidosis) can cause high serum calcium levels with suppressed PTH.
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Evidence-Based Workflows for Thyroid and Parathyroid Surgery
Figure 6. Primary hyperparathyroidism: Preoperative management (full-size, color version available at: www.thepermanentejournal.org/files/Summer2016/16035-6.pdf).
CT = computed tomography; GFR = glomerular filtration rate; HPT = hyperparathyroidism; MIBISPECT = technetium Tc 99 sestamibi single-photon emission-computed tomography
scintigraphy; PTH = parathyroid hormone; SPECT CT = single-photon emission computed tomography; TAV = telephone appointment “visit”; US = ultrasound.
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Evidence-Based Workflows for Thyroid and Parathyroid Surgery
Figure 7. Hyperparathyroidism: Intraoperative and postoperative management (full-size, color version
available at: www.thepermanentejournal.org/files/Summer2016/16035-7.pdf).
HPT = hyperparathyroidism; ioPTH = intraoperative parathyroid hormone (pg/mL); US = ultrasound; X 2 = twice.
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Diagnostic serum testing should include measurement of serum creatinine to rule out renal disease, 25-hydroxyvitamin D,
phosphorus, ionized calcium, albumin, and alkaline phosphatase. The latter may be elevated in predominant bone disease,
identifying high turnover and a resulting risk of hungry bone
syndrome.
In determining whether surgical removal of parathyroid tissue is
warranted, the clinician can use several criteria depending on the
presence or absence of symptoms. A 24-hour urine collection for
calcium and creatinine will allow the calculation of renal calcium
clearance. High urinary calcium loss may warrant surgical intervention; this is often present in PHPT. Low urinary calcium loss
suggests familial hypocalciuric hypercalcemia, a benign condition
for which surgery is not indicated.
Once the diagnosis of PHPT has been established, surgery is
the treatment of choice in the absence of a contraindication, such
as limited life expectancy, or evidence of end-organ damage (eg,
renal compromise, osteoporosis), especially in the presence of
evidence of disease progression.
If the patient is asymptomatic, we adhere to the guidelines for
surgery from the Management of Asymptomatic PHPT Fourth
International Workshop in 2013.6 We would consider surgery if
any of the following is present (see Figure 6):
• hypercalcemia: serum calcium level exceeding 1 mg/dL above
the upper limit of normal
• skeletal compromise
- low bone mineral density determined by dual-energy x-ray
absorptiometry: T-score at or below -2.5 at the lumbar spine,
total hip, femoral neck, or distal one-third radius (standard
bone density measurement sites); use Z-scores for premenopausal women and men younger than age 50 years
- vertebral fracture demonstrated using radiography, CT, or
vertebral fracture analysis
- history of fragility fracture (considered a skeletal complication of PHPT)
• renal compromise
- glomerular filtration rate below 60 mL/min/1.73 m2
- 24-hour urine calcium level above 400 mg/day and increased
stone risk by biochemical stone analysis
- nephrolithiasis or nephrocalcinosis by x-ray, ultrasound, or CT
• age under 50 years.
Meeting only a single criterion indicates the need for surgery.
Other general criteria that the workshop itemized as an indication for surgery include
• Medical surveillance is neither desired nor possible
• The disease has progressed
• The patient prefers surgery in the absence of meeting the aforementioned criteria (as long as there are no contraindications).
The task force members thought that the defining criteria for a
neurocognitive component (including but not limited to fatigue
and depression) were not definitive.
Once the decision to proceed with surgical consultation is
made, a preliminary thyroid sonogram is acquired to identify
thyroid nodules and potentially localize a parathyroid adenoma.
Ruling out medullary thyroid cancer (associated with MEN2A)
in a nodule and workup of thyroid nodules before surgery may
72
change the scope of the surgery. If the sonogram is nonlocalizing,
most experts proceed to parathyroid scintigraphy using technetium Tc 99m pertechnetate sestamibi washout imaging with or
without SPECT (or SPECT CT) to improve localization together
with sonography. Multiphasic CT may also be considered if the
combination of sonography and scintigraphy is nonlocalizing
or discordant. A presurgical discussion about the likelihood of
hyperplasia or multiple adenomas is recommended because of its
potential to alter the surgical approach.
HYPERPARATHYROIDISM: INTRAOPERATIVE
AND POSTOPERATIVE MANAGEMENT
Parathyroid Localization Studies
In advance of most surgical procedures, the surgeon knows
what will be resected and from which location (Figure 7). Parathyroid surgical therapy differs because the glands are small and
of variable number and location. Although localization studies
have improved greatly in the past three decades, we are sometimes
unable to reliably determine the number and location of all diseased glands preoperatively.
With the advent of an inexpensive and relatively rapid intraoperative PTH assay, localization studies have become increasingly important because minimally invasive procedures may be performed
in approximately 85% of cases. As localization studies continue to
be refined and new modalities are developed, our algorithm will
evolve: we currently recommend a combination of sonography and
sestamibi washout scintigraphy as first-line localization studies.
Parathyroid surgeons should become facile with in-office sonography. They have an excellent grasp of the anatomy and both
typical and atypical locations of the parathyroid glands; therefore,
using basic sonography skills, parathyroid surgeons may quickly
become proficient at parathyroid sonography. Sestamibi washout
scintigraphy is helpful should the sonogram be nonlocalizing,
especially in mediastinal disease, in which there is no utility of
sonography. Sestamibi washout scintigraphy is limited in the
presence of multiglandular parathyroid disease or synchronous
hyperfunctioning thyroid nodules. Multiphasic enhanced neck
CT may be of benefit when the sonography and scintigraphy are
nonlocalizing, discordant, or both but has a distinct disadvantage
of a very high radiation dose; it is thus not currently recommended as an initial localizing study. Additional studies—MRI,
FNA with sonographic guidance, and venous sampling—may
be used, especially in revision cases for which we recommend
having concordant results with at least two modalities before
reexploration whenever possible.
Intraoperative and Postoperative Management
A skilled parathyroid surgeon navigates the subtleties and
complexities of hyperparathyroidism. Before taking the patient
to the operating theater, the surgeon will have thoroughly reviewed the case and its corresponding localization studies to be
certain of the diagnosis of PHPT. If a localization study is not
validated in the operating room and four normal glands are
found, a surgeon who is certain of the diagnosis may confidently
expand the exploration, find the abnormal gland, and conclude
surgery successfully.
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Evidence-Based Workflows for Thyroid and Parathyroid Surgery
A baseline intraoperative PTH measurement is critical for a
focused exploration and also helps determine when to stop in a
bilateral exploration; more than 4 glands are present in approximately 6% of cases. Owing to variable PTH kinetics, no perfect
criterion exists for terminating an operation. The more stringent
the criteria, the higher the number of unnecessary explorations
that will occur. We now recognize that a drop in intraoperative
PTH level exceeding 50% from the preexcision value does not
result in an adequate cure rate, and we recommend continued
exploration if the final PTH exceeds 65 pg/mL. In addition,
current thinking suggests that patients with values exceeding
40 pg/mL may have hyperplasia. It is almost always better to
perform a bilateral exploration than to return at a later date to
face a scarred operative field, where finding the diseased gland
is more challenging and could result in greater complications.
The nature of renal hyperparathyroidism mandates bilateral
exploration. A hyperplastic process involving all the glands is
generally present even when a localization study identifies only
one or two abnormal glands, and hyperplastic glands can vary
greatly in size. Postsurgical hypercalcemia should be expected in
most cases of renal hyperparathyroidism. Monitor patients who
have clinically significant bone disease with special vigilance.
CONCLUSION
These workflows synthesize the best evidence currently available about caring for patients with thyroid nodules and PHPT
and represent an attempt to standardize the care of patients with
thyroid and parathyroid diseases. The evidence-based decision
points and workflows presented here support an initiative of
specialty care redesign to provide consistency in delivery of care
and outcomes for our patient population. v
Disclosure Statement
The author(s) have no conflicts of interest to disclose.
Acknowledgment
The authors would like to thank Violeta Rabrenovich for material support of
this work. Jennifer Green provided editorial assistance.
Kathleen Louden, ELS, of Louden Health Communications provided editorial
assistance.
How to Cite this Article
Meltzer C, Budayr A, Chavez A, et al. Evidence-based workflows for
thyroid and parathyroid surgery. Perm J 2016 Summer;20(3):16-035.
DOI: http://dx.doi.org/10.7812/TPP/16-035.
References
1. Haugen BR, Alexander EK, Bible KC, et al. 2015 American Thyroid Association
management guidelines for adult patients with thyroid nodules and differentiated
thyroid cancer: the American Thyroid Association guidelines task force on thyroid
nodules and differentiated thyroid cancer. Thyroid 2016 Jan;26(1):1-133. DOI:
http://dx.doi.org/10.1089/thy.2015.0020.
2. Meltzer C, Klau M, Gurushanthaiah D, et al. Safety of outpatient thyroid and
parathyroid surgery: a propensity score-matched study. Otolaryngol Head Neck
Surg 2016 May;154(5):789-96. DOI: http://dx.doi.org/10.1177/0194599816636842.
3. Meltzer C, Klau M, Gurushanthaiah D, et al. Surgeon volume in thyroid and
parathyroid surgery: surgical efficiency, outcomes, and utilization. Laryngoscope
2016 Jun 23 [Epub ahead of print]. DOI: http://dx.doi.org/10.1002/lary.26119.
4. Meltzer C, Klau M, Gurushanthaiah D, et al. Risk of complications after thyroidectomy
and parathyroidectomy: a case series with planned chart review. Otolaryngol Head
Neck Surg 2016 May 3 [Epub ahead of print]. DOI: http://dx.doi.org/10.1177/
0194599816644727.
5. Cibas ES, Ali SZ; NCI Thyroid FNA State of the Science Conference. The Bethesda
system for reporting thyroid cytopathology. Am J Clin Pathol 2009 Nov;132(5):658-65.
DOI: http://dx.doi.org/10.1309/AJCPPHLWMI3JV4LA.
6. Udelsman R, Akerstrom G, Biagini C, et al. The surgical management of
asymptomatic primary hyperparathyroidism: proceedings of the Fourth International
Workshop. J Clin Endocrinol Metab 2014 Oct;99(10):3596-606. DOI: http://dx.doi.
org/10.1210/jc.2014-2000.
The Third View
The practical surgical question as to whether the cretinous symptoms following
thyroidectomy are due to—1) Chronic asphyxia, as believed by Kocher;
2) Injury of the sympathetic and other nerve trunks;
3) Arrest of function of the thyroid gland;
is almost settled in favor of the third view,
and with it also the pathology of Myxoedema.
— Sir Victor Alexander Haden Horsley, FRS, 1857-1916, English neurosurgeon and neuroscientist
The Permanente Journal/Perm J 2016 Summer:20(3):16-035
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ORIGINAL RESEARCH & CONTRIBUTIONS
Special Report
The Truth about Truth-Telling in American Medicine: A Brief History
Bryan Sisk, MD; Richard Frankel, PhD; Eric Kodish, MD; J Harry Isaacson, MD
E-pub 06/22/2016
ABSTRACT
Transparency has become an ethical cornerstone of American
medicine. Today, patients have the right to know their health information, and physicians are obliged to provide it. It is expected
that patients will be informed of their medical condition regardless
of the severity or prognosis. This ethos of transparency is ingrained
in modern trainees from the first day of medical school onward.
However, for most of American history, the intentional withholding of information was the accepted norm in medical practice. It
was not until 1979 that a majority of physicians reported disclosing cancer diagnoses to their patients. To appreciate the current
state of the physician-patient relationship, it is important to understand how physician-patient communication has developed
over time and the forces that led to these changes. In this article,
we trace the ethics and associated practices of truth-telling during
the past two centuries, and outline the many pressures that influenced physician behavior during that time period. We conclude
that the history of disclosure is not yet finished, as physicians still
struggle to find the best way to share difficult information without
causing undue harm to their patients.
A HISTORY OF DISCLOSURE IN MEDICINE
Pre-20th Century Communication
Disclosing bad news to patients has challenged physicians since
the early days of American medicine. In the 19th century, physicians
often made medical decisions on behalf of their patients, in what
they perceived to be the patient’s best interest. This paternalistic
approach led most physicians to disclose only information that they
believed would not harm the patient, as embodied in the 1847 Code
of Ethics of the newly founded American Medical Association:
A physician should not be forward to make gloomy prognostications, because they savour of empiricism. … But he should
not fail, on proper occasions, to give to the friends of the patient
timely notice of danger, when it really occurs; and even to the
patient himself, if absolutely necessary. … For, the physician
should be the minister of hope and comfort to the sick.1
On one level, paternalism in this period was rooted in benevolent
concern for the patient’s well-being. As further stated in the Code:
“The life of a sick person can be shortened, not only by the acts
but also by the words or the manner of a physician. It is, therefore, a sacred duty to guard himself carefully in this respect, and
to avoid all things which have a tendency to discourage the patient
and to depress his spirits.”1 This ethical standard followed directly
from Thomas Percival’s 1803 treatise on medical ethics: “For the
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http://dx.doi.org/10.7812/TPP/15-219
physician should be the minister of hope and comfort to the sick
that by such cordials to the drooping spirit he may smooth the bed
of death, revive expiring life, and counteract the depressing influence of those maladies which rob the philosopher of fortitude, and
the Christian consolation.”2 In his writings, Percival also discussed
whether a “falsehood may lose the essence of lying, and become
even praiseworthy, when the adherence to truth is incompatible
with the practice of some other virtue of still higher obligation.”2
At the same time, there were less benevolent incentives for physicians to occasionally refrain from honesty. American medicine in the
mid-19th century was poorly organized and had limited authority
in society. Physicians were the product of a fractured apprenticeship
model with no oversight to ensure quality of training, which led to an
increase in the number of physicians, many of them poorly trained,
while professional competition also loomed from other medical sects,
including Thomsonians, eclectics, and homeopaths.3 In short, the
mid-19th century medical market was saturated with physicians.
For physicians to succeed, ensuring an ample number of patients
was paramount, and honesty occasionally took a backseat. In his
1888 manual for success as a physician, DW Cathell intricately laid
out methods by which physicians could create respectable images of
themselves while also protecting their claim to patient populations.4
Neuhauser5 observed, “His book was so popular that it was in its
10th edition in 1892, last revised in 1922 and republished finally in
1932.” In addition to meticulously describing the type of clothing to
wear and the medical paraphernalia to display in the office, Cathell
also encouraged physicians to withhold information to prevent
patients from becoming medically self-sufficient. For example, he
encouraged physicians to inscribe Latinate terms on medication
vials to conceal their ingredients. He also believed that physicians
should “avoid giving self-sufficient people therapeutic points that
they can thereafter resort to. … It is not your duty to cheat either
yourself or the other physicians out of legitimate practice by supplying this person and that with a word-of-mouth pharmacopoeia
for general use.”4 For both benevolent and self-serving reasons,
honesty was lower on the physician’s list of priorities.
THE DAWN OF THE 20TH CENTURY
As the 20th century dawned, the physician’s standing in society
began to rise, in part because medical science was growing more sophisticated and physicians were becoming indispensable. “Every man,
it became clear, could not be his own physician.”3 This enhancement
of status furthered a social divide between physicians and laymen, as
evidenced by an 1898 excerpt from the Philadelphia Medical Journal:
Bryan Sisk, MD, is a Pediatrics Resident at the St Louis Children’s Hospital in MO. E-mail: [email protected].
Richard Frankel, PhD, is a Professor of Medicine and Geriatrics at the Indiana University School of Medicine Education
Institute in Indianapolis. E-mail: [email protected]. Eric Kodish, MD, is the Director of the Center for Ethics, Humanities
and Spiritual Care at the Cleveland Clinic in OH. E-mail: [email protected]. J Harry Isaacson, MD, is the Director of
Clinical Education at the Cleveland Clinic Lerner College of Medicine and an Internist in the Department of General
Internal Medicine at the Cleveland Clinic in OH. E-mail: [email protected]
74
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ORIGINAL RESEARCH & CONTRIBUTIONS
The Truth about Truth-Telling in American Medicine: A Brief History
Into many homes the doctor brings the only refinement
and culture that its inmates ever come in contact with. They
recognize it, just as do even dumb animals, and it must have
an elevating effect, if only a temporary one. His quiet air of
composure, and that reserved force which education and culture set up in a man, appeal to poor fallen wretches as something worthy of admiration, even if they have not the strength
remaining to care to strive toward it.6
The growing class divide and the perceived dangers of bad news
perpetuated the paternalistic approach of benevolent deception.
An article in 1898, more than 50 years after the initial American
Medical Association Code of Ethics, repeated this same principle of nondisclosure nearly verbatim: “In regard to cancer, the
consensus of opinion is that patients be kept in ignorance of the
nature and probable outcome of the disease as long as possible,
in this way obviating the severe mental depression which invariably accompanies such knowledge.”7 The cause for concern was
unchanged: “It is not merely the danger of ‘fatal shock’ that should
restrain a physician in many cases from disclosing the truth to his
patient, but the almost certainty that such a disclosure will be the
greatest obstacle to a cure.”8 In 1909, William Osler declared, “It
is a hard matter … to tell a patient that he is past all hope. As Sir
Thomas Browne says: ‘It is the hardest stone you can throw at a
man to tell him that he is at the end of his tether.’”9 The reasoning was simple. “With many hospital patients once we gain their
confidence and inspire them with hope, the battle is won.”9
MID-20TH CENTURY AND BEYOND
Although there were some opponents of benevolent deception,
physician surveys during the first half of the 20th century consistently demonstrated a belief in nondisclosure. As recently as
1961, 90% of physicians preferred not to disclose cancer diagnoses
to patients.10 This was despite the results of a 1950 study showing that a vast majority of patients wanted to know the truth.11
On the basis of his observations in a veterans’ hospital in 1966,
Glaser12 proposed several factors that influenced the physicians’
approaches to disclosure:
Few doctors get to know each terminal patient well enough
to judge his desire for disclosure or his capacity to withstand
the shock of disclosure … . Some doctors simply feel unable
to handle themselves well enough during disclosure. … Others
do not tell because they did not want the patient to “lean” on
them for emotional support, or because they simply wish to
preserve peace on the ward by preventing a scene.12
During the 1960s, tremors of change began rumbling through
American society. After the assassination of President John Kennedy, President Lyndon Johnson “sponsored the largest reform
agenda since Roosevelt’s New Deal.”13 From 1963 through 1966,
Johnson undertook a major reform agenda that touched on many
aspects of society. With the expansion of Social Security to include
Medicare and Medicaid, as well as the passage of the Food Stamp
Act,14 Housing and Urban Development Act,15 Child Protection
Act,16 and the Child Nutrition Act,17 the government assumed additional responsibility for the safety and well-being of its citizens.
The 1960s also marked the start of a great transformation in
American social norms as underrepresented groups challenged
The Permanente Journal/Perm J 2016 Summer;20(3):15-219
the status quo. The Civil Rights Movement pushed for passage of
the Civil Rights Bill18 and the Voting Rights Act.19 The feminist
movement demanded more autonomous control of women’s reproductive health and a shift in society’s view of women.20,21 The
1960s also marked the beginning of a psychedelic culture of drug
experimentation, the sexual revolution, and the countercultural
“hippie” movement.22 It was not uncommon for people to wear
buttons stating “Question Authority.” As society was redefining
itself, “a new wave of individualism was breaking over the Western
world—most marked and most advanced in the United States.”23
Long-held social norms were being turned upside down in all
segments of society, including the physician-patient relationship.
Owing in part to several well-publicized controversies, there was
a new call for protection from the medical establishment. In 1963, it
was revealed that researchers in New York had injected humans with
live cancer cells without consent.24 In 1964, a surgeon transplanted
chimpanzee kidneys into patients with renal failure without medical
approval from the hospital.25 By 1966, Henry Beecher published a
special report highlighting and summarizing the widespread presence of “troubling practices” in clinical research.26
Perhaps most notably, the ethical concerns of the Tuskegee Syphilis Study came to light in July 1972. This study, initiated in 1932,
was a “long-term evaluation of the effect of untreated syphilis in
the male Negro.”27 Physicians informed participants that they were
being treated for “bad blood” but not specifically syphilis. When
the study began, treatments for syphilis were harsh and minimally
effective. However, penicillin was established as an effective treatment and became readily available by the late 1940s.28 Yet 20 years
later, only 33% of participants had received curative therapy, and
many had died of complications from syphilis.27 This story quickly
became front-page news in the New York Times29 on July 25, 1972
with the headline “Syphilis Victims in US Study Went Untreated
for 40 Years.” Other headlines in the following weeks included “A
Shocking Medical Experiment,” “Humans as Guinea Pigs,” and “A
Violation of Human Dignity.” The fallout from this exposé further
exacerbated the adversarial relationship between medicine and society, especially in the African American community.
Twenty years earlier in 1951, an African American woman
named Henrietta Lacks was diagnosed with cervical cancer in
Baltimore, MD. When the physicians diagnosed her with cancer,
they took a specimen from her cervix without her knowledge or
consent. She died soon after, but her cells lived on as the HeLa
cell line, using the first 2 letters of her first and last name. These
cells had an enormous impact on public health and the advancement of science, but the family was not informed until the 1970s,
20 years after Ms Lacks’ death.30 Though this was not as widely
publicized as the Tuskegee scandal, it provides yet another example
of troubling research practices at that time.
As controversies grew, new protections for patients and research
subjects were established. In 1962, the Senate passed the KefauverHarris Drug Amendments,31 requiring for the first time that drug
manufacturers “prove to FDA the effectiveness of their products
before marketing them.”32 That same year, President Kennedy proclaimed a “Consumer Bill of Rights,” which included “the right to
safety, the right to be informed, the right to choose, and the right
to be heard.”32 In 1964, the World Medical Association published
75
ORIGINAL RESEARCH & CONTRIBUTIONS
The Truth about Truth-Telling in American Medicine: A Brief History
the Declaration of Helsinki, an international code of research ethics
affirming that the physician’s first duty is to the research subject.33
Simultaneously, informed consent law was growing in strength,
mandating honest communication between physicians and patients under threat of legal liability. Also, Dame Cicely Saunders
introduced the concept of hospice and palliative care to the US in
the 1960s, further encouraging discussions between physician and
patient about death. By 1973, the American Hospital Association
created “A Patient’s Bill of Rights,” stating that “The patient has
the right to and is encouraged to obtain from physicians and their
direct caregivers relevant, current, and understandable information
concerning diagnosis, treatment, and prognosis.”34
Responding to these pressures, physicians began calling for
more transparency with patients. Nahum noted in 1963, “The
responsible physician should have no hesitation in frankly but
tactfully and at the correct time answering questions asked by the
patient,” with the goal of being “truthful with the patient while
at the same time avoiding a major emotional upset.” However,
Nahum moderated this approach with a list of stipulations. “In
patients judged to be unstable emotionally, the exact information
should be withheld.” Additionally, “if he does not [ask for specific
information], then the doctor’s legal and moral obligations have
been discharged for such a person … is aware of his trouble but
does not wish to have it put into words.”35 An article from 1974
pushed disclosure further, concluding that several factors could
“justify me in modifying my primary approach and making the
patient or his relatives, directly or indirectly, aware of the diagnosis
and perhaps even of the prognosis, grave as it may be.”36 In 1969,
Kubler-Ross37 declared, “The question should not be ‘Should
we tell…?’ but rather ‘How do I share this with my patient?’”
The medical profession was transitioning from paternalism to a
partnership-based medical ethics where patients participated in
the decision-making process. In 1979, a landmark study using the
same research questionnaire from 1961 showed that more than
90% of a new cohort of physicians preferred disclosing cancer
diagnoses, a complete reversal from 18 years prior.38
The progressive movement of the 1960s and 1970s pushed
physicians toward more open and transparent communication
with patients. This transition was reinforced by social pressure, legal mandates, and large numbers of young, progressive physicians
entering the field. In the midst of these changes, Family Practice
(now Family Medicine) developed as a new field, with an emphasis
on the individual patient and his or her social environment. This
trend toward transparency has continued over the ensuing decades, reinforced in part by developments in the field of bioethics.
The 1979 “Belmont Report” established the fundamental ethical
principles of research on human subjects, including respect for
persons, beneficence, and justice.39 These principles have served as
the foundation for current research practices.
Advancements in research on physician-patient communication
have also supported the trend toward disclosure. In 1987, Menahem40 showed that communication in a partnership model was
more effective than either a laissez-faire or physician-dominated
model. In 1995, Girgis and Sanson-Fisher41 published consensus
guidelines for giving bad news, which have provided a basis for
discussion and improvement of communication in medicine.
76
Standards of care now include an explicit focus on disclosure
and communication skills. In 2013, the Institute of Medicine
published a monograph on delivering high-quality cancer care
that focused an entire chapter on evidence for best practices in
communicating with cancer patients.42 The National Cancer Institute produced an entire monograph on patient-centered communication in cancer care, devoting four of its six chapters to key
communication skills including delivery of difficult news.43 Most
recently in 2014, the Institute of Medicine issued a new report that
focused on end-of-life care in America, much of which centered
on ways to improve the physician-patient dialogue about bad
news.44 Medical students and residents are now routinely trained
in how to effectively communicate in challenging situations, and
patients expect transparency in their interactions with physicians.
However, communication in medicine is still far from perfect.
For example, a recent report from the Alzheimer’s Association
in 2015 showed that less than half of patients with Alzheimer’s
disease or their family members had knowledge of their loved
one’s or their own diagnosis.45 One physician noted in a media
interview following the report, “It’s difficult to disclose a diagnosis
of a fatal brain disease in just a few minutes.”46 In parallel with
these changes, the American Medical Association Code of Ethics
has evolved substantially since 1847, with its current form stating
“The patient has the right to receive information from physicians
and to discuss the benefits, risks, and costs of appropriate treatment alternatives.”47
Reinforcing these changes, the medical record has also evolved
from a tool solely for physicians to a new means of communicating with patients. In 1973, Shenkin and Warner48 proposed that
“legislation be passed to require that a complete and unexpurgated
copy of all medical records … be issued routinely and automatically to patients as soon as the services provided are recorded.”
This article furthered the belief that patients are owners of their
medical information. In 1991, McLaren49 proposed that medical
records should not only be available, but also be understandable
to patients. The Health Insurance Portability and Accountability
Act50 was passed in 1996, creating new protections for patient
confidentiality by restricting disclosure of medical information
without the patient’s consent. This act reinforced the patient’s
authority over his or her health information, while also mandating
that physicians respect their patients’ confidentiality.
Communication in medicine has undergone dramatic changes
during the past 170 years. Where once physicians withheld information for the benefit of the patient, it is now clearly recognized that
patients have a right to know the truth. The medical profession has
responded to both internal and external pressures and developed a
standard of care based on honesty and patient-centered communication. However, many uncertainties remain. How much disclosure
is enough? How much is too much? Can we cause harm by telling
too much or in the wrong way? Is there ever a role for benevolent
deception? Should physicians be the gatekeepers of medical information? How will the recent emphasis on shared medical records
affect this relationship? Currently, several organizations are actively
promoting sharing of medical data and notes with patients.51 Some
current-day patients might have their test results available electronically before ever speaking with their physicians.
The Permanente Journal/Perm J 2016 Summer;20(3):15-219
ORIGINAL RESEARCH & CONTRIBUTIONS
The Truth about Truth-Telling in American Medicine: A Brief History
Though we can certainly say that “patients ought to know,” it is
difficult to know exactly what they ought to know, and how to best
share this information. These are critical questions that are worthy of
study. The truth about truth-telling is that it is an unfinished history
that continues to evolve. Physicians and patients will undoubtedly
need to partner to develop the next chapter in this story. v
Disclosure Statement
The author(s) have no conflicts of interest to disclose.
Acknowledgments
Thank you to Lauren Yaeger, MA, MLIS, medical librarian at St Louis
Children’s Hospital, for assisting our research in Internet databases and the
historical archives.
Mary Corrado, ELS, provided editorial assistance.
How to Cite this Article
Sisk B, Frankel R, Kodish E, Isaacson JH. The truth about truth-telling in
American medicine: a brief history. Perm J 2016 Summer;20(3):15-219.
DOI: http://dx.doi.org/10.7812/TPP/15-219.
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23. Cassell EJ. The nature of suffering and the goals of medicine. 2nd ed. New York, NY:
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24. Katz J. Experimentation with human beings: the authority of the investigator, subject,
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30th year of observation. Arch Intern Med 1964 Dec;114:792-8. DOI: http://dx.doi.org/
10.1001/archinte.1964.03860120104011.
28. Kampmeier RH. The Tuskegee study of untreated sphilis. South Med J 1972
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29. Heller J. Syphilis victims in US study went untreated for 40 years. The New York Times
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30. Skloot R. The immortal life of Henrietta Lacks. New York, NY: Broadway Paperbacks; 2011.
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and Drug Administration; 2014 Dec 19 [cited 2015 Sep 21]. Available from: www.fda.
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35. Nahum LH. To tell the truth. Conn Med 1963 Aug;27:443-5.
36. Snyman HW. Should the doctor tell? South Afr Cancer Bull 1974 Oct-Dec;18(4):130-4.
37. Kubler-Ross E. On death and dying. New York, NY: Macmillan; 1969.
38. Novack DH, Plumer R, Smith RL, Ochitill H, Morrow GR, Bennett JM. Changes in
physicians’ attitudes toward telling the cancer patient. JAMA 1979 Mar 2;241(9):897900. DOI: http://dx.doi.org/10.1001/jama.241.9.897.
39. The National Commission for the Protection of Human Subjects of Biomedical and
Behavioral Research. The Belmont report: ethical principles and guidelines for the
protection of human subjects of research [Internet]. Washington, DC: US Department
of Health and Human Services; 1979 Apr 18 [cited 2014 Dec 15]. Available from:
www.hhs.gov/ohrp/humansubjects/guidance/belmont.html.
40. Menahem S. Teaching students of medicine to listen: the missed diagnosis from a
hidden agenda. J R Soc Med 1987 Jun;80(6):343-6.
41. Girgis A, Sanson-Fisher RW. Breaking bad news: consensus guidelines for medical
practitioners. J Clin Oncol 1995 Sep;13(9):2449-56.
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charting a new course for a system in crisis. Washington, DC: Institute of Medicine of
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44. Committee on Approaching Death: Addressing Key End-of-Life Issues. Dying in
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46. Hamilton J. Many doctors who diagnose Alzheimer’s fail to tell the patient [Internet].
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47. AMA’s code of medical ethics [Internet]. Chicago, IL: American Medical Association;
1957 Jun [revised 2001 Jun; cited 2015 Sep 21]. Available from: www.ama-assn.org/
ama/pub/physician-resources/medical-ethics/code-medical-ethics.page?.
48. Shenkin BN, Warner DC. Sounding board. Giving the patient his medical record: a
proposal to improve the system. N Engl J Med 1973 Sep 27;289(13):688-92. DOI:
http://dx.doi.org/10.1056/nejm197309272891311.
49. McLaren P. The right to know. BMJ 1991 Oct 19;303(6808):937-8. DOI: http://dx.doi.
org/10.1136/bmj.303.6808.937.
50. The Health Insurance Portability and Accountability Act of 1996. Public Law 104-191,
104th Congress, 110 Stat 1936, HR 3103, enacted 1996 Aug 21.
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77
REVIEW ARTICLE
Hyperparathyroidism of Renal Disease
Noah K Yuen, MD; Shubha Ananthakrishnan, MD; Michael J Campbell, MD
Perm J 2016 Summer;20(3):15-127
E-pub: 07/22/2016
ABSTRACT
Renal hyperparathyroidism (rHPT) is a common complication
of chronic kidney disease characterized by elevated parathyroid
hormone levels secondary to derangements in the homeostasis of
calcium, phosphate, and vitamin D. Patients with rHPT experience
increased rates of cardiovascular problems and bone disease. The
Kidney Disease: Improving Global Outcomes guidelines recommend that screening and management of rHPT be initiated for all
patients with chronic kidney disease stage 3 (estimated glomerular
filtration rate, < 60 mL/min/1.73 m2). Since the 1990s, improving
medical management with vitamin D analogs, phosphate binders,
and calcimimetic drugs has expanded the treatment options for
patients with rHPT, but some patients still require a parathyroidectomy to mitigate the sequelae of this challenging disease.
BACKGROUND
In the US, chronic kidney disease (CKD) affects 14% of the
population,1,2 including approximately 660,000 patients with
end-stage renal disease (ESRD) who are dialysis-dependent.2
Renal hyperparathyroidism (rHPT) is a common complication
of CKD characterized by derangements in the homeostasis of
calcium, phosphorus, and vitamin D.3 rHPT is associated with
increased cardiovascular morbidity and mortality4-8 and has a
significant economic burden on the US health care system.9
rHPT is classically broken into 2 types on the basis of the
patient’s serum calcium level. Secondary hyperparathyroidism
(2° HPT) is the elevation of parathyroid hormone (PTH) in
response to hypocalcemia induced by phosphate retention and
reduced calcitriol synthesis as a consequence of reduced renal function.10 In 2° HPT, all the parathyroid glands become enlarged owing to parathyroid hyperplasia. Because 2° HPT is a compensatory
mechanism of the parathyroid glands, it commonly resolves with
normalization of calcium and phosphorus homeostasis (eg, renal
transplantation). Tertiary hyperparathyroidism (3° HPT) is seen
when a patient with longstanding 2° HPT develops autonomous
PTH secretion, often associated with hypercalcemia. This is observed in up to 30% of patients with ESRD, who then undergo
renal transplant.11 3° HPT is classically thought to have come from
parathyroid hyperplasia, but some studies have suggested that
up to 20% of patients may have single or double adenomas.11,12
Since the 1990s, improving medical management with vitamin D analogs, phosphate binders, and calcimimetic drugs
has expanded the treatment options for patients with rHPT,
but parathyroidectomy remains necessary for many patients.
http://dx.doi.org/10.7812/TPP/15-127
NORMAL CALCIUM AND PHOSPHORUS HOMEOSTASIS
Calcium and phosphorus homeostasis is maintained through
a complex relationship between the bones, intestine, kidneys,
and parathyroid glands. PTH is probably the most important
regulator of calcium metabolism and functions primarily via 3
mechanisms:
1.PTH is thought to stimulate PTH receptors mainly on osteoblasts, which then, through multiple cell-to-cell mechanisms,
stimulate osteoclast formation and bone resorption, leading
to increased serum calcium and phosphorus levels.13
2.PTH activates 1-α-hydroxylase in the kidney, which catalyzes
the conversion of nonactive 25-hydroxy (25-OH) vitamin D
to activated 1,25 dihydroxy (1,25-OH) vitamin D. This leads
to increased absorption of calcium and phosphorus in the gut.
3.PTH increases reabsorption of calcium and decreases reabsorption of phosphorus in the kidney.
Recently, there has been much interest in the role of fibroblast growth factor 23 (FGF-23), a protein secreted by bone in
response to hyperphosphatemia, which functions primarily in
maintaining phosphorus homeostasis. FGF-23 stimulates phosphorus excretion in the kidney mainly through reduced action of
sodium-phosphate co-transporter in the proximal tubule. It also
decreases 1-α-hydroxylase activity, leading to reduced 1,25-OH
vitamin D levels.14,15 In CKD, FGF-23 levels progressively rise
and are initially thought to be beneficial, given the phosphaturic effects. However, increasing FGF levels are also associated
with increased cardiovascular mortality in patients with CKD.16
PATHOGENESIS
The pathogenesis of rHPT is complex and incompletely
understood (Figure 1). An increase in PTH levels typically develops when the glomerular filtration rate (GFR) drops below
60 mL/min/1.73 m2. Abnormalities in serum levels of phosphorus and calcium tend to occur much later in the course of CKD
(typically when the GFR drops below 40 mL/min/1.73 m2).17
Initially, the elevated PTH levels serve to increase renal phosphorus excretion. However, as the GFR declines further, serum phosphorus levels start to rise and induce hypocalcemia
by binding bioavailable calcium as CaHPO4, which indirectly
leads to a further rise in PTH production. CKD also leads to
decreased activity of 1-α-hydroxylase, thereby decreasing 1,25OH vitamin D. A lack of 1,25-OH vitamin D inhibits gastrointestinal absorption of calcium and also directly stimulates the
parathyroid glands.14
Noah K Yuen, MD, is a Surgical Resident at the University of California, Davis in Sacramento.
E-mail: [email protected]. Shubha Ananthakrishnan, MD, is an Assistant Professor of Internal
Medicine at the University of California, Davis in Sacramento. E-mail: [email protected].
Michael J Campbell, MD, is an Assistant Professor in the Department of Surgery at the University of
California, Davis in Sacramento. E-mail: [email protected].
78
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Hyperparathyroidism of Renal Disease
CLINICAL MANIFESTATIONS
Figure 1. Schematic of the pathogenesis of renal hyperparathyroidism.
CKD = chronic kidney disease; FGF-23 = fibroblast growth factor 23.
In CKD, chronic stimulation of the parathyroid glands triggers diffuse polyclonal hyperplasia. As the chronic stimulation
of CKD continues, the parathyroids begin to develop monoclonal nodules within a background of parathyroid hyperplasia.
These nodules demonstrate increased resistance to vitamin D
and calcimimetic medications and may be the etiology of the
loss of negative feedback seen in 3° HPT.18,19
Figure 2. Radiograph of the hands of a 55-year-old patient with renal osteodystrophy and brown tumors of the fourth metacarpal and third phalanx of the left
hand (arrows). Image is courtesy of John Hunter, MD.
The Permanente Journal/Perm J 2016 Summer;20(3):15-127
The two most important sequelae of rHPT are 1) renal osteodystrophy and 2) cardiovascular disease. Recognizing that
the bone and cardiovascular complications seen in CKD are
manifestations of a broader interrelated syndrome, the National
Kidney Foundation initiated the term “CKD-mineral and bone
disorder” to describe the complex pathophysiology of the calcium, phosphorus, and PTH derangements seen in CKD. The
paradigm of “think beyond the bones” is emphasized to bring
early attention to the complications of rHPT in an attempt to
improve morbidity and mortality.20
Renal osteodystrophy refers to a group of bone disorders
caused by dysregulation of mineral metabolism in CKD,
including osteomalacia, adynamic bone disease, and osteitis
fibrosa cystica. Osteomalacia is a state of low bone turnover
leading to poor mineralization. Adynamic bone disease is also a
low-turnover pathology with normal mineralization that probably results from a low PTH state. The incidence of adynamic
bone disease increasing is likely secondary to PTH oversuppression from vitamin D agents, calcimimetics, and phosphate
binders.14,21 Osteitis fibrosis cystica is a high-turnover bone
disease that stems from elevated PTH concentrations stimulating osteoclast activity, bone breakdown, and resorption.
This can lead to subsequent bone pain and fractures.22 With
longstanding bone resorption, patients may develop localized
regions of bone loss that are then replaced by fibrous tissue,
resulting in a brown tumor. These “tumors” appear as welldefined, lytic lesions on radiograph and may be mistaken for
metastasis (Figure 2).
The derangements in calcium and phosphate that result from
rHPT may accelerate vascular calcification, including coronary
artery calcification. Calcification of the cardiovascular tissue
can affect the myocardium, atrial-ventricular conduction, and
valvular function.23 Furthermore, coronary calcification may
put patients at an increased risk of cardiovascular events and
death.24 It is difficult to distinguish the unique detrimental effects of rHPT from those of hyperphosphatemia, which is also
associated with cardiovascular disease in patients with CKD.
Some studies have suggested that FGF-23 may induce arterial smooth muscle myocytes to change into osteoblast-like
cells that lead to vascular calcification.17 Moderate to severe
hyperparathyroidism (PTH concentrations ≥ 600 pg/mL) may
increase risk of cardiovascular death,7 though the causality of
this association is debatable.
There is an association between CKD and medial calcification
in the arterioles of the skin and soft tissue leading to vascular
compromise and ulceration. This constellation of complications
was formerly called calciphylaxis but is now termed calcific
uremic arteriolopathy, and it is associated with an eight-fold
increase in mortality rate.25 Tumoral calcinosis is an uncommon
complication of longstanding rHPT and is classically associated
with high serum levels of calcium and phosphorus. In tumoral
calcinosis, the patient can develop soft-tissue calcium deposits
that can appear to be soft-tissue malignant tumors on imaging
studies (Figure 3).26
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Hyperparathyroidism of Renal Disease
The National Kidney Foundation previously recommended that
patients with CKD restrict dietary phosphorus to 800 to 1000
mg/day. However, it should be noted that there is a paucity of
good quality data regarding dietary phosphorus restriction and
outcomes in CKD.
Phosphate Binders
Figure 3. Radiograph of the right hip of a 63-year-old man with tumoral calcinosis.
DIAGNOSIS AND MANAGEMENT
The Kidney Disease: Improving Global Outcomes work
group recommends screening and management of rHPT be
initiated for all patients with CKD stage 3 (estimated GFR <
60 mL/min). The frequency of monitoring for serum calcium,
phosphorus, and PTH are listed in Table 1.27
The initial management of rHPT follows a stepwise approach with the goal of optimizing serum phosphorus and
calcium levels through a combination of a low phosphorus
diet, phosphate binders, vitamin D derivatives, and calcimimetic medications.
Low Phosphorus Diet
A low phosphorus diet is recommended for patients with
CKD and 2° HPT with hyperphosphatemia.27 Dietary restriction of phosphorus in patients without elevated levels of phosphorus, but with elevated PTH levels only, is controversial.
Unfortunately, this is very difficult given the high prevalence of
phosphorus in Western diets. Dietary phosphorus comes from 2
sources: 1) protein-rich food groups such as meat and milk; and
2) phosphorus additives, which are used to process meats and
cheeses. Phosphorus used as an additive is often only implied in
the ingredients list, and not individually reported on the food
label. Therefore, the true amount of phosphorus contained in a
product may be underestimated.14 Patient education regarding
this distinction may help them avoid phosphorous-rich foods.
Because of the difficulty in maintaining a low phosphorus
diet, phosphate binders are usually an essential part of medical
therapy for patients with CKD. Phosphate binders have been
shown to decrease serum phosphorous and PTH levels.28 Isakova et al29 reported that treatment with phosphorus binders
was independently associated with decreased mortality when
compared with no treatment.
Several phosphate binders are available, including aluminum
hydroxide, calcium salts, sevelamer hydrochloride, sevelamer
carbonate, and lanthanum carbonate. In general, aluminum
hydroxide should be limited to a short period because of the
risk of aluminum toxicity. Newer agents such as lanthanum have
unknown long-term effects of bone deposition. Iron-based binders such as sucroferric oxyhydroxide are also available to lower
serum phosphorous. The Kidney Disease Outcomes Quality
Initiative recommends for patients with CKD stages 3 and 4,
that phosphate binders be used if phosphorus levels cannot be
controlled within the target range despite dietary phosphorus
restriction. In patients who remain hyperphosphatemic despite
initiation of a single phosphate binder, combination therapy
can be used.23 It is interesting to note that lanthanum, being a
heavy metal, commonly shows up as radiopaque in noncontrast
radiologic studies of the gastrointestinal tract.30
Vitamin D Analogs
As described above, 1,25-OH vitamin D deficiency is a major mechanism of rHPT, and vitamin D replacement has been
shown to effectively suppress PTH secretion.31-34 Several forms
of vitamin D are available, including ergocalciferol (which requires activation in the kidney to 1,25-OH vitamin D), as well
as activated forms such as calcitriol, paricalcitol, and doxercalciferol. Although observational studies have suggested improved
survival in patients treated with vitamin D analogs, a 2007 metaanalysis showed no difference in mortality, bone pain, vascular
disease, or rate of parathyroidectomy when comparing patients
on vitamin D analogs versus those not taking vitamin D.14,35
The Kidney Disease: Improving Global Outcomes work group
recommends that in patients with CKD stages 3 to 5 (not on
dialysis), attempts to control hyperphosphatemia, hypocalcemia,
Table 1. Summary of National Kidney Foundation guidelines on evaluation of calcium and phosphorus metabolism and parathyroid
hormone
CKD stage
Progressive stage 3
Stage 4
Stage 5
GFR range (mL/min/1.73 m2)
30-59
15-29
< 15 or dialysis
Measure PTH
Baseline
6-12 months
3-6 months
Measure calcium and phosphorus
6-12 months
3-6 months
1-3 months
Target PTH (pg/mL)
< the upper limit of normal for assay
< the upper limit of normal for assay
2-9 x the normal limit of the assay
CKD = chronic kidney disease; GFR = glomerular filtration rate; PTH = parathyroid hormone.
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and vitamin D deficiency be made first. If PTH remains elevated
or is progressively rising, treatment with calcitriol or vitamin
D analogs is suggested. Close attention must be paid to serum
levels of calcium and phosphorus, which if greater than 10.2
mg/dL and 4.6 mg/dL, respectively, may warrant modification in
therapy. In patients with CKD stage 5 on dialysis, active vitamin
D sterols (such as calcitriol, paricalcitol, or doxercalciferol) are
used to control hyperparathyroidism.
Calcimimetics
Cinacalcet HCL is a calcimimetic agent that exhibits allosteric
modulation of the calcium receptor on the parathyroid gland, increasing sensitivity to extracellular calcium and thereby suppressing PTH secretion.36 The effectiveness of cinacalcet in lowering
PTH concentrations in ESRD patients has been demonstrated
in multiple studies. Combined analysis of these studies showed
that cinacalcet decreases rates of parathyroidectomy, fractures,
and cardiovascular hospitalization. Patients receiving cinacalcet
treatment rather than placebo also have improvements in selfreported physical function and less bodily pain.37
In 2012, the Evaluation of Cinacalcet Hydrochloride Therapy
to Lower Cardiovascular Events Trial randomized patients with
ESRD and moderate to severe rHPT to cinacalcet or placebo
and found that cinacalcet did not significantly reduce overall or
cardiovascular mortality.38 A recent Cochrane review corroborated these findings but did find that patients taking cinacalcet
had a significant increase in the rate of nausea, vomiting, and
hypocalcemia, suggesting that the potential risks associated with
cinacalcet use in ESRD patients may outweigh the benefits.39
These clinical uncertainties further bring into question the costs
of cinacalcet treatment. Currently the US spends $260 million
annually on cinacalcet, accounting for the largest single drug cost
in dialysis patients.40 Despite maximal medical interventions,
surgical parathyroidectomy is still required for many patients.41
Indications for Surgical Treatment
As stated in the Clinical Practice Guidelines for Bone Metabolism
and Disease in Chronic Kidney Disease, published in 2003 by the
Kidney Disease Outcomes Quality Initiative, the indications for
parathyroidectomy are not well defined. High-quality studies are
currently lacking to evaluate which patients might benefit from
parathyroidectomy. In lieu of such data, the National Kidney
Indications for Consideration for Parathyroidectomy
Medical management of rHPT > 6 months with
Hypercalcemia or hyperphosphatemia
PTH > 800 pg/mL
Calciphylaxis with documented elevated PTH levels
Osteoporosis (T-score > 2.5 SD below mean), pathologic
bone fracture
Symptoms/signs
Pruritus
Bone pain
Severe vascular calcifications
Myopathy
Foundation recommends that the criteria in the Sidebar: Indications for Consideration for Parathyroidectomy be used to merit
referral to an experienced surgeon for evaluation.42
The three most common surgical procedures used in the treatment of rHPT are total parathyroidectomy (TPX) alone, TPX
with auto-transplantation, and subtotal parathyroidectomy.21
Each of these procedures may be accompanied by a bilateral
cervical thymectomy to minimize the risk of recurrence.43
TPX involves identification and removal of all parathyroid
glands. This operation may be associated with the lowest rate
of recurrent hyperparathyroidism.44 The clear disadvantage of
TPX is permanent hypoparathyroidism, and patients undergoing TPX require lifelong calcium and vitamin D replacement. In
TPX with autotransplantation, all 4 glands are removed, followed
by autologous reimplantation of 20 mg to 70 mg of the most
normal-appearing gland into the sternocleidomastoid muscle,
pectoralis major muscle, or forearm brachioradialis muscle.
This implant typically takes 3 to 4 weeks to revascularize and
resume function. The advantage of removal and reimplantation of parathyroid tissue into an ectopic site is ease of access
in the event of recurrence and reoperation. This avoids the
morbidity associated with re-exploration of the neck. Subtotal
parathyroidectomy entails removal of 3½ parathyroid glands,
leaving the remaining partial gland intact in its original anatomic location. Subtotal parathyroidectomy has the advantage
of minimizing the period of postoperative hypoparathyroidism
and therefore likely shortens a patient’s hospital course, but it
requires reoperation in the neck in the event of a recurrence.
This may be associated with an increased risk of injury to the
recurrent laryngeal nerve. All 3 operations are accepted surgical
treatment options for rHPT, and each is associated with specific
advantages and disadvantages.45
Successful parathyroidectomy can dramatically improve
symptoms, including bone pain, arthralgia, muscle weakness,
and psychological disturbances.45,46 Biopsy-proven changes in
trabecular bone mineral content and accelerated bone formation have been demonstrated within 1 week after surgery.47
Parathyroidectomy is associated with a 30-day postoperative
mortality of 3.1% throughout the US.48 Other risks of surgery
include recurrent laryngeal nerve injury (< 2%) and hematoma
requiring re-exploration (< 1 %).
Several studies have suggested a survival benefit from parathyroidectomy in the treatment of rHPT, including significant
reductions in the incidence of major cardiovascular events and
all-cause mortality.49,50 Long-term relative risks of death are reduced by 10% to 15%, and long-term survival is improved compared with those not undergoing surgery.50 Parathyroidectomy
is effective in improving hemoglobin levels for ESRD-associated
anemia,51 and it has beneficial effects on the immune system
and overall nutrition.52 Parathyroidectomy has also been shown
to be more cost-effective than cinacalcet in nearly all dialysis
patient subgroups, with the exception of those with high operative mortality risk, patients remaining on dialysis for less than 7
months, and/or individuals expecting kidney transplant quickly.
PTH = parathyroid hormone; rHPT = renal hyperparathyroidism, SD = standard
deviation.
The Permanente Journal/Perm J 2016 Summer;20(3):15-127
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CONCLUSION
rHPT is a common complication of CKD that stems from hypocalcemia, reduced bioactivity of vitamin D, and elevated levels
of FGF-23. rHPT leads to a host of bone and cardiovascular
problems that ultimately can cause fractures, decreased quality
of life, and an increased risk of death. A range of nonsurgical
options are available, including initiating a low phosphorus diet,
phosphate binders, vitamin D analogs, and calcimimetic agents,
but unfortunately the data on the efficacy of these treatments
at improving overall and cardiovascular mortality are mixed.
Some patients require parathyroidectomy, which may improve
symptoms and reduce cardiovascular and overall mortality, but
it carries the expected risks of surgery. v
Author Contributions
Noah K Yuen, MD, provided study conception and design and participated
in analysis and interpretation of data and writing the manuscript. Shubha
Ananthakrishnan, MD, participated in writing the manuscript and in critical
revision of the manuscript. Michael J Campbell, MD, provided study conception
and design and participated in analysis and interpretation of data, writing the
manuscript, and the decision to submit for publication.
Disclosure Statement
The author(s) have no conflicts of interest to disclose.
Acknowledgment
Mary Corrado, ELS, provided editorial assistance.
How to Cite this Article
Yuen NK, Ananthakrishnan S, Campbell MJ. Hyperparathyroidism of renal
disease. Perm J 2016 Summer;20(3):15-127. DOI: http://dx.doi.org/10.7812/
TPP/15-127.
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in Chinese patients with renal failure undergoing long-term dialysis. Arch Surg 2007
Jul;142(7):644-8.
Yasunaga C, Nakamoto M, Matsuo K, Nishihara G, Yoshida T, Goya T. Effects of a
parathyroidectomy on the immune system and nutritional condition in chronic dialysis
patients with secondary hyperparathyroidism. Am J Surg 1999 Oct;78(4);332-6.
A Small Organ Hardly as Big as a Hemp Seed
About three years ago I found on the thyroid gland … a small organ,
hardly as big as a hemp seed, which was enclosed in the same
connective tissue capsule as the thyroid, but could be distinguished therefrom
by a lighter color. A superficial examination revealed an organ of totally
different structure from that of the thyroid, and with a very rich vascularity. …
[I] suggest the use of the name Glandulae parathyreoidea; a name in which
the characteristic of being bye-glands to the thyroid is expressed.
— Ivar Victor Sandström, 1852-1889, Swedish physician
The Permanente Journal/Perm J 2016 Summer;20(3):15-127
83
REVIEW ARTICLE
Recurrence of Epithelioid Hemangioendothelioma
during Pregnancy: Case Report and Systematic Review
Michael McCulloch, LAc, MPH, PhD; Michael Russin, MD; Arian Nachat, MD
Perm J 2016 Summer;20(3):15-152
E-pub: 07/25/2016 http://dx.doi.org/10.7812/TPP/15-152
ABSTRACT
Introduction: Epithelioid hemangioendothelioma (EHE) is a family of blood vessel
tumors originating in blood vessels, bone, brain, kidney, liver, and lung. EHE is more common in women, and chemotherapy, radiation, and surgery have brought few successes.
Case presentation: We present a case of a 28-year-old woman whose EHE recurred
during pregnancy, suggesting hormonal involvement. We conducted a systematic review to provide analysis and interpretation of the potential significance of her disease
recurring, with fatal outcome, during pregnancy.
Discussion: Very little research has explored the use of individual hormonal markers.
Strongly positive expression of placenta growth factor (PlGF) and 17-beta estradiol
receptors have been reported. Expression of PlGF is noteworthy in our case, in that our
patient’s disease quickly and dramatically flared in the 25th week of pregnancy, near the
peak in maternal PlGF production. PlGF binds to vascular endothelial growth factor-1
(VEGF-1), and PlGF may accelerate VEGF-induced angiogenesis. Taken together, these
factors may explain our patient’s EHE recurrence and rapid flare-up during pregnancy.
Treatment of EHE with VEGF inhibition, potentially in combination with other antiangiogenic and tumor-inhibiting therapies such as lenalidomide, thalidomide, sorafenib,
and sunitinib, may also hold promise.
INTRODUCTION
Epithelioid hemangioendothelioma
(EHE) is a family of vascular tumors,
originating in the endothelium and
sharing clinical characteristics with both
angiosarcoma and benign hemangioma.
EHE was first identified in 19821 and is
extremely rare, with an incidence rate
of 0.1 per 100,000, and fewer than
200 cases ever reported in the medical
literature.2 Because there is limited research on prognosis, a layperson registry
has been established. The International
Hemangioendothioma, Epithelioid
Hemangioendothelioma, and Related
Vascular Disorders Support Group has
tracked more than 260 patients.3
The clinical presentation of EHE is
quite varied; it can originate in bone,
brain, kidney, liver, lung, and vascular and other soft tissues. Diagnosis is
sometimes delayed owing to uncertainty
about correct pathologic classification,
which can significantly worsen prognosis.4 Little is known about prognostic
factors for patients with EHE, although
recent work has identified genetic alterations involving activation of the ROS1
receptor tyrosine kinase, which for other
cancers has led to effective therapies
working through ROS1 inhibition.5
Two case series have described the
prognosis of patients with hepatic EHE.
In a series from China (N = 33), survival
was longer in patients younger than age
47 years (hazard ratio, 7.0; p = 0.035),
in those without symptoms (hazard ratio, 86.5; p = 0.001), and in those with
serum cancer antigen 19-9 below 37
units/mL (hazard ratio, 5.0; p = 0.018).6
In a series from the United Kingdom
(N = 50), patients with bilateral hepatic
disease had shorter 5-year survival (51%)
compared with those with unilateral disease (81%), although the study size was
too small to show a significant difference
(p = 0.1). There was additionally nonsignificant lower 5-year survival in metastatic (69%) compared with localized
(78.3%) disease (p = 0.7). Treatment with
any chemotherapy decreased 5-year survival, compared with no chemotherapy
(43.6% vs 82.9%; p = 0.02).7
Diagnostic approaches to EHE include
computed tomography (CT),8 magnetic
resonance imaging,9,10 CT and magnetic
resonance imaging, 9 and serial bone
scintigraphy.11 (18)F-fluorodeoxyglucosepositron emission tomography with
strong (18)F-fluorodeoxyglucose uptake
has been used12 but is limited by lack of
correlation between lesion size and maximum standardized uptake value.13
Little is known about efficacy of therapy because the low incidence of EHE
precludes conduct of human clinical
trials. Options currently include chemotherapy, radiation, hormone therapy,
thermo-ablation, and surgery, although
most do not change the usually poor
prognosis of a diagnosis with EHE. In
patients with primary hepatic EHE,
overall survival is no different following
liver resection or transcatheter arterial
chemoembolization (p = 0.50). 6 Although patients with hepatic EHE have
longer median survival compared with
those with other hepatic vascular tumors,
in these patients surgical resection does
not improve survival.14
Development and testing of newer
therapies based on vascular endothelial growth factor (VEGF) inhibition
is supported by recent studies showing
positive expression of VEGF receptor
in biopsied lesions.15,16 Additional case
reports of success with lenalidomide,17
thalidomide,2 sorafenib (possessing both
Michael McCulloch, LAc, MPH, PhD, is the Research Lead for Integrative Medicine at the Walnut Creek Hospital in CA
and a Research Chief at the Pine Street Foundation in San Anselmo, CA. E-mail: [email protected].
Michael Russin, MD, is the Oncology Chief at the Walnut Creek Hospital in CA. E-mail: [email protected].
Arian Nachat, MD, is the Director of Integrative Medicine at the Walnut Creek Hospital in CA. E-mail: [email protected].
84
The Permanente Journal/Perm J 2016 Summer;20(3):15-152
REVIEW ARTICLE
Recurrence of Epithelioid Hemangioendothelioma during Pregnancy: Case Report and Systematic Review
antiangiogenic and antiproliferative activity),18 and sunitinib19 suggest other
targeted molecular therapies may also
hold promise.
The current case report documents diagnosis of recurrent EHE in a pregnant
woman and discusses the case in the context of a systematic review of the current
literature. This report was prepared in accordance with the CARE (CAse REport)
guidelines.20
Figure 1. Hematoxylin/eosin stain showing epithelioid cells with cytoplasmic vacuoles (magnification
×400).
Figure 2. Hematoxylin/eosin stain showing epithelioid cells with cytoplasmic vacuoles (magnification
×600).
Figure 3. Immunohistochemical stain positive for
vascular marker CD31 (magnification ×600).
Figure 4. Immunohistochemical stain positive for
vascular marker CD34 (magnification ×600).
The Permanente Journal/Perm J 2016 Summer;20(3):15-152
CASE PRESENTATION
We report a case of a 28-year-old
woman originally diagnosed with EHE
in 2002, at age 18 years. CT-guided
biopsy of 1 of her liver lesions revealed
EHE based on hematoxylin/eosin and immunohistochemical stains (Figures 1-4).
Repeated CT of her chest, abdomen, and
pelvis 3 months later showed progression
of disease. At that time she underwent 6
cycles of carboplatin and etoposide with
stabilization of disease; however, significant chest pain remained, requiring high
doses of opiates. She received 1 dose of
interferon, which was not tolerated. The
patient was then followed up with serial
CT scan showing stable disease through
2011 (Figures 5 and 6).
In 2012, the patient presented to the
Emergency Department with chest pain
and in acute respiratory distress. A posterior-anterior/lateral chest radiograph
revealed multiple pulmonary nodules bilaterally, confirmed as “innumerable” by
chest CT, along with bulky mediastinal
adenopathy and multiple liver lesions consistent with metastatic disease (Figure 7).
In mid-2012, the patient presented
with diffuse joint pain 6 months into
her first pregnancy, and went into labor
at 25 weeks. The baby was delivered and
died 8 days later. The patient’s pain then
continued to escalate and she developed
severe cough. Repeat CT scan of her chest,
abdomen, and pelvis revealed significant
progression of disease, especially in the
lungs and mediastinum. Biopsy of mediastinal adenopathy confirmed recurrent
EHE, and the diffuse nature of disease
precluded surgery.
The patient’s diffuse joint and bone
pain continued to worsen, resulting in
hospitalization for pain control. Bone
Figure 5. Computed tomography angiography of the
chest, showing stable disease in 2008.
Figure 6. Computed tomography angiography of the
chest, showing stable disease in 2011.
scan was consistent with hypertrophic
osteoarthropathy. During this time her
respiratory status continued to worsen:
chest CT revealed compression of the
right upper lobe bronchus and right pleural effusion. A right-sided chest tube was
inserted with drainage of a large amount
of pleural fluid and palliative radiation to
the mediastinal adenopathy was started.
Unfortunately the patient’s respiratory
status continued to decline from progressive disease as well as pneumonia. She
was intubated; her condition continued
to decline; she was placed on comfort
measures, and she subsequently died.
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Recurrence of Epithelioid Hemangioendothelioma during Pregnancy: Case Report and Systematic Review
A timeline showing progression of the
case is provided in Figure 8.
DISCUSSION
Figure 7. Computed tomography angiography of the
chest, following disease recurrence in 2012.
Despite numerous publications, EHE
remains a little-understood disease of poor
prognosis. In the case of localized disease,
prompt surgical resection appears to confer a survival advantage. Improvements in
early clinical identification of suspected
lesions may be accelerated by further research on the integration of tumor marker
and/or hormonal testing.
In Table 1 we present results of a systematic search of treatment outcomes
published since January 2011. Tumor
marker expression in EHE has been reported for endothelial markers (CD31,
CD34, and factor VIII-related antigen),21
VEGF and VEGF receptor 2,15 and strong
expression of CD31 and vimentin. 12
Errani et al22,23 reported that WWTR1CAMTA1 fusion is a genetic hallmark
of EHE, regardless of site of origin; they
also used reverse transcription-polymerase
chain reaction and gene sequencing to
Table 1. Epithelioid hemangioendothelioma primary tumor sites, first-line therapy, and maximum reported survival with therapy
86
Primary
tumor site
Extent
of disease
First-line
therapy
Author, year
Case series
Angelini et al,1 2014
Bone
Unifocal (49%);
multifocal (13%)
Wide excision or intralesional
surgery
Zheng et al,2 2012
Brain
Surgery
Agulnik et al,3 2013
Multifocal
Intracranial, with
localized extension to
bone and muscle
Metastatic
Wang et al,4 2012
Liver
Localized and
extrahepatic
Theodosopoulos et al,5
2013
Case reports
Gherman and Fodor,6
2011
Sumrall et al,7 2010
Intracranial
Osawa et al,8 2012
Patient(s)
Survival
N = 62; men, n = 39;
women, n = 23; mean
age = 39 years
25-year-old man;
44-year-old woman
Survival at 10 years:
unifocal, 97%; multifocal,
74%
9 years
Bevacizumab
N=7
N = 33
Metastatic
Liver resection, transcatheter
arterial chemoembolization
(TACE), resection and TACE,
or liver transplantation
Surgery
Partial response, n = 2;
stable disease, n = 4;
progressive disease, n = 1
Up to 3 years of follow-up
N = 38; men, n = 23;
women, n = 15
2 months-11 years
Bone
Localized
Wide surgical excision
24-year-old man
Brain
Lenalidomide
31-year-old woman
Carotid artery
Intracranial, localized
extension to skull,
connective tissue
Localized
No local recurrence or
metastasis at 2 years
6 years, stable disease
Surgery
Tolkach et al,9 2012
Harada et al,10 2011
Kidney
Liver
Metastatic
Localized
Grenader et al,11 2011
Liver
Localized
Sunitinib
Transcatheter arterial
chemoembolization
Pegylated liposomal
doxorubicin
59-year-old man; 14
years after embolization
for carotid aneurysm
53-year-old man
83-year-old man
Sangro et al,12 2012
Salech et al,13 2011
Mizota et al,14 2011
Iimuro et al,15 2012
Liver
Liver
Lung
Retroperitoneum
Kerry et al,16 2012
Spinal region
Metastatic to lungs
Metastatic to lungs
Localized
Localized, then distant
lymph metastasis
months later
Multifocal
De Palma et al,17 2012
Vascular
Localized
Rapid death
Sorafenib
Thalidomide
Bevacizumab
Surgical removal of both
occurrences
22-year-old man
40-year-old woman
59-year-old woman
48-year-old woman
Endovascular embolization,
radiochemotherapy
Surgical removal of entire
azygos vein
25-year-old man
3 years, stable disease
Metastatic recurrence
after 3 months
2 years, stable disease
with maintenance therapy
at time of publication
2 years
9 years, stable disease
3 months
No recurrence at 13
months after resection of
metastasis
8 weeks
47-year-old man
No recurrence at 1 year
32-year-old man
(Continued on next page)
The Permanente Journal/Perm J 2016 Summer;20(3):15-152
REVIEW ARTICLE
Recurrence of Epithelioid Hemangioendothelioma during Pregnancy: Case Report and Systematic Review
ascertain that in multifocal EHE, those
multiple sites are monoclonal in nature,
and therefore metastatic implants of the
same tumor and not simultaneous occurrence of multiple neoplastic clones.
Additionally, both CD31 and VEGF
are overexpressed in non-small cell lung
cancer,24 breast cancer,25 prostate cancer,26 renal cell carcinoma,27 mantle cell
lymphoma, 28 meningioma, 29 pituitary
adenomas,30 and uveal melanoma.31
EHE is more common in women,
and there are 3 prior case reports of its
diagnosis during pregnancy,17 with ours
being the fourth. A case report has also
been published of successful management
of multifocal hepatic infantile hemangioendothelioma with tamoxifen-based
therapy.32 Tamoxifen (20 mg daily) was
part of the management strategy used for
our patient over a 9-day course during her
acute disease recurrence.
Very little research has explored the
clinical utility of individual hormonal
markers in EHE. There was strongly positive expression of placenta growth factor
(PlGF) in 1 case,33 positive expression of
17-beta estradiol receptors in only 1 of a
series of 5 EHE patients,34 and no estrogen or progesterone receptors in another
case.35 Expression of PlGF is noteworthy
in our case, in that our patient’s disease
quickly and dramatically flared in the
(Continued from previous page)
Primary
Author, year
tumor site
Case reports (continued)
Wu et al,18 2014
Vascular
Extent
of disease
First-line
therapy
Patient(s)
Localized
Surgery
58-year-old woman
Carboplatin, pharmorubucin
24-year-old woman
Excisional biopsy
22-year-old woman
Carboplatin, docetaxel,
pharmorubucin
Carboplatin/etoposide,
followed by surgical excision
49-year-old woman
Demir et al,19 2013
Liver
Kiratli et al,20 2013
Eyelid
Parenchymal lesion
with metastases to lung
Localized
Pálföldi et al,21 2013
Lung
Metastatic to bone
Yu et al,22 2013
Lung
Lung (localized to
myocardium)
39-year-old woman
Survival
2 years, stable at time of
publication
No recurrence at 44
months
Stable disease 1 year
after diagnosis
Alive 14 months after
surgery
Angelini A, Mavrogenis AF, Gambarotti M, Merlino B, Picci P, Ruggieri P. Surgical treatment and results of 62 patients with epithelioid hemangioendothelioma of bone. J Surg Oncol
2014 Jun;109(8):791-7. DOI: http://dx.doi.org/10.1002/jso.23587.
2
Zheng J, Liu L, Wang J, Wang S, Cao Y, Zhao J. Primary intracranial epithelioid hemangioendothelioma: a low-proliferation tumor exhibiting clinically malignant behavior. J Neurooncol
2012 Oct;110(1):119-27. DOI: http://dx.doi.org/10.1007/s11060-012-0945-x.
3
Agulnik M, Yarber JL, Okuno SH, et al. An open-label, multicenter, phase II study of bevacizumab for the treatment of angiosarcoma and epithelioid hemangioendotheliomas. Ann
Oncol 2013 Jan;24(1):257-63. DOI: http://dx.doi.org/10.1093/annonc/mds237.
4
Wang LR, Zhou JM, Zhao YM, et al. Clinical experience with primary hepatic epithelioid hemangioendothelioma: retrospective study of 33 patients. World J Surg 2012
Nov;36(11):2677-83. DOI: http://dx.doi.org/10.1007/s00268-012-1714-x.
5
Theodosopoulos T, Dellaportas D, Tsangkas A, et al. Clinicopathological features and management of hepatic vascular tumors. A 20-year experience in a Greek University Hospital. J
BUON 2013 Oct-Dec;18(4):1026-31.
6
Gherman CD, Fodor D. Epithelioid hemangioendothelioma of the forearm with radius involvement. Case report. Diagn Pathol 2011 Dec 6;6:120. DOI: http://dx.doi.org/10.1186/1746-1596-6-120.
7
Sumrall A, Fredericks R, Berthold A, Shumaker G. Lenalidomide stops progression of multifocal epithelioid hemangioendothelioma including intracranial disease. J Neurooncol 2010
Apr;97(2):275-7. DOI: http://dx.doi.org/10.1007/s11060-009-0017-z.
8
Osawa S, Saito A, Shimizu H, Ogawa T, Watanabe M, Tominaga T. A case of intravascular epithelioid hemangioendothelioma occurring 14 years after coil embolization for an extracranial
internal carotid artery aneurysm. J Vasc Surg 2012 Jan;55(1):230-3. DOI: http://dx.doi.org/10.1016/j.jvs.2011.06.108.
9
Tolkach Y, Petrov S, Lerut E, Van Poppel H. Epithelioid hemangioendothelioma of the kidney treated with sunitinib. Onkologie 2012;35(6):376-8. DOI: http://dx.doi.org/10.1159/000338944.
10
Harada J, Yoshida H, Ueda J, et al. Malignant hepatic epithelioid hemangioendothelioma with abdominal pain due to rapid progression. J Nippon Med Sch 2011;78(4):246-51. DOI: http://
dx.doi.org/10.1272/jnms.78.246.
11
Grenader T, Vernea F, Reinus C, Gabizon A. Malignant epithelioid hemangioendothelioma of the liver successfully treated with pegylated liposomal doxorubicin. J Clin Oncol 2011 Sep
1;29(25):e722-4. DOI: http://dx.doi.org/10.1200/jco.2011.35.5891.
12
Sangro B, Iñarrairaegui M, Fernández-Ros N. Malignant epithelioid hemangioendothelioma of the liver successfully treated with Sorafenib. Rare Tumors 2012 Apr 12;4(2):e34. DOI: http://
dx.doi.org/10.4081/rt.2012.e34.
13
Salech F, Valderrama S, Nervi B, et al. Thalidomide for the treatment of metastatic hepatic epithelioid hemangioendothelioma: a case report with a long term follow-up. Ann Hepatol 2011
Jan-Mar;10(1):99-102.
14
Mizota A, Shitara K, Fukui T. Bevacizumab chemotherapy for pulmonary epithelioid hemangioendothelioma with severe dyspnea. J Thorac Oncol 2011 Mar;6(3):651-2. DOI: http://dx.doi.
org/10.1097/jto.0b013e31820b9e23.
15
Iimuro Y, Nakai N, Asano Y, et al. Primary epithelioid hemangioendothelioma of the retroperitoneum: report of a case. Surg Today 2012 Oct;42(10):1026-31. DOI: http://dx.doi.org/10.1007/
s00595-012-0173-1.
16
Kerry G, Marx O, Kraus D, et al. Multifocal epithelioid hemangioendothelioma derived from the spine region: case report and literature review. Case Rep Oncol 2012 Jan;5(1):91-8. DOI:
http://dx.doi.org/10.1159/000336947.
17
De Palma A, Pagliarulo V, Ardò N, Loizzi D. Surgical treatment of a rare case of epithelioid hemangioendothelioma of the azygos vein. Interact Cardiovasc Thorac Surg 2012 Jan;14(1):913. DOI: http://dx.doi.org/10.1093/icvts/ivr064.
18
Wu XN, Chen MJ, Li DQ, Hu JG, Yu FL. Pulmonary artery pseudoaneurysm caused by a rare vascular tumor: epithelioid hemangioendothelioma. Thorac Cardiovasc Surg 2014
Feb;62(1):92-4. DOI: http://dx.doi.org/10.1055/s-0031-1299588.
19
Demir L, Can A, Oztop R, et al. Malignant epithelioid hemangioendothelioma progressing after chemotherapy and Interferon treatment: a case presentation and a brief review of the
literature. J Cancer Res Ther 2013 Jan-Mar;9(1):125-7. DOI: http://dx.doi.org/10.4103/0973-1482.110386.
20
Kiratli H, Tarlan B, Ruacan S. Epitheloid hemangioendothelioma of the palpebral lobe of the lacrimal gland. Orbit 2013 Apr;32(2):120-3. DOI: http://dx.doi.org/10.3109/01676830.2013.764443.
21
Pálföldi R, Radács M, Csada E, et al. Pulmonary epithelioid haemangioendothelioma studies in vitro and in vivo: new diagnostic and treatment methods. In Vivo 2013 Mar-Apr;27(2):221-5.
22
Yu L, Gu T, Xiu Z, Shi E, Zhao X. Primary pleural epithelioid hemangioendothelioma compressing the myocardium. J Card Surg 2013 May;28(3):266-8. DOI: http://dx.doi.org/10.1111/jocs.12094.
1
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Recurrence of Epithelioid Hemangioendothelioma during Pregnancy: Case Report and Systematic Review
Figure 8. Timeline of the patient’s case.
CT = computed tomography scan.
25th week of pregnancy, near the peak
in maternal PlGF production. Although
in our patient’s case PlGF was not tested,
we did note an abnormally low human
chorionic gonadotropin level during
the second trimester of pregnancy of
23 IU/mL.
A translocation involving PlGF has
also been discovered in a case of EHE.15
Furthermore, it is known that there is
binding of PlGF to VEGF receptor-1,
and that PlGF may influence VEGFinduced angiogenesis,36 which may explain our patient’s rapid disease flare-up.
Although the scarcity of cases impedes rapid progress in histochemical
characterization of EHE, a composite
picture has begun to emerge that may
aid researchers in its early identification, perhaps leading to earlier diagnosis
and more definitive treatment. VEGF
expression 15 and hormonal receptor
expression have been reported in EHE.
Furthermore, there are multiple reports
of successful management of this vascular cancer with antiangiogenic therapy
(lenalidomide, 17,18 thalidomide, 2,37-39
and sorafenib18). We therefore suggest
it is possible that combination therapy
of EHE with sequenced or concurrent
88
anti-angiogenic, hormonal, and antiVEGF agents has value as an avenue of
future clinical investigation. v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
Acknowledgment
Mary Corrado, ELS, provided editorial assistance.
How to Cite this Article
McCulloch M, Russin M, Nachat A. Recurrence
of epithelioid hemangioendothelioma during
pregnancy: Case report and systematic review.
Perm J 2016 Summer;20(3):15-152.
DOI: http://dx.doi.org/10.7812/TPP/15-152
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Turaga KK. Does histology predict outcome for
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org/10.1002/jso.23517.
15. Matsuzawa S, Kanazawa T, Yamaguchi T, Nishino H,
Kawada K, Ichimura K. Case of high-risk epithelioid
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hed.23160.
16. Park MS, Ravi V, Araujo DM. Inhibiting the VEGFVEGFR pathway in angiosarcoma, epithelioid
hemangioendothelioma, and hemangiopericytoma/
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cco.0b013e32833aaad4.
17. Sumrall A, Fredericks R, Berthold A, Shumaker G.
Lenalidomide stops progression of multifocal
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intracranial disease. J Neurooncol 2010
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s11060-009-0017-z.
18. Sangro B, Iñarrairaegui M, Fernández-Ros N.
Malignant epithelioid hemangioendothelioma of
the liver successfully treated with Sorafenib. Rare
Tumors 2012 Apr 12;4(2):e34. DOI: http://dx.doi.
org/10.4081/rt.2012.e34.
The Permanente Journal/Perm J 2016 Summer;20(3):15-152
REVIEW ARTICLE
Recurrence of Epithelioid Hemangioendothelioma during Pregnancy: Case Report and Systematic Review
19. Tolkach Y, Petrov S, Lerut E, Van Poppel H.
Epithelioid hemangioendothelioma of the kidney
treated with sunitinib. Onkologie 2012;35(6):376-8.
DOI: http://dx.doi.org/10.1159/000338944.
20. Gagnier JJ, Kienle G, Altman DG, Moher D, Sox H,
Riley D; CARE Group. The CARE guidelines:
consensus-based clinical case report guideline
development. J Clin Epidemiol 2014 Jan;67(1):46-51.
DOI: http://dx.doi.org/10.1016/j.jclinepi.2013.08.003.
21. Zhao AL, Zhou LX, Li XH. [Hepatic epithelioid
hemangioendothelioma in needle biopsy specimens:
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Jan;40(1):23-6.
22. Errani C, Sung YS, Zhang L, Healey JH,
Antonescu CR. Monoclonality of multifocal epithelioid
hemangioendothelioma of the liver by analysis
of WWTR1-CAMTA1 breakpoints. Cancer Genet
2012 Jan-Feb;205(1-2):12-7. DOI: http://dx.doi.
org/10.1016/j.cancergen.2011.10.008.
23. Errani C, Zhang L, Sung YS, et al. A novel WWTR1CAMTA1 gene fusion is a consistent abnormality
in epithelioid hemangioendothelioma of different
anatomic sites. Genes Chromosomes Cancer 2011
Aug;50(8):644-53. DOI: http://dx.doi.org/10.1002/
gcc.20886.
24. Mineo TC, Ambrogi V, Baldi A, et al. Prognostic
impact of VEGF, CD31, CD34, and CD105
expression and tumour vessel invasion after radical
surgery for IB-IIA non-small cell lung cancer. J Clin
Pathol 2004 Jun;57(6):591-7. DOI: http://dx.doi.
org/10.1136/jcp.2003.013508.
25. Arihiro K, Kaneko M, Fujii S, Inai K. Loss of CD9 with
expression of CD31 and VEGF in breast carcinoma,
as predictive factors of lymph node metastasis.
Breast Cancer 1998 Apr 25;5(2):131-8. DOI: http://
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26. Ding GF, Li JC, Xu YF, Sun Y, Tao L. [Correlation
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the vascular density of VEGF expression with
microvascular density determined with CD34
and CD31 staining and conventional prognostic
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2007;39(3):691-8. DOI: http://dx.doi.org/10.1007/
s11255-006-9123-4.
Molinský J, Klánová M, Maswabi B, et al. In vivo
growth of mantle cell lymphoma xenografts in
immunodeficient mice is positively regulated by
VEGF and associated with significant up-regulation
of CD31/PECAM1. Folia Biol (Praha) 2013;59(1):
26-31.
Lewy-Trenda I, Omulecka A, Janczukowicz J,
Papierz W. The morphological analysis of vasculature
and angiogenic potential in meningiomas:
immunoexpression of CD31 and VEGF antibodies.
Folia Neuropathol 2003;41(3):149-53.
Cristina C, Perez-Millan MI, Luque G, et al. VEGF
and CD31 association in pituitary adenomas. Endocr
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org/10.1007/s12022-010-9119-6.
Mouriaux F, Sanschagrin F, Diorio C, et al. Increased
HIF-1α expression correlates with cell proliferation
and vascular markers CD31 and VEGF-A in uveal
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iovs.13-13345.
Sondhi V, Kurkure PA, Vora T, et al. Successful
management of multi-focal hepatic infantile
hemangioendothelioma using TACE/surgery followed
by maintenance metronomic therapy. BMJ Case Rep
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bcr.12.2011.5456.
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Ohori NP, Yousem SA, Sonmez-Alpan E, Colby
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10.1159/000082932.
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Dec 22;4:413. DOI: http://dx.doi.org/10.1186/17521947-4-413.
All Attempts at a Rational Method of Cure
The main part of the science of disease is of a purely descriptive character,
a scientific interpretation of facts and a clear insight into the intimate
connection subsisting between different phenomena, which may precede all
attempts at a rational method of cure, having been attained in a few instances
only. … Therapeutic researchers must be regulated in the same manner as
pathological. … The more careful tracing of the progress of morbid processes,
and the insight into their modes of origin and retrogression, enable us to
determine the principles of treatment with greater clearness than formerly.
— Friedrich Theodor von Frerichs, 1819-1885, German pathologist
The Permanente Journal/Perm J 2016 Summer;20(3):15-152
89
COMMENTARY
Quality Over Quantity: Integrating Mental Health
Assessment Tools into Primary Care Practice
Darrell L Hudson, PhD, MPH
E-pub: 06/17/2016
ABSTRACT
Depression is one of the most common, costly, and debilitating
psychiatric disorders in the US. There are also strong associations
between depression and physical health outcomes, particularly
chronic diseases such as diabetes mellitus. Yet, mental health
services are underutilized throughout the US. Recent policy
changes have encouraged depression screening in primary care
settings. However, there is not much guidance about how depression screeners are administered. There are people suffering
from depression who are not getting the treatment they need. It is
important to consider whether enough care is being taken when
administering depression screeners in primary care settings.
I was at the doctor’s office, a family medicine practice for a
routine check-up.
“I have to ask you these questions about mental health,” the
nurse said sheepishly after recording my heart rate and blood
pressure.
The preface immediately put me on guard and I tensed up.
On the one hand, I thought, does anyone suspect that something is wrong with me? Could they tell I was anxious because
I forgot to get cash and would have to dive for quarters in my
glove box to get out of their parking deck? On the other hand,
I conduct mental health research, so I knew the nurse was
probably going to ask me questions from the Patient Health
Questionnaire (PHQ). I was encouraged that mental health was
being integrated into a medical visit in a primary care setting.
During the past two weeks, have you found little interest or
pleasure in doing things?
Have you felt down, depressed, or hopeless?
The answer to both of these questions was no. But the opening
statement from the nurse about her obligation to ask questions
about mental health set me on edge a bit. The nurse’s demeanor
changed from when she was taking my blood pressure and recording my weight. In one sentence, she made it abundantly
clear that she was asking only because of obligation, she was
not comfortable asking, and she was not particularly interested
in hearing my answers to the questions. I wondered, if I was
feeling down or losing interest in doing things I had previously
enjoyed, would I feel comfortable telling her? Considering her
apparent disinterest, did she even care? Would I believe that she
would do anything about my feelings?
Depression is one of the most common, costly, and debilitating conditions in the US, affecting millions of Americans
each year.1-5 Disability from depression is associated with lower
Perm J 2016 Summer;20(3):15-148
http://dx.doi.org/10.7812/TPP/15-148
educational attainment and income earned as well as increased
days off work.6-10 Depression is also associated with suicide11-13
in addition to a wide range of chronic diseases such as heart
disease and diabetes mellitus.14-18 Recent national policy changes
related to mental health coverage, namely the Patient Protection
and Affordable Care Act of 201019 and the Mental Health Parity
and Addiction Equity Act,20 have promoted the integration of
mental health screening and treatment into primary care settings. Indeed, most patients are initially diagnosed and treated
for mental health problems within primary care settings.21,22
Many practices and health care systems, such as Kaiser Permanente, use the PHQ to screen for mental health problems.
Results from numerous studies indicate that this measure is
effective in screening for mental health problems in primary
care settings; even versions with fewer items do a good job of
identifying depression.23-25
Although there are numerous resources that describe different
versions of the PHQ as well as information about reliability and
validity, in addition to steps on how to score the screener, there
are no clear guidelines about how clinicians should go about
asking patients questions about their mental health. However,
the manner in which questions are asked and by whom have a
profound effect on the answers that patients provide.26,27 This is
especially true when asking about sensitive information.27 Race/
ethnicity, sex, social class, and sexual orientation are additional
considerations that mental health service clinicians must contend with and which make recognition and treatment of depression even more challenging. Further, mental health conditions
remain highly stigmatized. This seems to be an important factor
that should be addressed at the individual clinician level as well
as at the system level.
Practices and health care plans should be applauded for taking steps to integrate mental health and primary care. Despite
the efficacy and effectiveness of the PHQ, I wondered how
probable someone suffering from depression would be to share
such feelings during a similar clinical interaction. I wondered
if the nurse’s preface and, more importantly, her demeanor
would affect the comfort of patients who do suffer from mental health problems and give them pause about answering the
questions honestly.
Is it enough to simply ask questions, especially if the person
asking the question does not seem the least bit interested or
enthused about doing so? If the goal is to screen patients who
may be suffering from depression and other mental health
problems, there must be better care in the administration of
Darrell L Hudson, PhD, MPH, is an Assistant Professor at the Brown School of Social
Work at Washington University in St Louis, MO. E-mail: [email protected].
90
The Permanente Journal/Perm J 2016 Summer;20(3):15-148
COMMENTARY
Quality Over Quantity: Integrating Mental Health Assessment Tools into Primary Care Practice
the PHQ within primary care settings. If patients are anxious
about their answers or fear judgment, they might give biased
answers. And that will not help anyone. If the nurse’s preface to
the questions put me on guard, I wondered how other primary
care patients might feel.
A search of the literature for best practices in administering
the PHQ or other depression screeners did not produce any specific guidelines to help clinicians to most effectively administer
these instruments. However, clinicians could help to mitigate
stigma by establishing rapport and asking about patients’ overall
well-being, whether they are feeling very stressed, and whether
there have been any substantial changes in their lives. It may
also help to have physicians incorporate these questions into
their general physical examination so that patients understand
that mental health is essential to overall well-being. Furthermore, there should be clinician continuity in who administers
depression screeners. In my case, a nurse with whom I do not
recall interacting before my visit administered the PHQ before
I saw my regular physician. I did not have a relationship with
her and would have found the screener questions less obtrusive
if they were incorporated into time with the physician, whom I
have been seeing for several years. The PHQ and other depression screeners avoid psychiatric terms that may be stigmatized
or confusing to patients. Similarly, clinicians should avoid these
terms. Additionally, once clinicians ask questions about mental
health, they must be prepared to discuss the challenges that patients are facing and be ready to provide referrals and resources
to help patients with mental health conditions.
There are probably many missed opportunities to address the
mental health needs of Americans. It is no secret that mental
health services are underutilized in the US.28-30 Fewer than
half of the people who have a mental health problem ever
seek services.31 Even in highly vulnerable populations, like
those who have diabetes, depression recognition (eg, diagnosis, medication, referral to mental health specialty care) can
be poor.32 It is probable that there are patients suffering from
mental health problems who do not seek treatment or who are
not being recognized with these problems when they interact
with clinicians for medical concerns. It is important to consider whether enough care is being taken when administering
depression screeners in primary care settings. Furthermore, it
may be important to alert patients that they should expect to
be screened for mental health issues even if they are visiting
for their physical examinations. v
Disclosure Statement
This work was supported by the Barnes-Jewish Hospital Foundation in
addition to Grant Number 1P30DK092950 from the National Institute of
Diabetes and Digestive and Kidney Diseases, and its contents are solely the
responsibility of the authors and do not necessarily represent the official views
of the National Institute of Diabetes and Digestive and Kidney Diseases. The
funding agreement ensured the authors’ independence in designing the study,
collecting and interpreting the data, writing, and publishing the results.
The author(s) have no other conflicts of interest to disclose.
Acknowledgment
Mary Corrado, ELS, provided editorial assistance.
The Permanente Journal/Perm J 2016 Summer;20(3):15-148
How to Cite this Article
Hudson DL. Quality over quantity: integrating mental health assessment
tools into primary care practice. Perm J 2016 Summer;20(3):15-148.
DOI: http://dx.doi.org/10.7812/TPP/15-148
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22. US Preventive Services Task Force. Screening for depression: recommendations
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Mental Distress
Every day brought some fresh proof of how great was the
influence of mental distress in augmenting bodily pain and
sickness. Whatever circumstances were calculated to make
a strong impression upon the spirits, threw them back at
once from a state of convalescence, into absolute disease
… . Passions and affections of the mind are wont to show
their power over the body especially by the manner in which
they influence the heart, even the healthy heart; rousing it to
tumultuous and irregular action and engendering pain within it.
— Peter Mere Latham, 1789-1875, physician and medical educator
92
The Permanente Journal/Perm J 2016 Summer;20(3):15-148
COMMENTARY
Plant-Based Diets: A Physician’s Guide
Julieanna Hever, MS, RD, CPT
Perm J 2016 Summer;20(3):15-082
E-pub: 07/06/2016 http://dx.doi.org/10.7812/TPP/15-082
ABSTRACT
Because of the ever-increasing body of evidence in support of the health advantages
of plant-based nutrition, there is a need for guidance on implementing its practice. This
article provides physicians and other health care practitioners an overview of the myriad
benefits of a plant-based diet as well as details on how best to achieve a well-balanced,
nutrient-dense meal plan. It also defines notable nutrient sources, describes how to get
started, and offers suggestions on how health care practitioners can encourage their
patients to achieve goals, adhere to the plan, and experience success.
SUMMARY OF HEALTH BENEFITS
Plant-based nutrition has exploded in
popularity, and many advantages have
been well documented over the past several decades.1 Not only is there a broad
expansion of the research database supporting the myriad benefits of plant-based
diets, but also health care practitioners
are seeing awe-inspiring results with
their patients across multiple unique
subspecialties. Plant-based diets have
been associated with lowering overall
and ischemic heart disease mortality2;
supporting sustainable weight management3; reducing medication needs4-6; lowering the risk for most chronic diseases7,8;
decreasing the incidence and severity of
high-risk conditions, including obesity,9
hypertension,10 hyperlipidemia,11 and hyperglycemia;11 and even possibly reversing
advanced coronary artery disease12,13 and
type 2 diabetes.6
The reason for these outcomes is twofold. First, there are inherent benefits to
eating a wide variety of health-promoting
plants. Second, there is additional benefit
from crowding out—and thereby avoiding—the injurious constituents found in
animal products, including the following:
• Saturated fats: Saturated fats are a
group of fatty acids found primarily in
animal products (but also in the plant
kingdom—mostly in tropical oils, such
as coconut and palm) that are well established in the literature as promoting
cardiovascular disease (CVD).14,15 The
American Heart Association lowered its
recommendations15 for a heart-healthy
diet to include no more than 5% to
6% of total calories from saturated fat,
which is just the amount found naturally in a vegan diet (one consisting of
no animal products).
• Dietary cholesterol: Human bodies
produce enough cholesterol for adequate functioning. Although evidence
suggests that dietary cholesterol may
only be a minor player in elevated serum
cholesterol levels, high intakes are linked
to increased susceptibility to low-density
lipoprotein oxidation, both of which
are associated with the promotion of
CVD.16-18 Dietary cholesterol is found
almost exclusively in animal products.
• Antibiotics: The vast majority (70% to
80%) of antibiotics used19,20 in the US
are given to healthy livestock animals
to avoid infections inherent in the
types of environments in which they
are kept. This is, therefore, the number one contributor to the increasingly
virulent antibiotic-resistant infections
of the type that sickened 2 million and
killed 23,000 Americans in 2013.20
• Insulin-like growth factor-1: Insulinlike growth factor-1 is a hormone
naturally found in animals, including humans. This hormone promotes
growth. When insulin-like growth
factor-1 is consumed, not only is the
added exogenous dose itself taken in,
but because the amino acid profile
typical of animal protein stimulates
the body’s production of insulin-like
growth factor-1, more is generated
endogenously.21 Fostering growth as a
full-grown adult can promote cancer
proliferation.
• Heme iron: Although heme iron, found
in animal products, is absorbed at a
higher rate than nonheme iron, found
in plant-based and fortified foods,
absorption of nonheme iron can be
increased by pairing plant-based protein sources with foods high in vitamin
C.22 Additionally, research suggests that
excess iron is pro-oxidative23 and may
increase colorectal cancer risk 24 and
promote atherosclerosis25 and reduced
insulin sensitivity.26
• Chemical contaminants formed from
high temperature cooking of cooked
animal products: When flesh is cooked,
compounds called polycyclic aromatic
hydrocarbons,27 heterocyclic amines,28
and advanced glycation end products29
are formed. These compounds are
carcinogenic, pro-inflammatory, prooxidative, and contributive to chronic
disease.
• Carnitine: Carnitine, found primarily in meat, may be converted in the
body by the gut bacteria to produce
trimethylamine N-oxide (TMAO).
High levels of trimethylamine n-oxide
are associated with inflammation, atherosclerosis, heart attack, stroke, and
death.30
• N-Glycolylneuraminic acid (Neu5Gc):
This compound is found in meat and
promotes chronic inflammation.31,32
On the other hand, there are infinite
advantages to the vast array of nutrients
found in plant foods. Phytochemicals
and fibers are the two categories of nutrients that are possibly the most health
promoting and disease fighting. Plants are
the only source of these nutrients; they
are completely absent in animals. Plants
contain thousands of phytochemicals,
Julieanna Hever, MS, RD, CPT, is a Dietitian and Author in Los Angeles, CA.
E-mail: [email protected].
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93
COMMENTARY
Plant-Based Diets: A Physician’s Guide
such as carotenoids, glucosinolates, and
flavonoids, which perform a multitude of
beneficial functions, including:
• Antioxidation, neutralizing free radicals33
•Anti-inflammation34
• Cancer activity reduction via several
mechanisms, including inhibiting tumor growth, detoxifying carcinogens,
retarding cell growth, and preventing
cancer formation35
• Immunity enhancement36
• Protection against certain diseases, such
as osteoporosis, some cancers, CVD,
macular degeneration, and cataracts37-39
• Optimization of serum cholesterol.40,41
Fibers found in whole plant foods
powerfully support the gastrointestinal,
cardiovascular, and immune systems
through multiple mechanisms. Yet more
than 90% of adults and children in the US
do not get the minimum recommended
dietary fiber.42
Thus, it can be advantageous for physicians to recommend and support plantbased eating to achieve optimal health
outcomes and possibly minimize the need
for procedures, medications, and other
treatments. Aiming for lifestyle changes
as primary prevention has been estimated
to save upwards of 70% to 80% of health
care costs because 75% of health care
spending in the US goes to treat people
with chronic conditions.43 Offering this
option and guiding patients through the
logistics and their concerns about plantbased eating is a viable first line of therapy
in the clinical setting. This article will
delineate how best to achieve a well-balanced, nutrient-dense meal plan, define
notable nutrient sources, describe how
to get started, and offer suggestions on
how physicians can encourage and work
with their patients who are interested to
maintain adherence and enjoy success.
NOTABLE NUTRIENTS
Although nutrient deficiency is a
primary concern for many people when
considering plant-based eating, the Academy of Nutrition and Dietetics states44
that “vegetarian diets, including total
vegetarian or vegan diets, are healthful,
nutritionally adequate, and may provide
health benefits in the prevention and treatment of certain diseases.” The Academy’s
position paper goes on to conclude that
94
Table 1. Food group recommended servings per day
Food group
Vegetables, all types, including starchy
Fruits, all types
Whole grains (eg, quinoa, brown rice, oats)
Legumes (beans, peas, lentils, soy foods)
Leafy green vegetables (eg, kale, lettuce,
broccoli)
Nuts (eg, walnuts, almonds, pistachios)
Seeds (eg, chia, hemp, and flax seeds)
Fortified plant milks (eg, soy, almond, cashew)
Fresh herbs and spices
“well-planned vegetarian diets are appropriate for individuals during all stages of
the life cycle, including pregnancy, lactation, infancy, childhood, and adolescence,
and for athletes.” Because any type of meal
plan should be approached with careful
thought, it is helpful to note that plantbased diets, including calorie-restricted,
weight-loss diets, have been found to be
more nutritionally sound than typical
dietary patterns.45
A well-balanced, plant-based diet is
composed of vegetables, fruits, whole
grains, legumes, herbs, spices, and a small
amount of nuts and seeds. Half of the plate
should consist of vegetables and fruits in
accordance with the US Department of
Agriculture, American Cancer Society,
and American Heart Association, because
they are filled with fiber, potassium, magnesium, iron, folate, and vitamins C and
A—almost all of the nutrients that tend
to run low in the American population,
according to the Scientific Report of the
2015 Dietary Guidelines Advisory Committee.46 Legumes are excellent sources of
lysine (an amino acid that may fall short
in a plant-based diet), fiber, calcium, iron,
zinc, and selenium. It is ideal to consume
one to one-and-a-half cups of legumes
per day. Substantiating meals with whole
grains aids with satiety, energy, and versatility in cuisine. Nuts are nutritional nuggets, brimming with essential fats, protein,
fiber, vitamin E, and plant sterols, and have
been shown to promote cardiovascular
health47 and protect against type 2 diabetes
and obesity,48 macular degeneration,49 and
cholelithiasis.50 One oz to 2 oz (or 30 g to
60 g) of nuts per day is recommended.
Recommended servings per day
Ad libitum, with a variety of colors represented
2-4 servings (1 serving = 1 medium piece or 1/2 cup)
6-11 servings (1 serving = 1/2 cup cooked or 1 slice
whole grain bread)
2-3 servings (1 serving = 1/2 cup cooked)
At least 2-3 servings (1 serving = 1 cup raw or
1/2 cup cooked)
1-2 ounces
1-3 tablespoons
Optional, 2-3 cups
Optional, ad libitum
Seeds, too, are special in that their essential fat ratios are well-balanced, and
they contain multiple trace minerals and
phytochemicals. One or 2 tablespoons per
day will boost overall nutrition. Opting for
whole food sources of fats, as opposed to
extracted fats as found in oils, is optimal
to decrease caloric density and increase
nutrient and fiber consumption. Herbs
and spices also contain phytochemicals
and help make food delicious, varied, and
exciting, and should be used according
to preference. Food group recommended
servings per day are shown in Table 1.
PLANT-BASED MACRONUTRITION
All calories (kcals) come from some
combination of carbohydrates (4 kcals/g),
proteins (4 kcals/g), and fats (9 kcals/g).
Alcohol also provides calories (7 kcals/g)
but is not considered an essential nutrient. The ideal ratio of intake of these 3
macronutrients is highly controversial
and debatable. There is plenty of evidence
supporting health and weight management
benefits of low-fat/high-carbohydrate diets, as seen in the traditional Okinawan
diet51 and in Dean Ornish, MD’s12 and
Caldwell Esselstyn, MD’s13 reversal of advanced coronary artery disease and Neal
Barnard, MD’s6 reduction of glycemia in
type 2 diabetes using a plant-based diet
with 10% of calories from fat. Similarly,
the Mediterranean52 and many raw food53
diets consisting of upwards of 36% or
more of calories from fat show consistently
positive health advantages. Thus, it appears
that it is likely the quality of the diet that
is responsible for health outcomes rather
than the ratio of macronutrients.
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COMMENTARY
Plant-Based Diets: A Physician’s Guide
Carbohydrates
The Institute of Medicine’s adequate
intake of carbohydrates54 is 130 g/d for
everyone (except during pregnancy and
lactation) beginning at age 1 year. Optimal
sources of carbohydrates, such as wholesome vegetables, fruits, whole grains, and
legumes, are high in fiber and nutrients.
Refined carbohydrates from sugars, flours,
and other processed foods can lead to malnourishment and promote illness.
Protein
Adequate intake54 of protein is based
on weight and is estimated at 1.5 g/kg/d
for infants, 1.1 g/kg/d for 1 to 3 year olds,
0.95 g/kg/d for 4 to 13 year olds, 0.85 g/kg/d
for 14 to 18 year olds, 0.8 g/kg/d for adults,
and 1.1 g/kg/d for pregnant (using prepregnancy weight) and lactating women. Protein
is readily available throughout the plant
kingdom, but those foods that are particularly rich in protein include legumes, nuts
and nut butters, seeds and seed butters, soy
foods, and intact whole grains.
Fats
Fats—or fatty acids—are more complicated because there are several different chemical varieties based on level and
type of saturation. Each category of fatty
acid performs different functions and
acts uniquely in the body.14
The essential fatty acids are polyunsaturated and include both omega-3 and
omega-6 fatty acids. Omega-3 fats are
found in their shorter chain form as alpha linolenic acid and are used as energy.
They are also converted by the body to
the longer-chain eicosapentaenoic acid
(EPA) and then docosahexaenoic acid
(DHA). Because this conversion process can be inefficient, some people may
require a direct source of these longerchain EPA and DHA in the form of a
microalgae supplement. Alpha linolenic
acid can be found in flaxseeds, hempseeds, chia seeds, leafy green vegetables
(both terrestrial and marine), soybeans
and soy products, walnuts, and wheat
germ, as well as in their respective oils.
A direct plant source of EPA and DHA
is microalgae, through which fish acquire
them. Plant sources may be superior because they do not contain the contaminants that fish contain, including heavy
The Permanente Journal/Perm J 2016 Summer;20(3):15-082
metals, such as mercury, lead, and cadmium, as well as industrial pollutants.55
Also, plant sources are more sustainable
than fish sources.56
Monounsaturated fats are not essential
but have been found to impart either a
neutral or slightly beneficial effect on
serum cholesterol levels, depending on
which nutrient they are replacing. When
swapped for saturated fats, trans fats, or
refined carbohydrates, monounsaturated
fats may lower low-density lipoprotein
and raise high-density lipoprotein cholesterol. These fatty acids are found in
olives, avocados, macadamia nuts, hazelnuts, pecans, peanuts, and their respective oils, as well as in canola, sunflower,
and safflower oils.
Saturated fats, as mentioned above,
are not essential in the diet and can
promote CVD. They are found primarily in animal products but are available
in some plant foods, mostly in tropical
fats and oils, such as palm and coconut,
and also in other high-fat foods, including avocados, olives, nuts, and seeds. If a
vegan diet contains an average of 5% to
6% of kcals from saturated fat, which is
what the American Heart Organization
recommends for a heart-healthy diet, any
added serving of animal products will
significantly increase the total intake.
Trans fatty acids are laboratory-made
via hydrogenation and are found in processed, fried, and fast foods. Although
they were originally developed to be a
healthy alternative to butter and lard,
trans fatty acids were found to significantly increase CVD risk. In November
2013, the US Food and Drug Administration issued a notice that trans fatty
acids were no longer considered safe57
and is now trying to eliminate artificially produced trans fatty acids (there
are small amounts found naturally in
meat and dairy products) from the food
supply. Be aware that a nutritional label
can state a food product contains “0 g
trans fats” even if it contains up to 0.5 g
per serving. Thus, advise your patients
to focus on the ingredient list on food
products and to avoid anything with the
words “partially hydrogenated.”
Dietary cholesterol is a sterol that is
found primarily in animal products.
Although cholesterol is required for the
production of hormones, vitamin D,
and bile acids, the liver produces enough
cholesterol on its own. Excessive intake
of dietary cholesterol is associated with
increased risk of CVD.
Phytosterols, which are similar to cholesterol, are plant-based sterols found in
all plant foods (especially wheat germ,
nuts, seeds, whole grains, legumes, and
unrefined plant oils). Phytosterols reduce
cholesterol absorption in the gut, thereby
optimizing lipid profiles. Together with
viscous fibers, soy proteins, and almonds,
phytosterols have been found to be as effective as statins in some studies in lowering low-density lipoprotein cholesterol.5,58
It is crucial to note that all whole foods
contain all three macronutrients. It is a
pervasive misunderstanding to identify
a food as a “carb,” “protein,” or “fat.”
Instead, these are all nutrients within a
complex of other myriad constituents
that are beyond the oversimplification
perpetuated by the media and trendy
diet fads.
Ideally, a healthful diet is loaded with
wholesome carbohydrates, moderate
in fat, and temperate in protein. The
emphasis must be on the quality of the
totality of foods coming from whole
plant sources as opposed to calculations
and perfect ratios.
PLANT-BASED MICRONUTRITION
All nutrients, with the exception of vitamin B12 and possibly vitamin D, which
is ideally sourced from the skin’s exposure
to the sun’s ultraviolet rays, can be found
in plants. They are also packaged together
with thousands of powerful disease-fighting nutrients that work synergistically to
support optimal health.59
Vitamin B12
Cobalamin, commonly referred to
as vitamin B12, is the only nutrient not
directly available from plants. This is
because vitamin B12 is synthesized by microorganisms, bacteria, fungi, and algae,
but not by plants or animals. Animals
consume these microorganisms along
with their food, which is why this vitamin
can be found in their meat, organs, and
byproducts (eggs and dairy). Vitamin B12
deficiency can lead to irreversible neurologic disorders, gastrointestinal problems,
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COMMENTARY
Plant-Based Diets: A Physician’s Guide
and megaloblastic anemia. Among other
populations, vegans who do not supplement with a reliable source of vitamin B12
or breastfeeding infants of vegan mothers
who are not consuming a regular reliable source of vitamin B12 are at risk for
deficiency.
The body can store vitamin B12 for approximately three to five years, but after
that, with no repletion or with inability to
absorb, deficiency symptoms may present;
deficiency may also be asymptomatic. Because of this lag time and because serum
tests for B12 levels can be skewed by other
variables, irreversible damage may occur
before a deficiency is caught.
In a vegan diet, vitamin B12 can be
found in fortified plant milks, cereals,
or nutritional yeast. However, these are
not dependable means of achieving B12
requirements. Although there are claims
that fermented foods, spirulina, chlorella,
certain mushrooms, and sea vegetables,
among other foods, can provide B12, the
vitamin is not usually biologically active.
These inactive forms act as B12 analogues,
attaching to B 12 receptors, preventing
absorption of the functional version, and
thereby promoting deficiency. The most
reliable method of avoiding deficiency for
vegans or anyone else at risk is to take a
B12 supplement.
Because the body can absorb only approximately 1.5 µg to 2.0 µg at a time, it
is ideal to supplement with a dose greater
than the Recommended Dietary Allowance (RDA) to ensure adequate intake.
Plant-based nutrition experts recommend
a total weekly dose of 2000 µg to 2500 µg.
This can be split into daily doses or into
2 to 3 doses of 1000 µg each per week to
help enhance absorption. Because vitamin
B12 is water soluble, toxicity is rare.
Vitamin D
Vitamin D, or calciferol, is also known
as the “sunshine vitamin” because it is
the only nutrient that is acquired from
the sun. Although vitamin D is classified
as and treated like a fat-soluble vitamin,
it is actually a prohormone produced in
the skin upon exposure to ultraviolet B
sun radiation and then activated by the
liver and kidneys.
Although human bodies evolved to
produce vitamin D via the sun, there
96
appears to be a worldwide epidemic
of deficiency. Vitamin D is not widely
available from the food supply. Sources
of preformed vitamin D include fish
liver oil, oily fish, liver, and in smaller
doses, meat and egg yolk—foods that also
contain high concentrations of saturated
fat, cholesterol, and other less-than-ideal
components. Vitamin D from sunshine
and animal sources is in the form of
cholecalciferol, or vitamin D3. A second
form called ergocalciferol, or vitamin
D2, is found in plant sources, mostly
in ultraviolet B-irradiated mushrooms.
However, a plant-derived version of D3
made by lichen was recently discovered.60
Dietary supplements may contain either
D2 or D3, both of which can be effective
at optimizing blood levels.
More and more physicians are testing
for serum levels of vitamin D using the
25-hydroxyvitamin D test. The Institute
of Medicine concluded that adequate
serum 25-hydroxyvitamin D levels are ≥
50 nmol/L (≥ 20 ng/mL).61
If patients have suboptimal levels, emphasizing food sources (especially fortified
plant milks) as well as supplements may
be helpful. Dosing may be tricky because
of variable responses in individuals and
differences in types of vitamin D formulas. Of note, although both of the 2 forms
of vitamin D—cholecalciferol (D3) and
ergocalciferol (D2)—are effective at raising serum D levels in small doses (4000
IU or less), cholecalciferol (D3) is superior when using large boluses. Because
the supplement industry is not regulated
by the Food and Drug Administration,
it is “buyer beware” in the supplement
market. Thus, aim to find well-reputed
companies. A few organizations, such as
Consumer Lab, NSF International, and
US Pharmacopeia, act as independent
third parties and offer seals of approval
after testing products for potency and
contaminants. They do not, however, test
for safety or efficacy.
Calcium
Calcium, a macromineral, is the most
abundant mineral in the human body. A
mere 1% of the body’s calcium circulates
in the blood and tissues; 99% is stored in
the bones and teeth. Calcium is a nutrient
of concern for the general population with
respect to bone mineral optimization during the lifespan. However, because bone
metabolism is multifactorial and complex,
it is important to emphasize consumption
of ample sources of calcium as well as vitamins K and B12, fluoride, magnesium,
phosphorus, and potassium; to maintain
serum vitamin D levels; and to ensure consistent exercise. Throughout the lifespan,
dietary recommendations for adequate
intake of calcium fluctuate.62
Excellent plant sources of calcium include leafy green vegetables—especially
bok choy, broccoli, napa cabbage, collard
greens, dandelion greens, kale, turnip
greens, and watercress—as well as fortified plant milks, calcium-set tofu, dried
figs, sesame seeds and tahini, tempeh, almonds and almond butter, oranges, sweet
potatoes, and beans. No matter how much calcium is consumed, the amount that is actually absorbed
is more significant. Many variables affect
calcium levels via absorption or excretion,
including:
• Overall consumption determines how
much is absorbed. Only about 500 mg
can be absorbed at a time, and absorption
decreases as calcium intake increases
• Age. Calcium absorption peaks in infants and children, as they are rapidly
growing bone, and then progressively
decreases with age
• Phytates, compounds found in whole
grains, beans, seeds, nuts, and wheat
bran, can bind with calcium as well as
with other minerals and inhibit absorption. Soaking, sprouting, leavening, and
fermenting improve absorption
• Oxalates are constituents found in some
leafy green vegetables, such as spinach,
Swiss chard, collard greens, parsley,
leeks, and beet greens; berries; almonds;
cashews; peanuts; soybeans; okra; quinoa; cocoa; tea; and chocolate. They
may also somewhat inhibit absorption
of calcium and other minerals, but some
may still be absorbed. Emphasizing variety in the foods eaten on a regular basis
encourages adequate absorption
• Serum vitamin D levels must be within
optimum range in order for the body to
absorb calcium. • Excessive intake of sodium, protein,
caffeine, and phosphorus (as from dark
sodas) may enhance calcium excretion.62
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COMMENTARY
Plant-Based Diets: A Physician’s Guide
Iron
Ironically, iron is one of the most
abundant metals on Earth and yet iron
deficiency is one of the most common
and widespread nutritional deficiencies.
It is the most common deficiency in the
world and is a public health problem in
both industrialized and nonindustrialized
countries.63 It is particularly prevalent
in women of childbearing age, pregnant
women, infants, children, teenage girls,
and anyone experiencing bleeding, such
as people with ulcers, inflamed intestines
caused by malabsorptive disorders, or
heavy menstruation. Iron-deficiency anemia is no more common in vegetarians
than in nonvegetarians.
Because plant-sourced iron is nonheme
iron, which is susceptible to compounds
that inhibit and enhance its absorption,
the recommendation for vegans and vegetarians is to aim for slightly more iron
than nonvegetarians. Fortunately, this is
easy to do with the wide array of iron-rich
food choices in the plant kingdom. Leafy
greens and legumes are excellent sources
of iron and a multitude of other nutrients,
so it is advantageous to include these
foods often. Other good choices include
soy products, dark chocolate, blackstrap
molasses, sesame seeds, tahini, pumpkin
seeds, sunflower seeds, raisins, prunes,
and cashews.
Iron absorption may be diminished
in the presence of phytates, tannic acids
from tea, calcium in dairy, fiber, polyphenols in coffee and cocoa, and certain
spices (eg, turmeric, coriander, chilies,
and tamarind). To minimize this, separate
iron-rich foods from these nutrients as
much as possible. An example is to drink
coffee or tea separately from meals or to
mix up meal combinations. One of the
best tips for optimizing iron absorption
is to eat iron-rich foods in combination
with foods high in vitamin C and organic
acids. This improves solubility, thereby
facilitating absorption. Examples of such
optimizing food combinations are a green
smoothie with leafy greens (iron) and fruit
(vitamin C) or salad greens (iron) with
tomatoes (vitamin C).
Iodine
Dietary sources of the trace mineral
iodine are unreliable and fluctuate geographically because of varying soil qualities. It is crucial for vegans to be mindful
Table 2. Sources of notable nutrients
Nutrient
Protein
Omega-3 fats
Fiber
Calcium
Iodine
Iron
Zinc
Choline
Folate
Vitamin B12
Vitamin C
Vitamin D
Vitamin K
Food sources
legumes (beans, lentils, peas, peanuts), nuts, seeds, soy foods (tempeh, tofu)
seeds (chia, hemp, flax), leafy green vegetables, microalgae, soybeans and soy foods,
walnuts, wheat germ
vegetables, fruits (berries, pears, papaya, dried fruits), avocado, legumes (beans,
lentils, peas), nuts, seeds, whole grains
low-oxalate leafy greens (broccoli, bok choy, cabbage, collard, dandelion, kale,
watercress), calcium-set tofu, almonds, almond butter, fortified plant milks, sesame
seeds, tahini, figs, blackstrap molasses
sea vegetables (arame, dulse, nori, wakame), iodized salt
legumes (beans, lentils, peas, peanuts), leafy greens, soybeans and soy foods,
quinoa, potatoes, dried fruit, dark chocolate, tahini, seeds (pumpkin, sesame,
sunflower), sea vegetables (dulse, nori)
legumes (beans, lentils, peas, peanuts), soy foods, nuts, seeds, oats
legumes (beans, lentils, peas, peanuts), bananas, broccoli, oats, oranges, quinoa, soy
foods
leafy green vegetables, almonds, asparagus, avocado, beets, enriched grains (breads,
pasta, rice), oranges, quinoa, nutritional yeast
fortified foods (nutritional yeast, plant milks), supplement (2500 mg per week)
fruits (especially berries, citrus, cantaloupe, kiwifruit, mango, papaya, pineapple), leafy
green vegetables, potatoes, peas, bell peppers, chili peppers, tomatoes
sun, fortified plant milks, supplement if deficient
leafy green vegetables, sea vegetables, asparagus, avocado, broccoli, Brussels
sprouts, cauliflower, lentils, peas, nattō (a traditional Japanese food made from
soybeans fermented with Bacillus subtilis var nattō)
The Permanente Journal/Perm J 2016 Summer;20(3):15-082
of consuming a source of iodine to avoid
thyroid issues. Sources of iodine include
iodized salt and sea vegetables. However,
it is important to note that iodine is not
found in sea salts, gourmet salts, or other
salty foods. One half-teaspoon of iodized
salt provides the daily recommended
150-µg dose. Also, iodine levels in sea
vegetables fluctuate dramatically, with
some (especially dulse and nori) containing safe amounts and others (such as kelp)
harboring toxic doses. Hijiki, also spelled
hiziki, should be avoided owing to its excessive arsenic levels. A preexisting iodine
deficiency, a selenium deficiency, or high
intake of goitrogens (antinutrients found
in cruciferous vegetables, soy products,
flaxseeds, millet, peanuts, peaches, pears,
pine nuts, spinach, sweet potatoes, and
strawberries) can interfere with iodine
absorption. There is no need to avoid
goitrogenic foods as long as iodine intake
is sufficient. If a patient does not enjoy sea
vegetables or is minimizing intake of salt,
an iodine supplement may be warranted.
Selenium
Selenium is a potent antioxidant that
protects against cellular damage and also
plays a role in thyroid hormone regulation, reproduction, and dialpha nucleic
acid (DNA) synthesis. Brazil nuts are
an especially rich source of selenium in
the plant kingdom. Although selenium
content varies depending on the source,
an average ounce (approximately 6 to 8
nuts) can provide 777% of the RDA.
When accessible, one Brazil nut a day is
an ideal way of meeting selenium recommendations. Other plant sources include
whole grains, legumes, vegetables, seeds,
and other nuts.
Zinc
Zinc supports immune function and
wound healing; synthesis of protein and
DNA; and growth and development
throughout pregnancy, childhood, and
adolescence. Because of the presence of
phytates, bioavailability of zinc from
plants is lower than from animal products. Zinc deficiency may be difficult
to detect in blood tests but can show
up clinically as delayed wound healing,
growth retardation, hair loss, diminished
immunity, suppressed appetite, taste
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COMMENTARY
Plant-Based Diets: A Physician’s Guide
abnormalities, or skin or eye lesions.
Consider advising patients to aim for
50% or greater than the RDA of zinc
daily by including legumes, cashews and
other nuts, seeds, soy products, and whole
grains. Preparation methods such as soaking, sprouting, leavening, and fermenting
will improve absorption. Table 2 provides
a convenient chart highlighting excellent
sources of notable nutrients.
HELPING PATIENTS GET STARTED
To support patients to delve into
this therapeutic nutrition plan to help
them prevent or manage chronic disease
and improve or maintain their state of
health, it is crucial to provide optimistic, simple, and strategic guidance. See
Sidebar: Six-Step Guide for Initiating
and Maintaining a Nutrition Dialogue
with Patients.
GUIDE FOR INITIATING AND
MAINTAINING A NUTRITION
DIALOGUE WITH PATIENTS
1. During the first part of an office visit
when interviewing patients regarding wellness behaviors (typically covering exercise
and smoking), include questions about
diet, such as the following:
• Do you eat at least 7 to 9 servings of
vegetables and fruits every day?64
• How many times per week do you eat
fried foods/red meat/processed meat/
refined sugars?
• How often do you choose whole grains
over refined grains?
• Do you eat at least a cup to a cup-anda-half of legumes (beans, lentils, peas)
per day?
• Do you include leafy green vegetables
in your daily diet?
2. When discussing a patient’s treatment
plan, include diet as a viable option with
positive effects (eg, improved gastrointestinal function, decreased risk for chronic
diseases, and better outcomes for existing
conditions).
3. Advocate simple suggestions to start
off. Instead of overwhelming a patient with
drastic renovations to their current way of
eating, begin with a few changes that can
be made within reason. Some examples
include the following:
• Incorporate leafy green vegetables with
at least two meals or snacks each day
(enjoy a salad, add broccoli to pasta,
try a green smoothie for breakfast or a
snack).
• Start reducing intake of red and processed meat to once per week or less.
• Opt for whole grains over refined (eg,
brown rice instead of white rice, whole
grain pasta instead of white pasta, 100%
whole grain or sprouted bread).
Suggested Internet Nutrition Resources
www.nlm.nih.gov
https://ndb.nal.usda.gov
http://vegetariannutrition.net
http://nutritionfacts.org
www.pcrm.org
www.brendadavisrd.com
www.veganhealth.org
http://plantbaseddietitian.com
www.theveganrd.com
www.vrg.org/nutrition/
https://fnic.nal.usda.gov/lifecyclenutrition/vegetarian-nutrition
www.vegansociety.com
Label-Reading Protocol
• Ignore misleading marketing terminology on labels (eg, “excellent
source of,” “free of,” “natural”)
• Focus solely on ingredient list and
ignore rest of packaging
• Strive to purchase foods with:
- Only recognizable ingredients
- Few total ingredients listed
- Absence of artificial colors/
flavorings/sweeteners,
refined sugars, preservatives,
stabilizers, thickeners, or any
unrecognizable names
Six-Step Guide for Initiating and Maintaining a Nutrition Dialogue with Patients
1. During the first part
of an office visit when
interviewing patients
regarding wellness behaviors (typically covering
exercise and smoking),
include questions about
diet.
2. When discussing a patient’s treatment plan, include diet as a viable option with positive effects
(eg, improved gastrointestinal function, decreased
risk for chronic diseases,
and better outcomes for
existing conditions).
98
3. Advocate simple suggestions to
start off. Instead of overwhelming
a patient with drastic renovations
to their current way of eating,
begin with a few changes that can
be made within reason.
4. Educate patients on both the risks
associated with inadequate intake
of produce and regular consumption of refined sugars and
animal products as well as the
advantages of emphasizing whole
plant foods. Enlist all health care
practitioners on the patient’s team
to be aware of diet modification
goals. One way to simplify this is
by charting progress and goals.
5. Offer patients educational support (see Sidebar:
Suggested Educational Support). Information in
the form of pamphlets, onsite nutrition counseling, in-house cooking classes, and articles on
the Internet (see Sidebar: Suggested Internet
Nutrition Resources) is ideal because there are
multiple points of reference and communication
for patients.
6. Maintain a plan for follow-up and continued
encouragement. It is common for people to lose
motivation, and to become frustrated over time,
particularly if there is not a strong support system
in place (see Sidebar: Tips for Patient Motivation).
Engage patients by ensuring they are enrolled
in classes, have family or friends participating alongside them, are connected to others in
similar phases of transition, and have access to
continued information, as designated above.55
The Permanente Journal/Perm J 2016 Summer;20(3):15-082
COMMENTARY
Plant-Based Diets: A Physician’s Guide
• Enjoy 2 to 4 servings of fruit per day.
• Include colorful vegetables with each
meal.
• Try making a plant-based meal and then
an entire plant-based day by prioritizing
previously loved plant-based dishes (eg,
pasta primavera, bean and rice burrito,
bean chili).
• Aim to eat a rainbow every day (foods
naturally red, orange, yellow, green, and
blue/purple).
For those patients eager to make more
dramatic changes, encourage switching
to eating a combination of vegetables,
fruits, legumes, and whole grains, according to the recommendations above.
4. Educate patients on both the risks
associated with inadequate intake of
produce and regular consumption of
refined sugars and animal products as
well as the advantages of emphasizing
whole plant foods. Enlist all health
care practitioners on the patient’s team
to be aware of diet modification goals.
One way to simplify this is by charting
progress and goals.
5. Offer patients educational support
(see Sidebar: Suggested Educational
Support). Information in the form of
pamphlets, onsite nutrition counseling,
in-house cooking classes, and articles
on the Internet (see Sidebar: Suggested
Suggested Educational Support
• Informational sheets, such as pamphlets and handouts, of meal options,
recipes, nutrient sources (as in Table 2), sample meal plans, benefits of eating
healthfully, additional resources, and advice based on the information in this
guide will support the patient in pursuing plant-based eating at home.
•Individual nutrition counseling as prescribed by a physician provides encouragement, reinforces positive outcomes, and helps address needs and concerns.
•Cooking classes, available in many communities, led by plant-based chefs or
registered dietitians are excellent tools for successful adaptation of healthy
cooking patterns in the home. Demonstrations and interactive methods whereby participants are able to prepare food or at least taste samples and receive
recipes to take home will inspire adherence.
•Articles on the Internet (see Sidebar: Internet Nutrition Resources) and other
online resources (or even nutrition-specific Web sites) are opportunities to
provide patients with ready-to-go information and perhaps a 24-hour interactive resource.
Tips for Patient Motivation
• Focus on optimism. Encourage every positive choice because food is deeply
personal and making significant changes is challenging for most people. Every bite
matters.
• Encourage the conversation with patients who are interested. The single person
most people trust for advice and recommendations on health, diet, and wellness is their physician. It is an honor and special occasion to be able to open
up the dialogue from a place of caring and support and without judgment. Offer advice and an ear to help propel patients onto the path of long-term health.
•Make it fun. Recalculating diet is similar to learning a new language. Initially,
a few new ingredients are discovered, which is like learning some new words.
Then enjoyable recipes and meals become part of the repertoire, which is similar to learning some phrases in the new language. Finally, the knowledge base
expands so greatly that it becomes second nature to choose and prepare plantbased meals, akin to speaking the language fluently. Health care practitioners
are ideally situated to easily guide patients toward fluency and success in this
new language.
The Permanente Journal/Perm J 2016 Summer;20(3):15-082
Internet Nutrition Resources) is ideal
because there are multiple points of reference and communication for patients.
It is also important to educate patients on the importance of reading
labels (see Sidebar: Label-Reading
Protocol).
6. Maintain a plan for follow-up and
continued encouragement. It is common
for people to lose motivation, and to become frustrated over time, particularly if
there is not a strong support system in
place (see Sidebar: Tips for Patient Motivation). Engage patients by ensuring
they are enrolled in classes, have family
or friends participating alongside them,
are connected to others in similar phases
of transition, and have access to continued information.65
CONCLUSION
Ultimately, it is a win-win situation—
for patients, and for health care practitioners—to have plant-based eating as a
powerful tool in the toolbox. Pharmaceuticals are an important tool in a physician’s
armamentarium, particularly in treating
acute illness, but lifestyle changes, eg diet,
can be an important and powerful tool in
treating chronic illness. To facilitate lower
health care costs and likely better health
outcomes, let food be medicine and the
route of the future. v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
Acknowledgment
Mary Corrado, ELS, provided editorial assistance.
How to Cite this Article
Hever J. Plant-based diets: A physician’s guide.
Perm J 2016 Summer;20(3):15-082.
DOI: http://dx.doi.org/10.7812/TPP/15-082.
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Food Rules
Eat food.
Not too much.
Mostly plants.
— Food Rules, Michael Pollan, b 1955, American author,
journalist, activist, and professor of journalism
The Permanente Journal/Perm J 2016 Summer;20(3):15-082
101
NARRATIVE MEDICINE
The Use of Narrative as a Treatment Approach for Obesity:
A Storied Educational Program Description
Marcus Griffith, MD; Jeana Griffith, PhD; Mellanese Cobb, MPH; Vladimir Oge, MPH
Perm J 2016 Summer;20(3):15-029
E-pub: 03/17/2016 http://dx.doi.org/10.7812/TPP/15-029
ABSTRACT
Introduction: Childhood obesity is a health care crisis according to the leading
pediatric advocacy groups (National Medical Association, American Academy of
Pediatrics, and American Diabetes Association) and the White House. The problem
has reached epidemic proportions for all children, but it has an even greater impact
on racial minorities. The subject of childhood obesity can lead to a host of medical,
psychological, and social problems, including low self-esteem and discrimination.
We wrote an interventional children’s book and workbook (The Tale of Two Athletes:
The Story of Jumper and The Thumper) and developed a three-step intervention based
on the narrative. The intervention’s purpose is to increase public awareness, reduce
stigma, and to help members of underserved communities become more comfortable
discussing obesity.
Methods: In classrooms and other community settings, a storied education program is
presented to students of various ages. Interactive storytelling is the first step: live narration
with direct listening and active participation. Didactic information on obesity is shared,
including a sociocultural explanation for why the issue is more problematic among racial
minorities. The audience is then introduced to the story of Jumper and The Thumper,
two larger-than-life characters who experience different outcomes as a result of their
choices about diet and exercise. True examples are described during the narration about
these two young men, accompanied by cartoons and photographs for visual emphasis.
The next step is reading: audience members are provided with a book to reinforce
what was learned. Readers are allowed to more closely examine the importance of
making healthy choices.
Practicing positive behaviors and decision making through games and exercises
from the companion workbook is the final step. These activities help children and their
families live a healthier lifestyle. The goal is that these three steps, linked to a common
narrative, will have a meaningful impact on obesity by creating behavioral change.
Results: Children, parents, and health care professionals have stated their enthusiastic
response to the information and message and that they have made positive changes in
children’s eating and exercise habits. The program has been presented in community
forums, churches, medical meetings, and elementary schools in at-risk communities.
Conclusion: New strategies must be developed to lead, uplift, and empower through
health and wellness education and through community collaboration if we are to change
the direction of course toward this devastating condition that affects our most valuable
commodity—our children. This community-based educational approach is a means to
help recognize and treat obesity in underserved communities.
INTRODUCTION
Obesity is a health care crisis according to leading medical and patient advocacy groups (Centers for Disease Control
and Prevention,1 American Academy of
Pediatrics,2 American Diabetes Association,3
American Medical Association,4 and National Medical Association5) and the White
House.6 Obesity is defined by excess body
fat, which is not the same as overweight. A
person may be overweight because of extra
muscle, bone, water, and/or fat.7 Although
obesity rates have reached epidemic proportions, there is a lack of culturally competent
interventions to educate the public and to
prevent and combat this condition. We
developed an innovative, culturally competent approach with narrative to address
this deficiency.
The statistics on obesity in both children
and adults are alarming; however, facts, figures, and epidemiologic information do not
tell the whole story. Obesity has grown into
such an enormous public health problem
that even the untrained observer can recognize that it is out of hand. The challenges
faced in elementary school lunchrooms are
one clue to this growing problem. According to the National Health and Nutrition
Examination Survey, more than 33% of
adults and 17% of youths in the US are
obese.8 Rates of obesity among children
and adolescents have tripled since 1980,
with an estimated 12.5 million children and
adolescents aged 2 to 19 years identified as
obese or overweight.8
The problem of obesity in children and
adolescents is perhaps one of the most
pressing public health concerns in the US.
Studies suggest that individuals who experience problems with excess weight during
childhood are commonly overweight or
obese as adults. The best method for preventing this potentially lifelong problem
is to control it during childhood through
education and behavioral intervention.9
Obesity may have the greatest impact
on racial minorities. Minority populations
and low-income communities appear to
have the highest risk. The 2001 report The
Surgeon General’s Call to Action to Prevent
and Decrease Overweight and Obesity10 was
Marcus Griffith, MD, is a Diplomate of The American Board of Obesity Medicine, a Staff Physician for Kaiser Permanente, and
Clinical Assistant Professor in the Department of Psychiatry for Morehouse School of Medicine and Emory University School
of Medicine in Atlanta, GA. E-mail: [email protected]. Jeana Griffith, PhD, is an Associate Director of Psychological
and Health Services for Georgia State University in Atlanta, GA. E-mail: [email protected]. Mellanese Cobb, MPH, is a Senior
Pharmaceutical Specialist with Boehringer Ingelheim in Atlanta, GA. E-mail: [email protected]. Vladimir Oge, MPH, is
the Director of Health Promotion for Georgia Institute of Technology in Atlanta. E-mail: [email protected].
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The Use of Narrative as a Treatment Approach for Obesity: A Storied Educational Program Description
one of the first to call attention to obesity
as a major health problem. More recently,
First Lady Michelle Obama launched the
Let’s Move initiative to examine root causes
and offer practical solutions.11
Obesity is believed to be a preventable
illness that many believe will one day have
greater rates of morbidity and mortality
than any other health condition. Because
racial minorities experience higher rates
of obesity than whites, this disease state is
linked to health care disparities in the US.
According to a 2001 Institute of Medicine
report, racial and ethnic disparities exist
regardless of socioeconomic status.12 The
reported data suggest that racial and ethnic
minorities tend to receive a lower quality
of health care than whites, even when
analyses control for access-related factors,
such as insurance status and income. Key
epidemiologic indices on these differences
include higher morbidity and mortality
from the leading causes of death, poorer
quality of care, and worse outcomes.12
A COMMUNITY-BASED
EDUCATIONAL APPROACH
A critical service line in the battle against
obesity is the need for new methods of
communication between health care organizations and underserved communities.
Traditional strategies for communicating
messages about obesity and other chronic
diseases have failed to improve population
health, as evidenced by worsening rates.
New, culturally competent interventions
must be developed so as to build relationships between people from different races,
cultures, and ethnicities. The spectrum of
health-related problems linked to obesity
is well documented; it includes diabetes,
hypertension, respiratory problems, and
depression. Low self-esteem, depression,
and social discrimination associated with
childhood obesity are frequently unaddressed.10 Battling the medical complications of obesity and forming solutions for
associated emotional distress has been the
focus of my (MG’s) work.
On the eve of the grand opening of my
(MG’s) medical practice, in 1994, I got
the sad news that my best friend had died
from a massive heart attack. I had always
dreamed of becoming a physician and
running my own office. I had imagined
that this day would be filled with a sense
The Permanente Journal/Perm J 2016 Summer;20(3):15-029
Marcus Griffith, MD, telling the story of The Tale of Two Athletes at the Boys and Girls Club in Seaside, CA.
of accomplishment and excitement; but
instead, it was overshadowed with grief.
That night I experienced a profound sense
of loss, and I made a commitment to fight
obesity. When I opened my office the following day, I began to incorporate that
fight into my daily clinical practice. Over
the years, I have continued to explore new
education and prevention strategies designed for clinical and community settings.
I (MG) wrote the story of Jumper and
The Thumper several years later, while
working in a mental health treatment center for children and adolescents with severe
behavioral and emotional problems. The
vast majority of the patients were African
American, low-income, and were obese or
overweight. The children learned about
diet, nutrition, and exercise as components
for improving their mental and physical
health. As we worked with dieticians,
encouraged a reduction in television and
video game time, and promoted increased
physical activity, our activities reinforced
the guidelines on obesity recommended
by the American Academy of Pediatrics.13
During the last several years I (MG)
traveled throughout the US and received a
number of awards for my work on obesity.
The work began through telling a story
about how a dear friend lost his life because of complications from obesity. I then
used the story as a platform to develop a
community-based educational program to
address both the mental and the physical
health problems associated with obesity.
The intervention’s purpose is to increase
public awareness, to reduce stigma, and to
help constituents of underserved populations become more comfortable discussing
obesity. The program also incorporates
nutrition, exercise, and other behavioral strategies to combat weight gain.
Community-based educational programs
that teach the benefits of healthy eating,
nutrition, and exercise have proved to be
effective tools for controlling weight and
promoting positive behavioral change.14
The initiative centers around a children’s
book that my wife and I (MG) wrote, entitled The Tale of Two Athletes—The Story
of Jumper and The Thumper. The story in
the book is told through the eyes of a little
girl named Jasmine who attended one of
my presentations at a community event
in Seaside, CA. Jasmine is battling childhood obesity and heard the story The Tale
of Two Athletes. This inspirational story is
based on my lifelong friendship with Joe
Drake, a professional football player who
died prematurely because of obesity. Recently, after reading a magazine article on
the number of football players who have
died from obesity-related complications,
I discovered from an ESPN story that Joe
was the heaviest player in the history of the
National Football League to die.15
Following the presentation, Jasmine
sought me (MG) out and asked if I could
help her. She told me that she had also
struggled with her weight all through her
life and could relate to many of the points
in the story. As we talked, Jasmine was curious about the two characters, Jumper and
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The Use of Narrative as a Treatment Approach for Obesity: A Storied Educational Program Description
The Thumper, and wanted to know more
about their lives. She stated that she would
never forget the story and did not want to
end up like The Thumper. Jasmine made a
promise that she would begin trying to live
a healthier lifestyle. In addition to children,
adults struggling with obesity are receptive
to the program’s message. The interactive
narrative, based on a true story, attempts
to inspire change and create solutions. It is
an alternative approach for examining the
causes of obesity and forming solutions,
especially in the context of racial minorities
and underserved communities.
One of the activities that generated
the most excitement resulted from the
relationship that we formed with the park
rangers at Davidson-Arabia Nature Preserve in DeKalb County, GA. Two park
rangers and I (MG) led three groups of
patients on a series of nature hikes through
the forest in an effort to increase exercise
and to create exposure to a new experience. We instructed the patients on the
importance of exercise and appreciation
of nature. Staff members from the day
treatment program also participated to
help ensure safety. To my surprise, many of
the children had never been outside of the
city or spent time in the woods. The healing power of nature was quite evident as
their negative behaviors decreased during
our outings. I made sure that the children
with the most severe behavioral issues were
placed in my group, with the appropriate
accompanying staff. No major issues were
encountered.
One rainy day when we were unable to
go outside for our nature hike, a young
man shared with me the pain he experienced because of excess weight. I (MG)
asked him to write down his feelings,
and he entitled his story “My Life as an
Obese Child.” His name just happened
to be Joseph—the same name as my late
friend. I was inspired to create a story and
use it as a component of a comprehensive
obesity program at the center (up until
the book was written the story was told
from memory in the old tradition of story
telling). I told the story about Jumper and
The Thumper so as to convey a powerful
message about obesity, from and about
someone the children knew.
The story about my (MG’s) relationship
with Joe Drake continues to be integral to
my personal and professional life. On February 28, 2012, I closed my private practice after 18 years of service and accepted
a position with Kaiser Permanente in GA.
Coincidently, as I was closing my office for
the final time and was saying goodbye to
my patients, the first copy of the published
book arrived. Closing my office and simultaneously receiving the first printed copy
of The Tale of Two Athletes was a powerfully
Marcus Griffith, MD, introducing Jumper and The Thumper to students at Hamilton Holmes Elementary
School in Atlanta, GA.
104
emotional experience, especially considering what had happened the night before
opening my office in 1994. The moment
of closure marked for me a beginning and
an end at the same time. Although it was
an end to my private practice, a new opportunity began in my quest to honor my
friend in the fight against obesity through
the telling of The Tale of Two Athletes.
NARRATIVES—
A THREE-STEP APPROACH
I (MG) developed a three-step approach
based on The Tale of Two Athletes to educate
the community about obesity. Storytelling is the primary concept that moves
from active listening to live narration as
the first step. Live narration aims to make
an impact on the audience through direct
listening and active participation. Didactic
information on obesity is shared, including statistics, easy-to-understand epidemiologic information, and a sociocultural
explanation for why the issue is more problematic among racial minorities. Jumper
and The Thumper are then introduced
to the audience as two larger-than-life
characters who experience different outcomes resulting from their choices in diet
and exercise. The true examples about the
young men are described during the narration, accompanied by cartoons and photographs to enhance the visual experience
and highlight the realities of the problem.
At the end of the story, when The Thumper
dies, the true names of the characters and a
photograph of the characters are revealed.
The audience then realizes that the narrator
is Jumper, which hopefully inspires them
and impresses on them the importance of
diet, nutrition, and exercise in the battle
against obesity.
The next step of the educational process
is reading the book to reinforce what was
learned in the live community educational
program. The book provides more intimate
details about the two young men and allows
the reader to more closely examine and
identify with the characters and to realize
the importance of making healthy choices.
The final step of the program uses the
companion workbook that my wife and
coauthor, Jeana Griffith, PhD, wrote
to personalize the story for each reader.
Participants practice positive behaviors
and decision making through games and
The Permanente Journal/Perm J 2016 Summer;20(3):15-029
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The Use of Narrative as a Treatment Approach for Obesity: A Storied Educational Program Description
Book signing with Marcus Griffith, MD, Jeana Griffith, PhD, and two children following a community outreach
program at the Stonecrest Library in Lithonia, GA.
exercises that help them set goals for
physical activity and a healthier diet. The
hope is that these three steps, linked to a
common narrative, will make a meaningful impact for creating behavioral change
related to obesity.
The use of narratives and storytelling
is now recognized as a culturally competent approach for reaching racial minorities and underserved populations. This
method may be a more effective process
for sharing health information in communities where traditional health education has failed. Storytelling may also be a
means of easing the disconnect between
health care professionals and underserved
communities.16
The intention is to offer a culturally
competent message that allows the audience to see, hear, understand, and feel
what obesity is all about and that they
are not alone in their struggles. The story
about the two characters, Jumper and The
Thumper, offers an opportunity for the
participants to build a relationship with
the characters and the storyteller. An expectation is that the listeners will become
immersed in the story and identify with
the message. This process, which Banks16
describes, emphasizes the importance of
building trust between the presenter and
the audience, using the experiences within
the story to create “a sense of oneness.”16
Furthermore, the companion workbook
to The Tale of Two Athletes is an example
The Permanente Journal/Perm J 2016 Summer;20(3):15-029
of how stories can incorporate games to
engage audiences and reinforce learning.
The University of Chicago and the
University of Ibadan, in Nigeria, formed
a partnership for reducing gaps in how
adolescents receive knowledge on sexual
health in disadvantaged communities.
The researchers developed this initiative
as they observed similarities between disadvantaged communities in developing
African nations and the US.17 Gilliam
et al17 combined traditional storytelling
with technologies of social media and
game design to reshape adolescent sexual
health behaviors. They believe that stories
and games can be used to communicate
information about other preventable illnesses where traditional health messaging
has been unsuccessful.
The use of narratives and
storytelling is now recognized as
a culturally competent approach
for reaching racial minorities and
underserved populations.
The researchers on the initiative developed a script with integrated images,
music, videos and personal messaging to
appeal to a select audience. Story content
was developed through a series of workshops with South Side Chicago youth
and touched on themes significant to that
environment, including neighborhood
violence, loss, abortion, sexual violence,
and bullying. Personal experiences were
incorporated into a narrative-driven
game. The game was used in an interactive
method to educate and to test knowledge
on sexual health and other topics, such
as rape, gender inequality, incarceration,
and parent communication. Following
the intervention the authors found that
the participants were more knowledgeable
and had improved critical thinking with
regard to the subject matter.17
Similarly, the children’s workbook created from The Tale of Two Athletes uses
games, images, and concepts from the
story to improve knowledge and critical thinking about obesity and healthy
lifestyle choices. Using the workbook is
the third and final step, following active
listening to the story and reading the
book. Once families are inspired by the
story to make changes in their lifestyle,
the workbook shows them, step by step,
how to make these changes. Games and
fun activities in the workbook further
educate participants about obesity and
healthier food intake. The workbook also
has charts and provides resources to help
families set individual goals.
DISCUSSION
Storytelling has been used since the
beginning of human communication as a
means to preserve history, culture, ideas,
and teaching. Ideally it is an interactive
process between the storyteller and the audience that helps listeners to conceptualize
and makes the message more meaningful. I
(MG) have been using a narrative approach
in my obesity education programs as a
means of conveying health information
to diverse populations (African-American
and Hispanic populations). I have attempted to construct a program that engages the
audience and inspires behavioral change
through humor, didactic material, and a
true, compelling story.
Health interventions typically focus on
changing individual behavior through traditional health policy and communications.
These approaches have done little to reduce
the differences in prevalence, mortality, and
burden of chronic diseases in underserved
communities. Examples include heart
disease, diabetes, preterm births, human
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The Use of Narrative as a Treatment Approach for Obesity: A Storied Educational Program Description
immunodeficiency virus, and obesity, which
continue to disproportionately affect African Americans, Hispanic, Native Americans, and low-income communities.16
CONCLUSION
Next steps are to expand programs
by obtaining grants and sponsorships to
promote it. We hope the three-step approach of active listening to the narrative,
reading the book, and practicing what was
learned by using the workbook will serve
as an additional model in the fight against
obesity. Up to this point, the program has
been funded by the article’s authors. The
resources to get it done were inspired by
the love of a friend and all those who have
lost someone because of obesity. v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
Acknowledgment
Leslie Parker, ELS, provided editorial assistance.
How to Cite this Article
Griffith M, Griffith J, Cobb M, Oge V. The use of
narrative as a treatment approach for obesity: A
storied educational program description. Perm J
2016 Summer;20(3):15-029. DOI: http://dx.doi.org/
10.7812/TPP/15-029.
References
1. Adult obesity. Atlanta, GA: CDC Vitalsigns; 2010
August 3.
2. Committee on Nutrition. Policy Statement: Prevention
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August;112(2):424-30. Reaffirmed 2010.
3. Marks JB. Obesity in America: It’s getting worse.
Clinical Diabetes 2004 Jan;22(1):1-2. DOI:
http://dx.doi.org/10.2337/diaclin.22.1.1.
4. D-440.980 Recognizing and taking action in
response to the obesity crisis [Internet]. Chicago,
IL: American Medical Association; 1995-2016 [cited
2016 Jan 5]. Available from: www.ama-assn.org/ssl3/
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members [Internet]. Silver Spring, MD: National
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6. Solving the problem of childhood obesity within a
generation: White House Task Force on childhood
obesity report to the President [Internet]. Washington,
DC: White House Task Force on Childhood Obesity;
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letsmove.gov/sites/letsmove.gov/files/TaskForce_on_
Childhood_Obesity_May2010_FullReport.pdf.
7. Obesity: MedlinePlus [Internet]. Bethesda, MD:
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8. Ogden CL, Carroll MD, Kit BK, Flegal KM.
Prevalence of childhood and adult obesity in
the United States, 2011-2012. JAMA 2014 Feb
26;311(8):806-14. DOI: http://dx.doi.org/10.1001/
jama.2014.732.
9. Stephenson PL, Taylor MV. Obesity in children and
adolescents: a webliography. J Consum Health
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Prevention and Health Promotion; Centers for
Disease Control and Prevention; National Institutes
of Health. The Surgeon General’s call to action
to prevent and decrease overweight and obesity
[Internet]. Rockville, MD: Office of the Surgeon
General; 2001 [cited 2015 Aug 24]. Available from:
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letsmove.gov/learn-facts/epidemic-childhood-obesity.
Betancourt JR, Maina AW. The Institute of Medicine
report “Unequal Treatment”: implications for
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Oct;71(5):314-21.
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School Health. Active healthy living: prevention of
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dx.doi.org/10.1542/peds.2006-0472.
Whetstone LM, Kolasa KM, Collier DN. Participation
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behaviors in youth. Am J Health Promot 2012 SepOct;27(1):10-6. DOI: http://dx.doi.org/10.4278/
ajhp.100415-QUAN-117.
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before 50 [Internet]. Bristol, CT: ESPN; 2006 Jan
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espn.go.com/nfl/news/story?id=2313476.
Banks J. Storytelling to access social context and
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Powerful Drugs
In medicine, as in stagecraft and propaganda,
words are sometimes the most powerful drugs we can use.
— Anonymous; Sara Murrah Jordan’s obituary in The New York Times
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credits available for this article — see page 112.
NARRATIVE MEDICINE
You Are Not Alone:
Ten Strategies for Surviving a Malpractice Lawsuit
Audrey Sheridan, MD
Perm J 2016 Summer;20(3):16-004
E-pub: 06/20/2016 I wasn’t even scheduled to work that
morning; I had just gone into the office
for a meeting. Chatting with coworkers
on my way out the door, I was told there
was someone asking for me at the reception
desk. So it was there, in front of a waiting
room full of patients, that I received the
papers notifying me of the lawsuit. “Have
a nice day,” the woman called out to me
as she left.
Over the next months, as the legalities
played out, I struggled to keep moving. My
confidence evaporated. I’d been taught that
physicians who build good relationships
are less likely to be sued, so I had obviously
failed. I didn’t know how I could face my
patients—I felt like a fraud. I couldn’t
sleep. I lost my appetite. Sometimes my
experience felt surreal, especially when my
attorney told me: “This case will not affect
your life in any way.”
I wondered if I would lose my job,
my license, my home. Even worse, I
wondered if I had lost the trust of my
colleagues.
I met a coworker who had survived a
lawsuit; she had been as stressed as I was,
and knowing that my reaction was not
abnormal reassured me. I began to practice strategies to help myself cope, and life
slowly improved.
As much as we hate to think about it,
most physicians, about 60%, will be sued
at some point in their career.1 Not everyone
will be as unnerved as I was, but physicians typically do feel intense strain when
faced with a lawsuit. Our trust in ourselves
and in our patients is shaken. We practice
more defensively. We are more likely to
suffer depression and burnout. We may
feel anxious, depressed, angry, and afraid.
Here I offer ten techniques for coping that
really work.
http://dx.doi.org/10.7812/TPP/16-004
RESIST ISOLATION
Asking for help can be tough for physicians; we’re used to being the ones people
come to for help, not the ones who need
help. You will be advised not to talk with
anyone about the case, but you’ve got to
know that you’re not alone. Conversations
with certain people are protected from
discovery. Ask your attorney for advice
here, but typically it is acceptable to talk
to family members, counselors, and your
personal physician. And you can generally
feel safe discussing your emotions while
avoiding the medical details of the case.
Some liability insurance providers cover
psychological counseling costs, so make
sure to ask about this option. If you think
you might benefit from talking to someone
who has had a similar experience, check to
see if your organization or insurance provider offers a peer support team.
It’s common for physicians undergoing litigation to contemplate suicide.2 If
you’re having thoughts of suicide, pick up
the phone and call someone immediately:
911, your physician, a counselor, your
spiritual advisor, or a friend or family
member. Don’t do anything until you’ve
spoken with someone. Keep a list in your
phone of people you can call for support.
If you are so depressed or anxious that
you can’t stop the negative thoughts, if
you’re not eating or not sleeping, or if
you feel overwhelmed, medication may
be helpful. Do not prescribe for yourself;
talk to a physician you can trust. It could
save your life.
USE YOUR STRENGTHS
We all developed skills for managing
stress as we made our way through college,
medical school, and residency. Remind
yourself that you have these tools, and turn
to them now. Focus, persistence, preparation, not taking things personally—we
know how to do these things.
RETRAIN YOUR BRAIN
We all have habitual thought patterns,
places our minds go when under stress. But
you can create new patterns for yourself.
Use your rational mind to respond to the
sometimes overwhelming fears that come
up; this is a technique that clinicians tend
to practice a lot. When the ugly thoughts
begin to spiral, and you start thinking
that you’re obviously a fraud, and no one
should trust you to care for them, stop
and remind yourself of the patients you’ve
helped, the procedures that went well, and
the successes you’ve had. These new neural
pathways will become more ingrained as
you continue to practice them.
Research by Martin Seligman, MD,
shows that a simple gratitude exercise increases happiness and resilience (read his
book Flourish3 or go to http://ggia.berkeley.edu/practice/three-good-things). Take
a few moments each evening to consider
what went well and write it down. At first
all you may be able to come up with is that
you have clean sheets, or that you had a
really great piece of chocolate for dessert.
But as you begin to look for the good, you
see it more, even when life seems bleak.
I look forward to this “what went well”
exercise at the end of my day.
TAKE CARE OF YOURSELF
It’s important to make room in your
hectic schedule for some downtime.
Staying busy can make you feel more in
control. It can distract you and keep you
from fixating on the case. But you need all
your strength right now, so you’ve got to
preserve that. Sleep is crucial, to give your
Audrey Sheridan, MD, is an Obstetrician/Gynecologist for the Colorado Permanente
Medical Group in Westminster. E-mail: [email protected]
The Permanente Journal/Perm J 2016 Summer;20(3):16-004
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You Are Not Alone: Ten Strategies for Surviving a Malpractice Lawsuit
brain time to recover from the stress of
each day. Exercise helps release stress.
Eating well fuels your body and brain
(but give yourself enough slack to turn
to comfort food when you most need
it—I might not have survived without
mint Newman-O’s). Take some relaxation time, whether it’s for a massage,
bedtime reading to your kids, a hot
bath, yoga, or meditation (research has
shown the effectiveness of Jon KabatZinn, MD’s mindfulness-based stressreduction program, for example). Just be
careful about using alcohol or drugs to
check out—they can quickly cause more
problems than they solve when used to
self-medicate.
GIVE YOURSELF A BREAK
Physicians tend to be perfectionists, and
being sued seems only to reinforce the expectation to be perfect. Much of the time
we are our own worst critics, and we say
things to ourselves that we’d never say to
a colleague. Show yourself the same compassion you’d show your child, patient, or
best friend. Read Kristin Neff, MD’s work
for more information on self-compassion
(http://self-compassion.org/).
SET PRIORITIES
It’s important to do things that make
you feel like you’re living in line with your
values: be a great parent to your kids, volunteer to do work you care about, spend
time with your religious community. Find
some activities that engage you enough to
distract you from your worries and that
feed your soul.
APPROACH LAW AS A FOREIGN CULTURE
As physicians we’re used to having time
pressures. Review the stat labs now! Call
the patient before you go home! Get to
the OR immediately! Things move much
differently in the legal world. Scheduling
a meeting may take days, weeks, or even
months. Phone calls may not be returned
the same day. It can be frustrating to just
wait when you’re used to taking care of
things quickly.
Your attorney is there to help you navigate. But just as a patient may be surprised
108
to find out that they need an IV to have
surgery whereas you take it for granted,
you may find the legal process confusing
and your attorney unaware of your uneasiness. So ask questions, and ask for preparation. If you’ve never given a deposition
before, ask to have the process explained
in detail. Again, use your strengths and
prepare as you would prepare for oral board
exams. You can even do a practice run,
answering questions in front of a video
camera. If you think that might help you,
ask your attorney to arrange it.
There will be times of relative quiet, and
then a period that is acutely stressful, like
the deposition. I realized that I needed to
approach those episodes the way I would a
crash C-section—push aside the emotions
and just do it.
The case will require your time and energy, but be reassured that generally your
liability insurance will cover the financial
aspects.
REGAIN PERSPECTIVE
Almost every day in my work, and every
time I do my volunteer shift with people
living on the streets, I am reminded of the
relative ease of my life. My problems still
feel big to me, but not insurmountable.
USE DISTRACTION
If your thoughts are stuck in a negative spiral, use distraction to pull yourself
out of the descent: movies, audiobooks,
printed books, intense exercise, time with
your kids, a hobby that engages you, a call
to a friend; find something that works for
you. I learned to queue up an audiobook
for my drive to work, so that I didn’t start
my day in worry, and to listen to a guided
meditation if I woke up feeling anxious
during the night.
FOCUS ON WHAT YOU CAN CONTROL
In the legal process, as in life generally,
there are some things you can control
but many more things you cannot. As
physicians we tend to believe that we’re in
charge, so it can be hard for us to accept
that there are things we can’t control. But
acceptance can bring relief. After one very
long and frustrating day, my attorney said
to me, “We gotta focus on what we can
control.” And he’s right: stressing and obsessing about what someone else may do
doesn’t help. We’ve all heard the Serenity
Prayer: “God, grant me the serenity to
accept the things I cannot change, the
courage to change the things I can, and
the wisdom to know the difference.” Make
this your mantra.
I encourage you to experiment to see
what works for you. None of these strategies will make the lawsuit, or the stress,
disappear. For me, they took the edge off
and made the situation bearable when I
wasn’t sure that bearing it was possible.
My case is over now, and I wish I could
tell you that there was a nice, neat ending—but there wasn’t; it was messy and
lasted much longer than I had hoped.
The unexpected good news is that I feel
more engaged now with my work than
ever. I’m more clear about the help and
healing that I have to offer my patients.
I have confidence that I can survive what
I thought was the worst thing that could
happen to me in my career. Stress, both
personal and professional, is inevitable.
These techniques help me cope. v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
Acknowledgment
Leslie Parker, ELS, provided editorial assistance.
How to Cite this Article
Sheridan A. You are not alone: Ten strategies
for surviving a malpractice lawsuit. Perm J 2016
Summer;20(3):16-004. DOI: http://dx.doi.org/
10.7812/TPP/16-004.
References
1. Jena AB, Seabury S, Lakdawalla D, Chandra A.
Malpractice risk according to physician specialty.
N Engl J Med 2011 Aug 18;365(7):629-36. DOI:
http://dx.doi.org/10.1056/NEJMsa1012370.
2. Balch CM, Oreskovich MR, Dyrebye LN, et al.
Personal consequences of malpractice lawsuits
on American surgeons. J Am Coll Surg 2011 Nov;
213(5):657-67. DOI: http://dx.doi.org/10.1016/j.
jamcollsurg.2011.08.005.
3. Seligman MEP. Flourish: a visionary new
understanding of happiness and well-being.
New York, NY: Simon & Schuster; 2011.
The Permanente Journal/Perm J 2016 Summer;20(3):16-004
NARRATIVE MEDICINE
The Handshake Layer Cake: Meeting and Regreeting
Difficulties for a Non-French Surgeon in France
Colin G Murphy, MCh, FRCSI
Perm J 2016 Summer;20(3):15-232
E-pub: 06/27/2016 “I’m not shaking hands with you,” my
friend and colleague says loudly. With a
dramatic flourish, he withdraws his hand
and hides it behind his back, pointing his
chin and lower lip towards me in a classic
Gallic pout. No one else present bats an
eyelid. The chomping of lunch and chewing the fat continues around the table,
and I am left offering my hand to empty
space. This response is slightly better than
the “Aaaagh, salaud” (“Agh, bastard”) I
received a few days earlier when committing the same social faux pas. Twice in one
week—not good.
These are two of the more aggressive responses to this particular social bêtise and
pointed reminders of the highly codified
systems of salutations here in France. Just
when this Irishman abroad thinks he has
the natives cracked, he realizes the magnitude of his ignorance for a new social
situation. Happily these rebukes are usually followed, and were immediately in the
two above cases, by a grin, a pppffffhhhh,
or a backslap.
There are kinder rebukes: “HEEEEY,
on croise les doigts cette fois-ci?” (“Hey, how
’bout we shake fingers this time instead?”),
or a big, exaggerated outstretched hand
followed by withdrawing the hand to do
the thumb-to-nose and wiggling fingers
maneuver—like we did when we were
kids—and a “OOOH, on se connaît déjà
nous!” (“Hey, we already know each other!”).
It is strange to see grown Frenchmen doing
this at you at work and stranger still that
you get used to it.
Typically the regreet conundrum develops like this: say you see a colleague
walking down the corridor, maybe with
a patient. You shake hands in passing and
give a Bonjour/Ça va?/Ça va, the absolutescraping-the-barrel-bare-minimum of conversational interactions. Then at lunch you
walk into the Café En Face (my colleagues
http://dx.doi.org/10.7812/TPP/15-232
rarely seem to eat in the hospital cafeteria—unsurprising given the quality of the
plat du jour at the local café), say with a
different colleague, where seven doctors
are sitting down eating away and chatting
animatedly. You don’t interrupt, but you
both start at the head of the table and
work your way around shaking hands or
giving les bises (the cheek-kissing of a female colleague). Sixth of seven at the table
is the colleague you greeted earlier that
morning in passing in the corridor. He is
deep in chat, holding court. What do you
do? Your colleague ahead of you has just
shaken his hand (first greeting of the day
for those two), and not wanting to make
a fuss or interrupt the flow of invective
of your seated colleagues, you might be
tempted to offer your hand to him, again.
Big mistake. Prepare to be taken to task.
You have just created a scene as now he
stops talking, leans back in his chair affecting deep insult, and pointedly refuses
to shake hands.
The best strategy for the regreet scenario is very much person and situation
dependent. I am becoming a big fan of
the index-finger shake, which can be done
with the same familiar and safe nonverbal
cues as a full handshake: approaching his
or her personal space, making eye contact,
and lifting your hand, but only the index
finger is offered for a playful sword-cross
style greeting. It is perfectly acceptable for
this all to be done without speaking.
For regreeting a senior colleague you
don’t know well enough yet to tutoyer (to address someone in French using the familiar
form of the pronoun “you”—“tu”—rather
than the more formal form of “vous”), I
copy my own boss who does an elegant
head nod and an “On s’est déjà vu” (“We’ve
already met”). This avoids committing to
a second-person singular familiar/secondperson singular respectful pronoun and
obviates the need to offer either hand or
index finger.
Maybe the index-finger shake is the
informal fist-pump to the more formal
handshake? I’m going to have to watch my
French gangster movies again to be sure,
but it seems one doesn’t regreet a senior
ranking surgeon with the index shake, or
thumb-to-nose-with-fingerwiggle. Layers
on layers. And so different from home.
Coming from a culture where work greetings are mostly nonverbal, this represents
a quantum change. Eye contact and a
nod are considered eminently sufficient
for both greeting and regreeting. Verbal
greetings are also acceptable; for colleagues
a clipped, “Morning” or “Doctor”; for the
consultant surgeon a “Mr/Ms O’Brien,”
usually with eye contact and a nod (if
feeling particularly effusive one could add
in a temporal “Good morning/afternoon
Mr/Ms O’Brien”). Tactile greetings in
Irish hospitals are almost unheard of. On
one six-month rotation, the only physical
contact I had with any of my bosses was a
backslap from the senior ranking surgeon
on the morning he came in late for the
morbidity and mortality conference after
I stood to vacate the chair nearest the exit
door for him.
But it’s not just the handshakes. Les
bises is another minefield and much more
complex than handshakes. I frequently
cringe at the different ways I achieve social awkwardness at work by getting even
the primary greeting wrong, let alone the
regreeting. We have all done it: offer the
cheek when she puts out the hand or vice
versa. At work, after a few months here
and meeting the same folks daily, playing
l’etranger card just isn’t an option anymore.
Reluctance to experiment with social greetings with female work colleagues means,
happily, that I can’t shed any light on the
regreet avec bises conundrum, but here is
Colin G Murphy, MCh, FRCSI, is a Consultant Orthopedic Surgeon
with Galway University Hospitals in Ireland. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-232
109
NARRATIVE MEDICINE
The Handshake Layer Cake: Meeting and Regreeting Difficulties for a Non-French Surgeon in France
a quick summary of what I have observed
to be the Initial Daily Greet the Ladies
at Work Rules: no handshake or bises for
the secretaries, just verbal Bonjour/Ça va?/
Ça va; a handshake for the female docs
one doesn’t know well; bises for the ones
one does know well; bises for any woman
sitting in the Café En Face regardless of
whether one knows her or not (it’s a social
context); bises for one’s scrub nurses (who
are friends at this stage), but only if they
aren’t scrubbed, and there isn’t an awake
patient in the room, in which case neither
bises nor handshake just verbal greeting;
no bises for the nurses on the ward or the
physiotherapists—except the pretty physio
who is a friend of the boss and who has
a slightly disinhibited demeanor and a
desire to chat about Irlande every time we
meet—she gets the bises greetings.
A particular ward round crystallized this
morass of mores for me. When I arrived
for the very first ward round on New Year’s
Day, I found all the nurses in the ward office were wearing little Santa hats, cheerfully calling, “Bonjour, Docteur.” I held
my distance, in truth a little intimidated
by an office full of French nurses all making eye contact, all chirping in sync and
looking expectantly at me. I remained in
the doorway, offered neither hand nor
cheek, but offered a group reply (in formalplatitude-banter mode) “Bonjour, vous allez
bien? Pas trop débordées?” (“All good? Not
too busy?”). There followed The Pause, the
one with which I am now quite familiar,
the one that corresponds with an ever-soperceptible thaw in the room that tells you
you’ve missed a social cue. The boss walked
in behind me, and I realized the magnitude
of the faux pas and how a seasonal trick
had been missed. Admirable in his ability
On mature reflection, when it
comes to the regreet dilemma,
it is probably better to receive the
playful rebuke for attempting to
steal a second handshake than
the sharp word for none at all,
but it is infinitely better, as with
most operative procedures,
to get it right the first time.
to round speedily and efficiently, he previously only ever paused to give bises to those
nurses he knew very well and liked (and
not infrequently the new, leggy or pretty
nurse he hadn’t met before), but on this
day he stopped to faires les bises with every
single female nurse, nurses’ assistant, and
catering staff on each ward (and it seemed
a few nurses who came back for seconds).
Romain, the solitary male nurse, got the
handshake. While giving un bisou, the boss
wished each of the nurses the New Year trio
of greetings—Bonne année, bonne santé,
et meilleurs voeux—and moved on. He
finished covered in lipstick and perfume,
looking very pleased with himself. I haven’t
been on a round that took so long since I
was a student doing general medicine in a
peripheral country hospital.
As always, the first work-greeting of
the day, be it a handshake or les bises, is
complicated by context: age, seniority,
work status, employer/employee status,
family, familiarity, the other people present at that interaction, whether it is break/
coffee time—these are all variables in play.
In the operating theater it gets further
complicated by physical barriers: being
scrubbed, wearing a facemask, and gloverelated issues. Such is the disdain for the
gloved handshake that people will offer
their bare forearm to shake instead of a
gloved hand. Offering a gloved hand, even
to someone wearing gloves, ce n’est pas cool,
and it’s not just because they might be
dirty or contaminated. As Serge, one of
the theater porters, pointed out to me in
no uncertain terms in my first week with
a slow head shake and a tut-tut, “Doc, c’est
pas cool du tout ça.”
All of this has to be balanced against
the unthinkable, not greeting someone
at all, or thinking (like an idiot) that the
wave or nod from a distance that you gave
earlier in the day constituted a greeting.
Failure to execute the primary, most basic
salutation of the day is le nec plus ultra of
social ignorance, regardless of distractions
or confounding factors. It is perceived as
a calculated snub, one that folks have no
problem letting you know about by marching up to you (regardless of who you are
with or what task you are engaged in) and
enquiring, “What’s the matter with you?”,
“Have I annoyed you?”, “I didn’t realize
we aren’t friends anymore, you and me?”,
or the classic “Ey-oh, tu fais la tête?” (“Are
you sulking?”).
Always the fine line in this wonderful
country. On mature reflection, when it
comes to the regreet dilemma, it is probably better to receive the playful rebuke
for attempting to steal a second handshake
than the sharp word for none at all, but it
is infinitely better, as with most operative
procedures, to get it right the first time. v
How to Cite this Article
Murphy CG. The handshake layer cake: meeting
and regreeting difficulties for a non-French surgeon
in France. Perm J 2016 Summer;20(3):15-232.
DOI: http://dx.doi.org/10.7812/TPP/15-232.
Who You Are
What you see and hear depends a good deal on where you are standing;
it also depends on what sort of person you are.
— CS Lewis, 1898-1963, British novelist, poet, academic, medievalist, literary
critic, lay theologian, broadcaster, lecturer, and Christian apologist
110
The Permanente Journal/Perm J 2016 Summer;20(3):15-232
NARRATIVE MEDICINE
Disconnection
Ahmed Obeidat, MD, PhD
Perm J 2016 Summer;20(3):15-165
E-pub: 06/17/2016 It was a very familiar object that I asked her to identify. She started
to look, feel, think, and she said, “It has buttons, numbers, and glass,
but I cannot put them together, I am unsure!” I then pushed a button and asked again. With an assertive voice, she said, “It’s a radio.”
I asked, “What else could it be?” With a tentative voice, she said, “A
video player?” I whispered, “You are so close, it’s a television.”
Then, I asked her to identify numbers. She said “four” instead of
“three” and “one” instead of “five.” Despite her confidence, her answers appeared random. I asked her to read the letters of my name
as spelled on my hospital ID. She spelled “TLOPZ” for “AHMED”;
no pattern that I could identify. I then pointed to my black jacket
and asked her to identify what it was, including what color. She said,
after a thoughtful pause, “I have seen it before, but I am unsure.”
She started to cry but then felt my jacket with her hand and readily
said, “Oh, it’s your jacket, and it is blue.” The last task I asked her
to perform was to write a sentence. I was thrilled that she wrote in
beautiful script, “Doctor, I want to know what is wrong with me.”
Yes, this was alexia (word blindness), without agraphia, associated with color anomia and visual/color agnosia (the inability to
interpret visual information and color). All implied a disconnection tragedy in her young brain. She was a creative writer in her
third decade of life who had battled lupus and antiphospholipid
syndrome for 12 years. Now her disease ravaged her left visual
cortex and further interrupted the connection between her intact
right occipital lobe and the dominant hemisphere, leaving her
blind to her own words. Apart from alexia, anomia, and visual
agnosia, she had no other language problems; she was able to
express her ideas in speech and in writing, and could fully comprehend spoken English. I quantified her deficits using the National Institutes of Health stroke scale assessment.1 Though the
examination earned her only 2 points, 1 for the field cut, and 1
for the naming difficulty, her disability was beyond what this scale
could convey. Nevertheless, her coming to our attention after a
day of symptoms precluded the use of a clot buster medication.
She was praying that her difficulties represented migraine with
visual disturbances. But symptoms lasted longer than they should
and her ophthalmologist asked her to go to the Emergency Department to be evaluated. I wondered whether an early arrival
might have made me consider treating with tissue plasminogen
activator despite her low stroke scale assessment score.
I feel safe carrying the stroke scale card in my pocket daily; it
reflects an inventory of brain functions that makes such a complicated machine comprehensible and under control. The naming
page reminds us to look for subtleties. Being able to name glove,
key, chair, cactus, feather, and hammock can be very reassuring,
whereas losing that ability is worrisome. Moreover, being able to
tell the story of the inattentive mother and her sneaky kids reaching
for the cookie jar helps us ferret out the elusive signs of language
and speech disorders. But, it is challenging to diagnose alexia
http://dx.doi.org/10.7812/TPP/15-165
without agraphia; it may pass unnoticed. Sometimes, even if observed, it can still be overlooked and blamed on its frequent fellow
traveler, “homonymous hemianopia.” Alexia without agraphia is
very disabling, very frustrating, and much more important than
its corresponding low stroke scale assessment score. The sum total
of our decision to treat or not weighs what we can’t always capture
by a number. The decision to treat or not emphasizes the concept
of art in our daily practice of medicine.
Several months after the event, she lives with her loving parents;
she is gradually coping with her loss. I talked to her again but this
time away from the Emergency Department.
She said, “I lost some capabilities. For example, I am not driving
anymore: it is hard to read the signs or even follow the navigation
system directions. Occasionally, I ask for help when I want to dress
for an important event. Otherwise, a perfectly matching outfit
means little to me. I believe in the beauty of each color and the
beauty of each soul.” I then asked about her writing. She looked
at me and smiled. She said, “I still enjoy writing and I love it even
more now! I write on my small notebook and then listen to my
mother’s voice carrying my own words; she reads them out loud,
once, twice, three times and sometimes even more; I enjoy and
then refine!” She went on to say, “I feel that I am learning again.
I believe that my perception and my ability to read are going to
eventually come back, but I also know that it might be long before
that moment arrives!”
During that visit, I asked her to read some simple sentences;
I was so excited to observe her success. She was able to read a
few letters and some simple words. Although it was still difficult
for her to name the colors or group them on the basis of their
similarities, she made some improvement. I can see her young,
talented brain marching on the path to recovery perhaps through
a “detour” bypassing the “disconnection.”
Finally, by observing her voyage, I gained significant insight into
the intricacies of brain connections, and most importantly, the
consequences of such seemingly minor deficits in a person’s life. v
Disclosure Statement
The author(s) have no conflicts of interest to disclose.
Acknowledgment
The author would like to thank Alberto Espay, MD, MS, and Rhonna Shatz, MD,
for comments on an earlier draft of this article.
How to Cite this Article
Obeidat A. Disconnection. Perm J 2016 Summer;20(3):15-165. DOI: http://
dx.doi.org/10.7812/TPP/15-165.
Reference
1. NIH stroke scale [Internet]. Bethesda, MD: National Institute of Health, National
Institute of Neurological Disorders and Stroke; 2013 Dec [cited 2016 Mar 3]. Available
from: www.ninds.nih.gov/doctors/stroke_scale_training.htm
Ahmed Obeidat, MD, PhD, is a Resident in Neurology at the University
of Cincinnati in Ohio. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-165
111
CASE REPORTS
Metastatic Renal Cell Carcinoma Presenting as Painful Chewing
Successfully Treated with Combined Nivolumab and Sunitinib
Fade Mahmoud, MD, FACP; Al-Ola Abdallah, MD; Konstantinos Arnaoutakis, MD; Issam Makhoul, MD
E-pub: 06/27/2016 ABSTRACT
Introduction: Metastatic renal cell
carcinoma (RCC) to the head and neck is
rare. It is the third-most common cause of
distant metastasis to the head and neck,
after breast cancer and lung cancer. Several drugs are available to treat metastatic
RCC including high-dose interleukin and
targeted therapy. Immunotherapy with
nivolumab was recently approved by the
US Food and Drug Administration (FDA)
as a second-line treatment for patients
with metastatic RCC.
Case Presentation: We present a
case of metastatic RCC in a 71-yearold man with a single complaint of a
1-year history of pain while chewing
food. Positron emission tomographycomputed tomography showed diffuse
metastatic disease. Nivolumab, off-label
use before its recent FDA approval, was
combined with sunitinib and resulted
in an excellent and ongoing response.
Discussion: RCC is the third-most
common cause of distant metastasis
to the head and neck. The patient described in this case did not have any
symptoms commonly seen in RCC,
such as painless hematuria, weight loss,
anorexia, fatigue, or anemia, despite the
bulk of his disease. The other important
aspect of this case is the almost complete response of his metastatic disease
to the combination of nivolumab and
sunitinib that was used off label before
the FDA issued the approval. Future
clinical trials should look at combining
immunotherapy with targeted therapy
in metastatic RCC.
Perm J 2016 Summer;20(3):15-149
http://dx.doi.org/10.7812/TPP/15-149
INTRODUCTION
Renal cell carcinoma (RCC) is more
common in men than in women, with an
overall annual incidence of approximately
3.7%.1 The median age of onset is around
64 years.1 Approximately 62,000 new cases
and 14,000 deaths caused by RCC occur
annually.1 Up to 30% of patients with
RCC present with metastatic disease. 1
Most patients are asymptomatic until
the disease is advanced. The classic triad
of flank pain, hematuria, and a palpable
abdominal mass is present in only 9% of
patients. Several risk factors are thought to
play a role in the etiology of RCC; these
include smoking, hypertension, obesity,
renal cystic disease, use of nonsteroidal
anti-inflammatory drugs and other analgesics, chronic hepatitis C infection, and
history of kidney stones.2-5
High-dose interleukin (HDIL-2) is the
only therapy that provides a potential cure
in a minority of patients.6 Several targeted
therapies are approved as first-line for those
patients who are not fit for HDIL-2.6
The recent advent of immunotherapy
with checkpoint inhibitors has brought
hope to patients with metastatic renal
cell carcinoma. In this case we discuss a
unique presentation of metastatic renal
cell carcinoma. Also we report an excellent
sustained tumor response to combined
sunitinib and nivolumab.
CASE PRESENTATION
A 71-year-old man presented with pain
while chewing, progressively worse, during
the last year. He initially saw his dentist,
and an oral exam did not reveal any abnormalities. Pain medications were prescribed for use as needed. His symptoms
gradually got worse, so he was referred to
an otolaryngologist.
Soft tissue neck computed tomography (CT) with contrast revealed a 5-cm
intensely enhancing mass with extensive
vascular supply in the left masticator space
(Figure 1). Fine needle aspiration of the
Figure 1. Soft tissue neck computed tomography revealing a 5-cm intensely enhancing
mass with extensive vascular supply in the left masticator space. A. Sagittal view.
B. Transverse view.
Fade Mahmoud, MD, FACP, is an Assistant Professor of Medicine in the Department of Hematology and
Oncology at the University of Arkansas for Medical Sciences in Little Rock. E-mail: [email protected].
Al-Ola Abdallah, MD, is a Fellow in the Department of Hematology and Oncology at the University of Arkansas
for Medical Sciences in Little Rock. E-mail: [email protected]. Konstantinos Arnaoutakis, MD, is an
Associate Professor of Medicine in the Department of Hematology and Oncology at the University of Arkansas
for Medical Sciences in Little Rock. E-mail: [email protected]. Issam Makhoul, MD, is an Associate
Professor of Medicine in the Department of Hematology and Oncology at the University of Arkansas
for Medical Sciences in Little Rock. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-149
1
CASE REPORTS
Metastatic Renal Cell Carcinoma Presenting as Painful Chewing Successfully Treated with Combined Nivolumab and Sunitinib
mass showed large cells with clear vesicular cytoplasm. These cells were reactive to
paired box gene 8 (PAX8) and pankeratin,
whereas the supporting cells were reactive
to smooth muscle actin. These findings were
suggestive of metastatic renal cell carcinoma
(RCC). Full-body positron emission tomography (PET)-CT confirmed the above
findings but also revealed masses at the inferior pole of the left kidney, retroperitoneal
lymphadenopathy, and bilateral lung nodules (Figure 2A). The differential diagnosis
based on the location of the mass included
schwannoma, hemangiopericytoma, angiosarcoma, lymphoma, and metastatic
carcinoma, particularly lung carcinoma
and RCC. Sunitinib, an inhibitor of cellular signaling that targets multiple receptor tyrosine kinases, was initiated at 50 mg
orally daily (4 weeks on and 2 weeks off).
His pain was controlled with opioids, but
we discussed with him palliative radiation
therapy to the left masticator space mass in
case his pain became resistent to opioids.
Follow up PET-CT postsunitinib therapy
showed an interval progression of his disease
(Figure 2B). Nivolumab, an anti-program
death receptor 1 inhibitor, was not approved
yet by the US Food and Drug Administration, but we decided to add it to sunitinib,
and the combined treatment resulted in
almost complete response (Figure 2C).
Table 1 illustrates a timeline of his followup visits, diagnostic tests, and interventions.
DISCUSSION
Surpassed only by breast cancer and
lung cancer, RCC is the third-most common cause of distant metastasis to the
head and neck.7 Head-and-neck metastasis
is the presenting complaint for 7.5% of
patients with RCC.8 However, only 1%
of patients with RCC have metastasis confined to the head and neck.8 A retrospective chart review of 21 cases of metastasis
of RCC to the head and neck found that
the most common sites of metastasis were
bone (n = 6), skin and subcutaneous tissue (n = 6), and lymph nodes (n = 5).9 A
head-and-neck metastasis may occasionally
be the presenting sign in a patient with
RCC or may follow the primary diagnosis
by many years.9 Our patient did not have
any symptoms commonly seen in RCC,
such as painless hematuria, weight loss,
anorexia, fatigue, or anemia, despite the
2
Figure 2. Sagittal positron emission tomography-computed tomography (PET-CT) scan images of full body.
A. Initial PET-CT clearly showing evidence of metastatic disease. B. Progression of disease on sunitinib.
C. Follow-up PET-CT scan revealing almost complete response to combined nivolumab and sunitinib.
bulk of his disease. It was only pain while
chewing food that led to the diagnosis of
metastatic RCC. CT scan with contrast is
the imaging modality of choice in demonstrating the vascularity and extent of
the lesion.7
The pathology revealed cells that are
reactive to PAX8 and pankeratin. PAX8
and paired box gene 2 (PAX2) are transcription factors important for fetal development of several organs, including
kidney, müllerian organs, brain, and eye.
Both are good markers for renal cell tumors. Almost all RCCs are positive for
PAX8, which is frequently expressed by
lymphoma (100%), nephrogenic adenoma
(100%), parathyroid tumors (62%), thyroid tumors (100%), and müllerian organderived tumors (92%).10,11 Tumors that
may be negative or infrequently positive
for PAX2, including chromophobe RCC,
oncocytoma, and sarcomatoid RCC, are
often positive for PAX8.12
Several drugs are available to treat metastatic RCC. Patients with good Karnofsky
performance status (≥ 80%) and intact
organ function are treated with high-dose
interleukin-2 (HDIL-2) up front. HDIL-2
can induce long-term remissions in approximately 10% of patients.12 This treatment is
associated with an approximately 4% mortality rate, so it is extremely important to
select patients who are fit for this therapy.
Several targeted therapies were approved
as first-line for those patients who are not
fit for HDIL-2, but treatment is based on
risk groups. The Memorial Sloan-Kettering
Cancer Center prognostic score stratifies
patients with metastatic RCC into poor,
intermediate, and favorable risk categories on the basis of the number of adverse
clinical and laboratory parameters present.13
Poor prognostic factors include a Karnofsky
performance status of less than 80 (80 indicates normal activity with effort and some
signs or symptoms of disease), time from
diagnosis to treatment less than 12 months,
serum lactate dehydrogenase more than 1.5
times the upper limit of normal, corrected
serum calcium greater than 10 mg/dL,
and hemoglobin less than the lower limit
of normal.13 Patients in the favorable-risk
group have no poor prognostic factors,
those in the intermediate-risk category
have 1 or 2 adverse prognostic factors, and
patients with poor-risk RCC have more
than 2 poor prognostic factors. Patients
in the favorable or intermediate risk group
are treated with sunitinib, pazopanib, or
interferon alpha plus bevacizumab, 14-16
whereas the front-line treatment for those
in the poor risk group is temsirolimus
alone.17 Axitinib and sorafenib has been
approved as second-line treatment, for use
after other targeted therapy or cytokine
therapy has failed.18
The Permanente Journal/Perm J 2016 Summer;20(3):15-149
CASE REPORTS
Metastatic Renal Cell Carcinoma Presenting as Painful Chewing Successfully Treated with Combined Nivolumab and Sunitinib
Activating the immune system appears
to be a promising strategy to treat metastatic RCC. Since 2011, 2 novel classes
of immunotherapy drugs have been approved: the cytotoxic T lymphocyte antigen 4 (CTLA-4) inhibitor ipilimumab
and the program death receptor 1 inhibitors pembrolizumab and nivolumab.19 In
melanoma the combination of ipilimumab
and nivolumab resulted in an objective
response rate of 61%.19
In a phase I trial, patients with metastatic
RCC received nivolumab in combination
with sunitinb (50 mg, 4 weeks on, 2 weeks
off) or pazopanib (800 mg daily), until
progression/unacceptable toxicity. The
starting dosage of nivolumab was 2 mg/kg
intravenously every 3 weeks with planned
escalation to 5 mg/kg intravenously every
3 weeks. Objective response rate was 52%
among patients receiving nivolumab and
sutent and 45% among those receiving
nivolumab and pazopanib. Almost half the
responses occurred by the first assessment,
which is week 6 of treatment. The investigators concluded that nivolumab plus
sutent or pazopanib showed encouraging
Table 1. Timeline of the case
Date
April 20, 2015
Date
April 18, 2015
May 19, 2015
July 7, 2015
August 5 September 15, 2015
September 21, 2015
December 15, 2015
March 8, 2016
Relevant past medical history and interventions
Chief complaint: A 71-year-old man with no past medical history presented with painful chewing during the past 1 year.
Family history:
Mother died from pancreatic cancer at the age of 69.
Father died from lung cancer at the age of 86.
Physical examination: Mild left cheek swelling.
Previous imaging: An outside-hospital, soft-tissue neck CT with contrast dated March 12, 2015 revealed a 5-cm intensely enhancing
mass with extensive vascular supply in the left masticator space.
Previous intervention: A CT-guided biopsy of the mass dated April 2, 2015 confirmed metastatic renal cell carcinoma (clear cell type).
Current intervention: Ordered whole-body PET-CT scan to complete the staging.
Summaries from initial
and follow-up visits
Diagnostic testing
Interventions
Follow-up visit
PET-CT: At least a 3.7-cm mass within the left pterygopalatine fossa,
Sunitinib 50 mg orally daily
SUV 2.4. A minimum of 10 nodules are seen scattered throughout both
(4 weeks on, 2 weeks off).
lungs; the largest measures 33 x 28 mm, SUV 6.2.
Liver: Approximately 2.1-cm focus in the posterior aspect of segment VIII,
SUV 3.1. Right suprarenal fossa: approximately 9 x 6-cm mass, SUV 2.7.
Left kidney, inferior pole: Approximately 9-cm mass, SUV 5.0.
Tolerating medication
None.
Sunitinib was approved by
without problems. States
his insurance and shipped
that he has some left
to patient. Medication
cheek swelling that comes
started May 1, 2015.
and goes
Left cheek swelling that
PET-CT: At least a 4.1 x 2.5-cm mass within the left pterygopalatine fossa, We decided to get
comes while off Sunitinib
SUV 5.5. A minimum of 10 nodules are seen scattered throughout both
nivolumab off label use. We
and goes away while on
lungs; the largest measures 36 x 29 mm, SUV 6.3.
told the patient to continue
Sunitinib
Liver: Approximately 5-cm focus in the posterior aspect of segment VIII, SUV taking sunitinib because
he had been on it for only
5.1. Right suprarenal fossa: Approximately 10.5 x 5.4-cm mass, SUV 5.3.
2 months.
Left kidney, inferior pole: Approximately 6.9-cm mass, SUV 5.6. These
findings are consistent with progression of his disease.
Patient was seen every 2
None.
Completed 4 cycles of
weeks while on nivolumab
nivolumab.
PET-CT: Complete opacification of the left maxillary sinus, SUV 6.3. A
Continue sunitinib and
minimum of 10 nodules are seen scattered throughout both lungs, most
nivolumab, restage disease
of which appear slightly improved; the largest measures 28 mm, SUV 5.5. in 3 months.
There is interval improvement in previously documented hypermetabolic
right hepatic focus, which on today’s study has an SUV of 2.9 (prior SUV
5.1). Stable to slight morphologic and metabolic improvement in previously
documented left and right renal masses.
Tolerating treatment well
PET-CT: Decreased extent and metabolic activity of left masticator
Continue combined sunitinib
with combined sunitinib
space metastasis, SUV 3.7. Decreased size of the left lower pole renal
and nivolumab, restage
and nivolumab
mass. Decrease in size, and metabolic activity of lung, right adrenal,
disease in 3 months.
retroperitoneal soft tissue and lymph node metastases.
Tolerating treatment well
PET-CT: Improving metabolic activity in the left masticator space, SUV 2.7
Continue combined sunitinib
with combined sunitinib
(prior SUV 3.6). Stable to slight improvement in the previously documented
and nivolumab, restage
and nivolumab
subcentimeter right lung nodules and 1.7-cm left upper lobe mass.
disease in 3 months.
CT = computed tomography; PET = positron emission tomography; SUV = standardized uptake value.
The Permanente Journal/Perm J 2016 Summer;20(3):15-149
3
CASE REPORTS
Metastatic Renal Cell Carcinoma Presenting as Painful Chewing Successfully Treated with Combined Nivolumab and Sunitinib
antitumor activity and a manageable safety
profile in patients with metastatic RCC.20
The decision to add nivolumab (off-label
use) in our patient was based on the results
of the above phase I trial. Three months later
(November 23, 2015), the FDA approved
nivolumab on the basis of results of an open
label, randomized study that showed an
overall survival advantage of nivolumab over
everolimus in patients with metastatic RCC
who failed antiangiogenic agents.21 Those
treated with nivolumab lived an average of
25 months compared with 19.6 months in
those treated with Afinitor. Additionally,
21.5% of those treated with nivolumab
experienced a complete or partial shrinkage
of their tumors, which lasted an average of
23 months, compared with 3.9% of those
taking everolimus, lasting an average of 13.7
months.21,22
Our patient appears to be tolerating the
combination of nivolumab and sunitinib.
His follow-up PET-CT showed improvement in his disease (Table 1).
CONCLUSIONS
Metastatic cancer to the head and neck is
rare. Breast cancer, lung cancer, and RCC
are the most common causes of distant
metastasis to the head and neck. In our
case, pain while chewing food was the only
presenting symptom of metastatic RCC.
Immunotherapy with interleukin-2 or
interferon-alpha, biologic, or targeted therapy are all viable options for patients with
metastatic RCC. Most recently the FDA
approved nivolumab in the second-line setting after patients have failed antiangiogenic
agents. Our patient had an almost complete
response to combined nivolumab and
sunitinib. Further studies should look into
the combination of targeted therapy and
immunotherapy in the front-line setting
among patients with metastatic RCC. v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
Acknowledgment
Leslie Parker, ELS, provided editorial assistance.
How to Cite this Article
Mahmoud F, Abdallah AO, Arnaoutakis K,
Makhoul I. Metastatic renal cell carcinoma
presenting as painful chewing successfully treated
with combined nivolumab and sunitinib. Perm J
2016 Summer;20(3):15-149. DOI: http://dx.doi.org/
10.7812/TPP/15-149.
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2. Hunt JD, van der Hel OL, McMillan GP, Boffetta P,
Brennan P. Renal cell carcinoma in relation to
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org/10.1002/ijc.20618.
3. Ljungberg B, Campbell SC, Choi HY, et al. The
epidemiology of renal cell carcinoma. Eur Urol 2011
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eururo.2011.06.049. Erratum in: Eur Urol 2011
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eururo.2011.09.001.
4. Cho E, Curhan G, Hankinson SE, et al.
Prospective evaluation of analgesic use and risk
of renal cell cancer. Arch Intern Med 2011 Sep
12;171(16):1487-93. DOI: http://dx.doi.org/10.1001/
archinternmed.2011.356.
5. Gordon SC, Moonka D, Brown KA, et al. Risk
for renal cell carcinoma in chronic hepatitis C
infection. Cancer Epidemiol Biomarkers Prev
2010 Apr;19(4):1066-73. DOI: http://dx.doi.
org/10.1158/1055-9965.EPI-09-1275.
6. Klapper JA, Downey SG, Smith FO, et al. High-dose
interleukin-2 for the treatment of metastatic renal
cell carcinoma: a retrospective analysis of response
and survival in patients treated in the surgery branch
at the National Cancer Institute between 1986 and
2006. Cancer 2008 Jul 15;113(2):293-301. DOI:
http://dx.doi.org/10.1002/cncr.23552.
7. Pritchyk KM, Schiff BA, Newkirk KA, Krowiak E,
Deeb ZE. Metastatic renal cell carcinoma to the head
and neck. Laryngoscope 2002 Sep;112(9):1598-602.
DOI: http://dx.doi.org/10.1097/00005537-20020900000012.
8. Boles R, Cerny J. Head and neck metastases from
renal carcinomas. Mich Med 1971 Jul;70(16):616-8.
9. Langille G, Taylor SM, Bullock MJ. Metastatic renal
cell carcinoma to the head and neck: summary
of 21 cases. J Otolaryngol Head Neck Surg 2008
Aug;37(4):515-21.
10. Ozcan A, Shen SS, Hamilton C, et al. PAX 8
expression in non-neoplastic tissues, primary
tumors, and metastatic tumors: a comprehensive
immunohistochemical study. Mod Pathol 2011
Jun;24(6):751-64. DOI: http://dx.doi.org/10.1038/
modpathol.2011.3.
11. Truong LD, Shen SS. Immunohistochemical
diagnosis of renal neoplasms. Arch Pathol Lab
Med 2011 Jan;135(1):92-109. DOI: http://dx.doi.
org/10.1043/2010-0478-RAR.1.
12. Gupta R, Balzer B, Picken M, et al. Diagnostic
implications of transcription factor Pax 2 protein
and transmembrane enzyme complex carbonic
anhydrase IX immunoreactivity in adult renal
epithelial neoplasms. Am J Surg Pathol 2009
Feb;33(2):241-7. DOI: http://dx.doi.org/10.1097/
PAS.0b013e318181b828.
13. Motzer RJ, Mazumdar M, Bacik J, Berg W,
Amsterdam A, Ferrara J. Survival and prognostic
stratification of 670 patients with advanced renal cell
carcinoma. J Clin Oncol 1999 Aug;17(8):2530-40.
14. Motzer RJ, Hutson TE, Cella D, et al. Pazopanib
versus sunitinib in metastatic renal-cell carcinoma. N
Engl J Med 2013 Aug 22;369(8):722-31. DOI: http://
dx.doi.org/10.1056/NEJMoa1303989.
15. Motzer RJ, Hutson TE, Tomczak P, et al. Sunitinib
versus interferon alfa in metastatic renal-cell
carcinoma. N Engl J Med 2007 Jan 11;356(2):115-24.
DOI: http://dx.doi.org/10.1056/NEJMoa065044.
16. Escudier B, Pluzanska A, Koralewski P, et al;
AVOREN Trial Investigators. Bevacizumab plus
interferon alfa-2a for treatment of metastatic renal
cell carcinoma: a randomised, double-blind phase III
trial. Lancet 2007 Dec 22;370(9605):2103-11. DOI:
http://dx.doi.org/10.1016/S0140-6736(07)61904-7.
17. Hudes G, Carducci M, Tomczak P, et al; Global
ARCC Trial. Temsirolimus, interferon alfa, or both
for advanced renal-cell carcinoma. N Engl J Med
2007 May 31;356(22):2271-81. DOI: http://dx.doi.
org/10.1056/NEJMoa066838.
18. Hutson TE, Lesovoy V, Al-Shukri S, et al. Axitinib
versus sorafenib as first-line therapy in patients
with metastatic renal-cell carcinoma: a randomised
open-label phase 3 trial. Lancet Oncol 2013
Dec;14(13):1287-94. DOI: http://dx.doi.org/10.1016/
S1470-2045(13)70465-0.
19. Postow MA, Chesney J, Pavlick AC, et al.
Nivolumab and ipilimumab versus ipilimumab in
untreated melanoma. N Engl J Med 2015 May
21;372(21):2006-17. DOI: http://dx.doi.org/10.1056/
NEJMoa1414428.
20. Amin A, Plimack ER, Infante JR, et al. Nivolumab
(anti-PD-1; BMS-936558, ONO-4538) in combination
with sunitinib or pazopanib in patients (pts) with
metastatic renal cell carcinoma (mRCC). ASCO
Annual Meeting Abstracts. J Clinical Oncol 2014 May
20;32(15 Suppl):5010.
21. FDA News Release: FDA approves Opdivo to treat
advanced form of kidney cancer [Internet]. Silver
Spring, MD: US Food and Drug Administration; 2015
Nov 23 [cited 2016 Mar 9]. Available from: www.fda.
gov/NewsEvents/Newsroom/PressAnnouncements/
ucm473971.htm.
22. Motzer RJ, Escudier B, McDermott DF, et al;
CheckMate 025 Investigators. Nivolumab versus
Everolimus in advanced renal-cell carcinoma.
N Engl J Med 2015 Nov 5; 373(19):1803-13. DOI:
http://dx.doi.org/10.1056/NEJMoa1510665.
Flexibility
Fixity of purpose requires flexibility of method.
— Harold G Wolff, 1898-1962, American physician, neurologist, and scientist
4
The Permanente Journal/Perm J 2016 Summer;20(3):15-149
CASE REPORTS
Treatment of Tracheoinnominate Fistula with
Ligation of the Innominate Artery: A Case Report
Rhiana S Menen, MD; Jimmy J Pak, MD; Matthew A Dowell, PA; Ashish R Patel, MD;
Simon K Ashiku, MD; Jeffrey B Velotta, MD
E-pub: 06/22/2016 ABSTRACT
Introduction: Tracheoinnominate
fistula, a rare complication of tracheostomy, carries high mortality regardless
of treatment; therefore prevention and
quick diagnosis is pertinent to survival.
Case Presentation: A 76-year-old
man who underwent emergent tracheostomy placement presented on
postoperative day 10 with massive
hemorrhage concerning for tracheoinnominate fistula and was treated with
median sternotomy and ligation of the
innominate artery.
Discussion: This presentation describes a concise diagnosis and treatment plan for a rare event. The key to
good outcomes is quick diagnosis and
urgent surgical intervention.
INTRODUCTION
Tracheoinnominate fistula (TIF) is a devastating complication of tracheostomy with
100% mortality reported in the absence
of treatment. Here we report the case of a
76-year-old man who survived ligation of
the innominate artery, and discuss diagnosis, control of initial hemorrhage, and efficacy of this and other approaches to repair.
CASE PRESENTATION
A 76-year-old man with a history of
recurrent papillary thyroid cancer, modified radical neck dissection, and previous
neck radiation that was complicated by
bilateral recurrent laryngeal nerve injury,
underwent emergent tracheostomy. On
postoperative day 8, less than a teaspoon
of blood emanated from the tracheostomy
site after coughing. This was thought to
be related to granulation tissue around
the stoma, thus bronchoscopy was not
Perm J 2016 Summer;20(3):15-166
http://dx.doi.org/10.7812/TPP/15-166
performed. Massive hemorrhage through
the tracheostomy occurred on day 10.
Direct tamponade through the neck incision (Utley maneuver) was immediately
lifesaving. Massive transfusion protocol
was activated and thoracic and vascular
surgical services were emergently consulted. Median sternotomy with ligation
of the innominate artery was performed.
The innominate artery was extremely
friable, consistent with postradiation
changes, and was ligated and divided
with the addition of a pericardial patch
and pledgeted 2-0 prolene sutures owing
to the poor quality of the artery. The patient was stabilized and returned to the
intensive care unit fully neurologically
intact. On postoperative day 2, with the
patient medically stable in the intensive
care unit, he returned to the operating
room for formal revision of the innominate stump owing to concern over its friability from extensive radiation changes,
as well as to prevent its constant contact
with tracheal secretions. The stump was
debrided, ligated, and buttressed with a
pedicled left pectoralis major muscle flap
to prevent refistulization. On postoperative day 3, he became hypotensive longer
than 10 minutes owing to intermittent
atrial fibrillation. He was later noted on
examination to have a left-sided hemiparesis. A moderate right middle cerebral
artery hemispheric infarct was visualized
on urgent computed tomography scan
of the brain. On the basis of imaging
and timing of onset of hypotension, the
cause of the stroke was determined to be
ischemia from prolonged hypotension,
rather than a direct result of decreased
perfusion after ligation. Over time he
regained his strength and was fully alert
and communicative. The patient was
transferred to the ward and is currently
doing well in a rehabilitation facility.
DISCUSSION
TIF is a rare but devastating complication
of tracheostomy. The incidence of TIF is
reported from 0.1% to 1%.1 There is 100%
mortality if no intervention is pursued.1
TIF occurs within the first 3 weeks after
tracheostomy in 72% of the patients that
develop this condition1 but may occur years
after the surgical procedure.2 Risk factors
for TIF include tracheal infection, steroid
use, creation of the tracheostomy below the
third tracheal ring, pressure necrosis caused
by overinflation of the cuff or malposition,
and chest deformity leading to a high-riding
innominate artery. Surgical texts dictate immediate repair or ligation of the innominate
artery; however, there are only sporadic case
reports available in the literature.
Diagnosis and Management
of Initial Hemorrhage
Bleeding from the tracheostomy site
is relatively common, though true TIF is
rare. “Early” bleeding occurs within hours
after tracheostomy and is generally caused
by failure of local hemostasis or underlying
coagulopathy. Incidence of TIFs, however,
peak 1 to 2 weeks postoperatively and may
manifest as a “sentinel bleed,” wherein
there is a brief episode of bright red, often
pulsatile bleeding from the tracheostomy
site. Unfortunately, only 35% of patients
with TIF exhibit this pathognomonic sign,2
making preemptive diagnosis challenging.
Confirming the diagnosis of TIF can
be difficult and may include bronchoscopy, arteriography, or computed tomography angiography with 3-dimensional
Rhiana S Menen, MD, is a Surgeon at the University of California San Francisco-Eastbay in Oakland. E-mail:
[email protected]. Jimmy J Pak, MD, is a Vascular Surgeon at the Oakland Medical Center in CA.
E-mail: [email protected]. Matthew A Dowell, PA, is a Thoracic Surgery Physician Assistant at the Oakland
Medical Center in CA. E-mail: [email protected]. Ashish R Patel, MD, is a Thoracic Surgeon at the
Oakland Medical Center in CA. E-mail: [email protected]. Simon K Ashiku, MD, is a Thoracic Surgeon
at the Oakland Medical Center in CA. E-mail: [email protected]. Jeffrey B Velotta, MD, is a Thoracic
Surgeon at the Oakland Medical Center in CA. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-166
1
CASE REPORTS
Treatment of Tracheoinnominate Fistula with Ligation of the Innominate Artery: A Case Report
reconstruction. Taken together, these studies have only a 20% to 30% sensitivity
to confirm the diagnosis3 and therefore a
high clinical suspicion must be employed
to improve mortality. Any tracheostomal
bleeding and/or hemoptysis beyond the
first 48 postoperative hours must be considered a sentinel bleed and investigated for
the possibility of TIF.2 Even with prompt
identification, surgery is associated with a
greater than 50% mortality owing to both
perioperative hemorrhage and infectious
complications.4 Overall prognosis remains
poor, with 56% of survivors reported dead
within 2 months,5 probably because of the
high prevalence of associated comorbidities
within this critically ill population.
Early Control of Hemorrhage
When patients present with massive hemorrhage, a stepwise progression of bedside
interventions can be rapidly applied to temporize bleeding, maintain a patent airway,
and bridge patients to definitive therapy. The
most common site of TIF is at the level of
the endotracheal cuff; therefore, overinflation of the tracheostomy cuff should be attempted first. This technique is successful in
nearly 85% of cases.1 In patients in whom it
is not, the tracheostomy should be replaced
with a cuffed endotracheal tube distal to
the site of the bleeding.1 If hemorrhage persists, the Utley maneuver can be employed
wherein a finger is placed into the airway,
with or without extension of the incision,
and the innominate artery is compressed
against the posterior sternum. Furukawa
and colleagues6 describe prompt control of
the tracheostomy hemorrhage by insertion of
a tracheostomy cannula with a wired silastic
tube and an adjustable wing, and overinflating the cuff to provide hemostasis. This
resulted in control of hemorrhage in 7 of 7
patients in their case series.
Innominate Artery Ligation
Once TIF has been identified as the
cause of hemorrhage, surgical texts describe division of the innominate artery
and the separation of the oversewn ends
from the trachea. By ligating only the innominate artery, the subclavian and carotid
circulation are left in continuity. Innominate artery ligation has an estimated 10%
risk of neurologic deficit.6 This number
is roughly supported by case reports in
the literature, although this is probably
2
because of a reporting bias in favor of successful patient outcomes.
One of the largest case series of TIF
ligation by Furukawa and colleagues6 describes excellent results seen in 7 pediatric
patients with existing severe neurologic
deficits. Operative repair was approached by
collar incision with partial sternotomy and
innominate artery division. Cerebral blood
flow was monitored by the blood pressure
difference in the bilateral upper extremities
and by near-infrared spectroscopy. Only 1
of 7 patients was noted to have evidence of
decreased cerebral perfusion after innominate artery clamping, and an innominate to
right carotid artery bypass was performed.
The tracheal fistula was left adherent to the
innominate artery in all but 1 patient, in
whom a pericardial covering was placed
between the trachea and innominate artery.
Long-term follow-up confirmed no new
neurologic deficits including any vascular,
tracheal, or new computed tomography
findings postoperatively. Overall survival
was an impressive 84% at 37 months,7
compared with the reported 15% to 71%
cited elsewhere in the literature.8
In the case presented in this report,
ligation was accomplished via median
sternotomy, which allowed full exposure
of the supra-aortic trunk. This was particularly useful in the context of an infected,
postradiation operative field. However,
this approach also carries the risk of both
mediastinitis and wound infection. A 39%
incidence of sternal wound complications
has been reported in patients with tracheostomy and median sternotomy.7
Recent technologic advancements in
interventional radiology and endovascular techniques have allowed clinicians to
pursue less invasive options to manage TIF.
Troutman et al5 managed to successfully
deploy an endovascular stent graft via the
right common carotid artery in addition to
a carotid to subclavian bypass. The patient
survived the initial event; however, after
three months the patient succumbed to
recurrent hemoptysis and subsequent cardiac arrest. Troutman et al5 concluded that
endovascular stent management of TIF
offers a less invasive option and can substitute as a bridge for poor surgical candidates
with the potential for becoming better
surgical candidates. The main advantage
to endovascular management of TIF is
less morbidity. The limitations to the use
of endovascular stent grafting include 1)
inadequacy of resources and expertise at
smaller community-based hospitals; 2)
inadequate landing zones for stent placement, necessitating an additional surgical
bypass to maintain flow; and 3) lack of
data because of so few cases.
TIF is a rare but devastating sequela of
a common surgical procedure. With early
recognition, rapid control of hemorrhage,
and prompt intervention, disruption of the
innominate artery through division and
ligation is a viable repair option that has
been shown to produce sustained survival
with minimal risk of neurologic deficit. v
Disclosure Statement
The author(s) have no conflicts of interest to
report.
Acknowledgment
Mary Corrado, ELS, provided editorial assistance.
How to Cite this Article
Menen RS, Pak JJ, Dowell MA, Patel AR, Ashiku SK,
Velotta JB. Treatment of tracheoinnominate fistula
with ligation of the innominate artery: a case report.
Perm J 2016 Summer;20(3):15-166. DOI: http://
dx.doi.org/10.7812/TPP/15-166.
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http://dx.doi.org/10.1093/bja/aei282.
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5. Troutman DA, Dougherty MJ, Spivack AI, Calligaro KD.
Stent graft placement for a tracheoinnominate artery
fistula. Ann Vasc Surg 2014 May;28(4):1037.e21-4.
DOI: http://dx.doi.org/10.1016/j.avsg.2013.08.021.
6. Furukawa K, Kamohara K, Itoh M, Morokuma H,
Morita S. Operative technique for tracheoinnominate artery fistula repair. J Vasc Surg 2014
Apr;59(4):1163-7. DOI: http://dx.doi.org/10.1016/j.
jvs.2013.09.013.
7. Hazarika P, Kamath SG, Balakrishnan R, Girish R,
Harish K. Tracheo-innominate artery fistula: a rare
complication in a laryngectomized patient. J Laryngol
Otol 2002 Jul;116(7):562-4. DOI: http://dx.doi.
org/10.1258/002221502760132502.
8. Gelman JJ, Aro M, Weiss SM. Tracheo-innominate
artery fistula. J Am Coll Surg 1994 Nov;179(5):626-34.
The Permanente Journal/Perm J 2016 Summer;20(3):15-166
CASE REPORTS
Monoarticular Poncet Disease after Pulmonary Tuberculosis:
A Rare Case Report and Review of Literature
Paritosh Garg, MD; Nikhil Gupta, MD, MBBS; Mohit Arora, MS
Perm J 2016 Summer;20(3):15-199
E-pub: 07/15/2016 http://dx.doi.org/10.7812/TPP/15-199
ABSTRACT
Introduction: Tuberculosis is a major health problem worldwide, more
so in Asian countries and especially
India. Being a communicable disease,
it can affect the lives of many people.
Tuberculosis has varied manifestations
and can affect almost every part of the
human body. Pulmonary tuberculosis
is the most common form. Poncet
disease (tuberculous rheumatism) is a
polyarticular arthritis that occurs during
acute tuberculosis infection in which
no mycobacterial involvement can
be found or no other known cause of
polyarthritis is detected.
Case presentation: We describe an
atypical presentation of active pulmonary tuberculosis with monoarticular
Poncet disease of the right knee in a
24-year-old woman.
Discussion: The diagnosis of Poncet
disease is mainly clinical with exclusion
of other causes. It generally presents as
an acute or subacute form; however,
chronic forms have been described in
the literature.
INTRODUCTION
Tuberculous arthritis is a monoarticular,
infectious, and destructive disease. However, tuberculous rheumatism, popularly
known as Poncet disease, is a nondestructive parainfective polyarthritis occurring
in patients with active tuberculosis (TB),
which resolves completely with antituberculosis therapy.1 The diagnosis of this
entity is largely clinical and is made by
excluding other causes of polyarthritis
in a patient with documented active TB.
Monoarticular involvement in tubercular
rheumatism has not been previously described, to our knowledge. We describe
a rare and atypical presentation of Poncet disease with involvement of only the
right knee.
CASE PRESENTATION
A 24-year-old woman presented with
complaints of continuous fever for 15
days, which was associated with suddenonset swelling of her right knee for 5 days.
There was a history of anorexia. There was
no history of cough, burning micturition,
vaginal discharge, abdominal complaints,
or trauma. There was no history of TB,
and the patient was sexually inactive. Results of the physical examination revealed
swelling in the right knee, which was not
tender. The temperature over the swelling
was normal. The remaining findings of the
examination were normal.
The laboratory tests showed a leukocyte
count of 10.4 × 109/L (10,400/μL; 65% of
segmented neutrophils), erythrocyte sedimentation rate of 32 mm/h, and C-reactive
protein level of 159 mg/dL. The Mantoux
test result was strongly positive (16 × 12
mm). The urinalysis result was normal,
and urine culture and blood culture were
negative. The antinuclear antibody test
result was normal, and the test results for
rheumatoid factor were negative. Sexually
transmitted diseases were ruled out, and
the serologic test result for human immunodeficiency virus was negative. The
serum uric acid level was 5.8 mg/dL. Fifty
milliliters of synovial fluid was aspirated
from the knee joint. The analysis of the
synovial fluid showed a leukocyte count
of 5 × 109/L with a differential count of
polymorphs being 55% and leukocytes being 45%. The synovial fluid was negative
for TB using polymerase chain reaction.
There were no crystals and the cultures
were sterile.
Figure 1. Contrast-enhanced computed tomography
scan of chest reveals multiple enlarged pretracheal
lymph nodes.
Figure 2. X-ray film of right knee joint (at right)
shows periarticular soft-tissue swelling.
The chest x-ray film was normal.
Contrast-enhanced computed tomography scan of the chest revealed multiple
enlarged lymph nodes in the pretracheal
region (Figure 1) and the prevascular and
precarinal regions. However, the contrastenhanced computed tomography scan of
the abdomen was normal. The x-ray film
of the right knee joint showed periarticular
soft-tissue swelling, and active TB with no
changes (Figure 2). Fine-needle aspiration
Paritosh Garg, MD, is a Pathologist at the University College of Medical Sciences and Guru Tag Bahadur Hospital in
Dilshad Garden, Delhi, India. E-mail: [email protected]. Nikhil Gupta, MD, MBBS, is a Fellow in Clinical
Immunology and Rheumatology at the Christian Medical College and Hospital in Vellore, Tamil Nadu, India. E-mail:
[email protected]. Mohit Arora, MS, is an Orthopedician at the University College of Medical Sciences and
Guru Tag Bahadur Hospital in Dilshad Garden, Delhi, India. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-199
1
CASE REPORTS
Monoarticular Poncet Disease after Pulmonary Tuberculosis: A Rare Case Report and Review of Literature
Figure 3. Fine-needle aspiration cytology of
pretracheal lymph nodes reveals epithelioid cell
granulomas.
cytology of the pretracheal lymph nodes
revealed epithelioid cell granulomas
(Figure 3). The acid-fast bacillus test
from the epithelioid cell granulomatous
lymph node material was positive.
The patient began antitubercular therapy. On follow-up examination, she was
afebrile. The joint swelling reduced after
two weeks of treatment and disappeared
in about a month. In the patient’s continuation phase of treatment, she became
symptom-free (Figure 4).
The etiopathogenesis of Poncet disease is
proposed to be molecular mimicry and
thermal shock proteins.6
Our patient had active pulmonary tubercular findings on a computed tomography scan and swelling of the right knee,
which was found to be inflammatory,
without any evidence of organism in the
synovial fluid. Thus, a diagnosis of Poncet
disease was made. Our patient responded
to the antitubercular drugs, and her knee
swelling was reduced over two weeks.
Although Poncet disease has been
described as a polyarthritis, a review of
the literature reveals it to be an often
pauciarticular, symmetrical arthritis predominantly involving the large joints.1,7,8
The tuberculous septic monoarthritis, in
which the mycobacterium can be isolated
from the culture of the affected joint, is a
known entity. However, to the best of our
knowledge, monoarticular Poncet disease
has not been described in the literature.
2
CONCLUSION
Poncet disease has been described in the
literature as polyarticular disease without
any evidence of organism isolated from
the synovial fluid. However, because of
a scarcity of data and lack of knowledge,
we may be missing quite a few cases of
monoarticular Poncet disease. Thorough
research and sharing of knowledge may
be required for the discovery of such a rare
presentation. v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
Acknowledgment
Kathleen Louden, ELS, of Louden Health
Communications provided editorial assistance.
How to Cite this Article
Garg P, Gupta N, Arora M. Monoarticular Poncet
disease after pulmonary tuberculosis: A rare
case report and review of literature. Perm J 2016
Summer;20(3):15-199. DOI: http://dx.doi.org/
10.7812/TPP/15-199.
DISCUSSION
TB is a major communicable disease.
According to the World Health Organization’s 2011 report, there were an estimated
8.7 million incident cases of TB (range,
8.3 million to 9.0 million) globally.2 Because of such a massive burden of TB,
extrapulmonary manifestations of TB,
including arthritis, are increasing. Musculoskeletal manifestations are the most
common form of extrapulmonary TB,
accounting for 10% to 19% of cases.3-5
Along with septic TB arthritis, nonsuppurative reactive arthritis has been described
in association with TB, a condition that
is also known as Poncet disease.6 Because
of complicated and atypical presentations,
this entity is likely to be underdiagnosed.
Moreover, few physicians know the disease well, and the literature related to
this disease is scarce and restricted to case
reports, which probably contributes to its
underdiagnosis.
The diagnosis of Poncet disease is
mainly clinical with exclusion of other
causes. It generally presents as an acute
or subacute form; however, chronic forms
have been described in the literature.4
This lack of reporting may be because of
a scarcity of data and a lack of knowledge
about this entity called Poncet disease.
References
Figure 4. Timeline of history, relevant investigations,
and treatment of patient with Poncet disease.
AFB = acid-fast bacillus; CECT = contrast-enhanced
computed tomography; FNAC = fine-needle aspiration
cytology; L = leukocytes; P = polymorphs; PCR = polymerase chain reaction; TB = tuberculosis.
1. Isaacs AJ, Sturrock RD. Poncet’s disease—fact or
fiction? A re-appraisal of tuberculous rheumatism.
Tubercle 1974 Jun;55(2):135-42. DOI: http://dx.doi.
org/10.1016/0041-3879(74)90007-5.
2. Global tuberculosis report 2012 [Internet]. Geneva,
Switzerland: World Health Organization; 2011 [cited
2016 Mar 16]. Available from: www.who.int/tb/
publications/global_report/gtbr12_main.pdf.
3. Malaviya AN, Kotwal PP. Arthritis associated with
tuberculosis. Best Pract Res Clin Rheumatol 2003
Apr;17(2):319-43. DOI: http://dx.doi.org/10.1016/
s1521-6942(02)00126-2.
4. Hunfeld KP, Rittmeister M, Wichelhaus TA, Brade V,
Enzensberger R. Two cases of chronic arthritis of the
forearm due to Mycobacterium tuberculosis. Eur J
Clin Microbiol Infect Dis 1998 May;17(5):344-8. DOI:
http://dx.doi.org/10.1007/s100960050079.
5. Wollheim FA. Enteropathic arthritis. In: Kelley WN,
Harris ED Jr, Ruddy S, Sledge CB, editors. Textbook
of rheumatology. 5th ed. Phildelphia, PA: WB
Saunders Co; 1997 Jan 15. p 1006-14.
6. Pereira JCB. [Artropatia de Poncet—série de casos].
[Article in Portuguese]. Pulmão RJ 2005;14(4):321-4.
7. Bloxham CA, Addy DP. Poncet’s disease: parainfective tuberculous polyarthropathy. Br Med J 1978
Jun 17;1(6127):1590. DOI: http://dx.doi.org/10.1136/
bmj.1.6127.1590.
8. Arora VK, Verma R. Tuberculous rheumatism
(Poncet’s disease): three case reports. Indian J
Tuberc 1991 Jan;38:229-30.
The Permanente Journal/Perm J 2016 Summer;20(3):15-199
CLINICAL MEDICINE
Image Diagnosis: Encephalopathy Resulting
from Dural Arteriovenous Fistula
Ana Filipa Santos, MD; Célia Machado, MD; Sara Varanda, MD; João Pinho, MD;
Manuel Ribeiro, MD; Jaime Rocha, MD; Ricardo Maré, MD
E-pub: 07/08/2016 Perm J 2016 Summer;20(3):15-218
http://dx.doi.org/10.7812/TPP/15-218
CASE REPORT
A 69-year-old woman presented to the
Neurology Department with 2 months
of progressive psychomotor slowing, inability to concentrate, and periods of disorientation. Her past medical history was
unremarkable, and she was taking no medication. There was no history of trauma. On
neurologic examination she was alert but
taking a long time to answer, apathetic,
distractable, and hypophonic with right
visual and sensitive hemiextinction and left
hemiparesis. Montreal Cognitive Assessment Exam score was 11/30. A computed
tomography scan of the brain (Figure 1)
showed possible convexity subarachnoid
hemorrhage that the brain magnetic resonange imaging (MRI)/MRI angiography
(Figures 2 and 3) revealed to be engorged
cerebral vessels. Hyperintensity in the deep
white matter of the cerebral hemispheres
was also present. Cerebral angiography
(Figure 4) revealed a dural arteriovenous
fistula (DAVF) of the superior sagittal sinus
and torcula (Cognard classification IIb1).
The patient underwent endovascular
embolization, with combined transarterial
(n-butyl-cyanoacrylate) and transvenous
(coils) approach, resulting in proximal
occlusion of the superior sagital sinus,
torcula, and transverse sinus (Figure 5).
Posttreatment angiography revealed near
complete DAVF occlusion (Figure 6). Control MRI revealed a marked decrease of the
deep white matter hyperintensity and no
engorged cerebral veins (Figures 7 and 8).
The patient’s mental status improved post
procedure (Montreal Cognitive Assessment
Exam score, 20/30), and she progressively
came back to her baseline.
Figure 1. Computed tomography scan of the brain showing possible convexity subarachnoid hemorrhage.
Figure 2. Coronal-view T2-weighted magnetic
resonance image of the brain. The white arrows
indicate engorged cerebral veins visible over the
surfaces of the hemispheres bilaterally.
Figure 3. Axial-view T2-weighted magnetic resonance
image of the brain. The white crosses indicate the
increased signal that is diffusely present within the
deep white matter of the cerebral hemispheres.
Ana Filipa Santos, MD, is a Neurologist at Hospital de Braga in Braga, Portugal. E-mail: [email protected] Célia Machado, MD,
is a Neurologist at Hospital de Braga in Braga, Portugal. E-mail: [email protected]. Sara Varanda, MD, is a Neurologist at
Hospital de Braga in Braga, Portugal. E-mail: [email protected]. João Pinho, MD, is a Neurologist at Hospital de Braga in Braga,
Portugal. E-mail: [email protected]. Manuel Ribeiro, MD, is a Neuroradiologist at Centro Hospitalar de Vila Nova de Gaia-Espinho in
Gaia, Portugal. E-mail: [email protected]. Jaime Rocha, MD, is a Neuroradiologist at Hospital de Braga in Braga, Portugal. E-mail:
[email protected]. Ricardo Maré, MD, is a Neurologist at Hospital de Braga in Braga, Portugal. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-218
1
CLINICAL MEDICINE
Image Diagnosis: Encephalopathy Resulting from Dural Arteriovenous Fistula
Figure 4. Cerebral angiography performed before
endovascular embolization. The black arrowhead
indicates dural arteriovenous fistula of the superior
sagittal sinus. The black asterisk indicates dural
arteriovenous fistula of the torcula.
Figure 5. Cerebral angiography performed after
endovascular embolization. The black arrow
indicates transvenous coils.
DISCUSSION
acuity, seizures, Parkinsonism, cerebellar
symptoms, apathy, and dementia.2-4
DAVFs are abnormal arteriovenous connections within the dura, usually located
within the walls of a dural sinus or an adjacent cortical vein, and account for 10%
to 15% of all intracranial arteriovenous
lesions.2-4 The initiating events which lead
to their development are not clear, but the
literature reports association with trauma,
infection, recent surgery, and dural sinus
thrombosis.2-4 A wide variety of signs and
symptoms, which can vary because of lesion
location and pattern of venous drainage,
may arise from DAVFs, namely, pulsatile
tinnitus, ophthalmoplegia, proptosis, chemosis, retro-orbital pain, decreased visual
CONCLUSION
Our patient with DAVF presented with
encephalopathy with diffuse white matter
changes related to venous ischemia. Her
symptoms partially reverted with endovascular treatment.
DAVF should be considered in patients
with encephalopathy. This relatively nonspecific clinical picture may delay the diagnosis and result in further deterioration. A
high level of suspicion should be maintained
in patients who present in the context of unexplained intracranial hemorrhage without
Figure 6. Posttreatment cerebral angiography
shows near-complete occlusion of the dural
arteriovenous fistula.
significant risk factors (trauma, hypertension, or anticoagulation) or in possible subarachnoid hemorrhage in a nonaneurysmal
pattern. This should prompt imaging with
MRI and angiography, which are the gold
standard for diagnosis. DAVF recognition
is essential because these patients are potentially treatable. v
Disclosure Statement
The authors have no conflicts of interest to
disclose.
How to Cite this Article
Santos AF, Machado C, Varanda S, et al. Image
diagnosis: Encephalopathy resulting from dural
arteriovenous fistula. Perm J 2016 Summer;20(3):
15-218. DOI: http://dx.doi.org/10.7812/TPP/15-218.
References
Figure 7. Posttreatment magnetic resonance image
of the brain showing no engorged cerebral veins.
2
Figure 8. Posttreatment magnetic resonance image
of the brain. The white cross indicates a marked
decrease of the hyperintensity in the deep white
matter of the cerebral hemisphere.
1. Cognard C, Gobin YP, Pierot L, et al. Cerebral dural
arteriovenous fistulas: clinical and angiographic
correlation with a revised classification of venous
drainage. Radiology 1995 Mar;194(3):671-80. DOI:
http://dx.doi.org/10.1148/radiology.194.3.7862961.
2. Gandhi D, Chen J, Pearl M, Huang J, Gemmete JJ,
Kathuria S. Intracranial dural arteriovenous fistulas:
classification, imaging findings, and treatment. AJNR
Am J Neuroradiol 2012 Jun;33(6):1007-13. DOI:
http://dx.doi.org/10.3174/ajnr.A2798.
3. Oh JT, Chung SY, Lanzino G, et al. Treatment of
intracranial dural arteriovenous fistulas: clinical
characteristics and management based on location
and hemodynamics. J Cerebrovasc Endovasc
Neurosurg 2012 Sep;14(3):192-202. DOI:
http://dx.doi.org/10.7461/jcen.2012.14.3.192.
4. Vilela P, Goulão A. [Primary dural intracranial
arteriovenous lesions]. [Article in Portuguese].
Acta Med Port 2003 May-Jun;16(3):171-8.
The Permanente Journal/Perm J 2016 Summer;20(3):15-218
CLINICAL MEDICINE
Image Diagnosis: Pott Puffy Tumor
Diane Apostolakos, MD, MS; Ian Tang, MD
Perm J 2016 Summer;20(3):15-157
E-pub: 06/24/2016 CASE REPORT
A 20-year-old man was admitted to
our hospital with complaints of frontal
headache, sinusitis, and fever for one week.
He had a history of allergic rhinitis and
recurrent sinus infections. At admission his
temperature was 40˚C and his pulse rate
was 140 beats per minute. On physical examination, the center of his forehead had a
soft, tender, warm, swollen area that caused
an obvious bulge. The initial imaging
study, a computed tomography scan, failed
to clearly show the intracranial pathology.
A magnetic resonance imaging study of the
patient’s head with intravenous contrast
revealed osteomyelitis of the frontal bone
with localized swelling and underlying
epidural empyema (Figures 1 and 2). This
finding confirmed the diagnosis of Pott
puffy tumor, which is defined as forehead
swelling, usually from the anterior extension of frontal sinusitis, and associated
osteomyelitis of the frontal bone.1,2
The patient was seen by otorhinolaryngology as well as neurosurgery; he declined
the recommended surgery and consequently remained febrile with a maximum
temperature of over 38˚C for 6 consecutive
days. He continued to have occasional fever
spikes and was not discharged until hospital
Figure 1. Sagittal-view magnetic resonance image
of the cranium with intravenous contrast. The black
arrows indicate epidural empyema. The white arrow
indicates localized swelling.
http://dx.doi.org/10.7812/TPP/15-157
day 39. During hospitalization he was treated
with intravenous ampicillin and sulbactam
every 6 hours. At discharge, his treatment
was changed to oral metronidazole and
daily intravenous ceftriaxone via a central
catheter. He received a total of 3 months of
antibiotic treatment and remained well after
the antibiotic treatment was completed.
DISCUSSION
Sir Percivall Pott (1714-1788), a surgeon at St Bartholomew’s Hospital in
London, first described Pott puffy tumor
in 1760.3 It was called a tumor because
tumor refers to one of the four historic
manifestations of inflammation noted by
Aulus Cornelius Celsus (c 25 BC-c 50
AD): rubor (redness), tumor (swelling),
calor (warmth), and dolor (pain). Originally described as a complication of head
trauma, Pott puffy tumor typically occurs
as a complication of frontal sinusitis. The
extracranial manifestations frequently include subperiosteal or subgaleal abscesses.
Intracranial complications may include
epidural empyema, subdural empyema,
intraparenchymal abscess, cavernous sinus
thrombosis, or meningitis.4
A review of 53 cases of Pott puffy tumor5
indicated that sinusitis, head trauma, or
Figure 2. Axial-view magnetic resonance image of
the cranium with intravenous contrast. The black
arrows indicate epidural empyema. The white arrow
indicates localized swelling.
cranial surgery are the usual predisposing
factors; the majority of cases occurred in
younger males. Culture results indicated
the frequent pathogens were Streptococcus
species (47%), anaerobic species (28%),
and Staphylococcus aureus (22%). Almost
half of the cultures revealed mixed infections with more than one isolate. Epidural
and subdural empyema were the most
frequently reported intracranial complications.5
Pott puffy tumor is treated with surgery and antibiotics. Surgical treatment
includes drainage of the frontal sinus and
other areas of infection. Broad-spectrum
antibiotics that have good central nervous
system penetration must be started on
diagnosis. Prolonged antibiotic treatment
is required after surgery because osteomyelitis is usually present. v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
How to Cite this Article
Apostolakos D, Tang I. Image diagnosis: Pott puffy
tumor. Perm J 2016 Summer;20(3):15-157. DOI:
http://dx.doi.org/10.7812/TPP/15-157.
References
1. Bambakidis NC, Cohen AR. Intracranial
complications of frontal sinusitis in children:
Pott’s puffy tumor revisited. Pediatr
Neurosurg 2001;35(2):82-9. DOI: http://dx.doi.
org/10.1159/000050395.
2. Koch SE, Wintroub BU. Pott’s puffy tumor. A clinical
marker for osteomyelitis of the skull. Arch Dermatol
1985;121(4):548-9. DOI: http://dx.doi.org/10.1001/
archderm.1985.01660040132029.
3. Pott P. Observations on the nature and
consequences of wounds and contusions of the
head, fractures of the skull, concussions of the brain,
&c. London, England: Hitch & Hawes; 1760. p 22-58.
4. Wells RG, Sty JR, Landers AD. Radiological
evaluation of Pott puffy tumor. JAMA 1986 Mar
14;255(10):1331-3. DOI: http://dx.doi.org/10.1001/
jama.1986.03370100125030.
5. Skomro R, McClean KL. Frontal osteomyelitis
(Pott’s puffy tumour) associated with Pasteurella
multocida—a case report and review of the literature.
Can J Infect Dis 1998 Mar;9(2):115-21.
Diane Apostolakos, MD, MS, is a Hospitalist at the North Sacramento Medical
Center in CA. E-mail: [email protected]. Ian Tang, MD, is a Physician at
Apicha Community Health Center in New York, NY. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-157
1
CLINICAL MEDICINE
Image Diagnosis: Tubo-ovarian Abscess with Hydrosalpinx
Kiersten L Carter, MD; Gus M Garmel, MD, FACEP, FAAEM
Perm J 2016 Fall;20(4):15-211
E-pub: 06/24/2016 Tubo-ovarian abscess (TOA) and hydrosalpinx are complications, though uncommon, of pelvic inflammatory disease (PID).
Both TOA and hydrosalpinx can lead to significant morbidity and, rarely, mortality, and
both necessitate treatment to reduce shortand long-term complications. Risk factors of
TOA include younger age, multiple sexual
partners, nonuse of barrier contraception,
and a history of PID.1 The clinical manifestations of TOA are similar to PID—lower
abdominal pain, fever, chills, and vaginal
discharge, with the addition of pelvic mass
noted on examination or imaging. Women
with TOA present with fever and chills
(50%), nausea (26%), vaginal discharge
(28%), abnormal vaginal bleeding (21%),
and acute lower abdominal pain (89%).2
Women with a presentation consistent
with TOA should be evaluated with a complete history; pelvic examination; laboratory
testing for complete blood count, erythrocyte sedimentation rate, and C-reactive
protein; cervical testing for gonorrhea and
chlamydia; and pregnancy testing to guide
antimicrobial therapy.3 In severe cases, TOA
can rupture and leak, causing sepsis. This
increases mortality and requires emergent
surgical intervention.
http://dx.doi.org/10.7812/TPP/15-211
The most useful diagnostic imaging
studies include transvaginal ultrasonography and computed tomography. Compared with ultrasonography, computed
tomography has increased sensitivity to
detect thick-walled, rim-enhancing adnexal
masses, pyosalpinx, and mesenteric stranding, as well as changes suggestive of ruptured
TOA.1 On computed tomography scan with
contrast, a hydrosalpinx is visualized as a
dilated, fluid-filled fallopian tube without
rim enhancement (Figures 1 and 2).
Although TOA is a complication of PID,
Neisseria gonorrhoeae and Chlamydia trachomatis are infrequently isolated from abscess
fluid. Instead, these organisms weaken
normal host defenses, facilitating invasion
and infection of the upper genital tract by
the lower genital tract flora.1 Treatment for
TOA includes inpatient admission for intravenous antibiotics to target polymicrobial
organisms likely to produce TOA—Escherichia coli, aerobic streptococci, Prevotella,
Bacterioides fragilis, and Peptostreptococcus.3
Cephamycin or cefotetan and doxycycline
or gentamicin and clindamycin are preferred, although local antibiotic resistance
patterns should be considered.4 Transition to oral antibiotics (clindamycin or
metronidazole with doxycycline) can usually be initiated within 24 hours to 48 hours
of clinical improvement to complete the
14-day treatment course.4 The majority of
small abscesses (< 9 cm in diameter) resolve
with antibiotic therapy alone.1
The aim of therapeutic management is
to be as noninvasive as possible. However,
if this approach fails to yield clinical improvement within 3 days, reassessment of
the antibiotic regimen, with consideration
for laparoscopy, laparotomy, adnexectomy,
hysterectomy, or image-guided abscess
drainage is necessary.3,4 Because of its association with shorter hospitalization and
improved pain control, image-guided percutaneous abscess drainage is an attractive
alternative to surgical intervention in the
management of TOA.3 The clinician should
inform, evaluate, test, and treat the patient’s
sexual partners. v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
How to Cite this Article
Carter KL, Garmel GM. Image diagnosis: Tubo-ovarian
abscess with hydrosalpinx. Perm J Fall;20(4):15-211.
DOI: http://dx.doi.org/10.7812/TPP/15-211.
References
Figure 1. Axial-view computed tomography scan of
the abdomen and pelvis. The long arrow indicates
left-sided hydrosalpinx. The short arrow indicates
the associated tubo-ovarian abscess.
Figure 2. Cross-sectional computed tomography
scan of the abdomen and pelvis. The arrow indicates the left-sided tubo-ovarian abscess.
1. Lareau SM, Beigi RH. Pelvic inflammatory disease
and tubo-ovarian abscess. Infect Dis Clin North
Am 2008 Dec;22(4):693-708. DOI: http://dx.doi.
org/10.1016/j.idc.2008.05.008.
2. Landers DV, Sweet RL. Tubo-ovarian abscess:
contemporary approach to management. Review of
Infectious Diseases 1983 Sep;5(5):876-84.
3. Granberg S, Gjelland K, Ekerhovd E. The
management of pelvic abscess. Best Pract Res Clin
Obstet Gynaecol 2009 Oct;23(5):667-78. DOI: http://
dx.doi.org/10.1016/j.bpobgyn.2009.01.010.
4. Workowski KA, Bolan GA; Centers for Disease
Control and Prevention. Sexually transmitted
diseases treatment guideline, 2015. MMWR Recomm
Rep 2015 Jun 5;64(RR-03):78-83. Erratum in:
MMWR Recomm Rep 2015 Aug 28;64(33):924.
Kiersten L Carter, MD, is an Emergency Medicine Resident Physician at the Stanford/Kaiser Emergency
Medicine Residency Program in CA. Gus M Garmel, MD, FACEP, FAAEM, is a Senior Emergency Physician
at the Santa Clara Medical Center, Co-Program Director of the Stanford/Kaiser Emergency Medicine
Residency Program, and Clinical Professor (Affiliate) of Surgery (Emergency Medicine) at Stanford
University in CA. He is also a Senior Editor for The Permanente Journal. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Fall;20(4):15-211
1
CLINICAL MEDICINE
Image Diagnosis:
Gastric Migration of Hookworms in a Patient with Anemia
Chalapathi Rao Achanta, MD
Perm J 2016 Summer;20(3):15-201
E-pub: 06/24/2016 CASE REPORT
http://dx.doi.org/10.7812/TPP/15-201
Ancylostoma duodenale and Necator
americanus are the common species of
hookworm that attach to the small intestinal mucosa. Some 570 million to 740
million people are estimated to be infected
with hookworms worldwide, and infection
rates in India range from 16% to 30% of the
population.1-3 Although the majority of the
infected population remain asymptomatic,
10% of those infected suffer from anemia,4
bringing them to medical attention. Infestation impairs the physical, intellectual, and
nutritional development of children.4
The adult female hookworm releases eggs,
which are passed in stool. Rhabditiform
larvae are released in soil after hatching and
undergo two molts before reaching an infective third-stage filariform larvae. These larvae
can survive for 3 to 4 weeks in contaminated
soil under favorable climate conditions. They
penetrate human skin upon contact and
reach the lungs through the heart via blood
circulation. Once these larvae penetrate the
pulmonary alveoli, they ascend the bronchus
to the pharynx. From there they are swallowed and reach the small intestine, where
they mature to adult worms.
Adult hookworms inhabit the small intestine and ingest intestinal epithelial and
red blood cells, causing iron-deficiency
anemia. On average, daily intestinal blood
loss is estimated to be between 0.01 mL to
0.3 mL depending on the parasite species.5
Very rarely, these worms migrate and reach
the gastric antrum.6,7 According to Thomas
et al, retrograde jejuno-duodenogastric
reflux results in the gastric migration of
the hookworms, especially in cases of high
Figure 1. Upper endoscopy of the distal gastric
antrum, showing hookworms (black arrow) close to
the pylorus (white asterisk).
Figure 2. Upper endoscopy of the duodenum,
showing hookworms attached to the duodenal
mucosa.
A 65-year-old man presented to our
hospital with 4 months of fatigue and
weakness. He denied any bleeding manifestations and had pallor on examination.
Laboratory test results showed hemoglobin
of 8.2 gm/dL with microcytosis and low
iron stores. There was no peripheral eosinophilia. Liver and renal function tests were
normal. Upper endoscopy was ordered for
evaluation of iron deficiency anemia.
The patient’s esophagus was normal, but
there were motile hookworms in the gastric antrum (Figure 1) and heavy loads of
hookworms in the duodenum (Figure 2).
His stool examination showed hookworm
eggs. The patient received 400 mg of
oral albendazole therapy along with iron
therapy. At 3-month follow-up, his anemia
was corrected, and he was symptom free.
DISCUSSION
worm burden.8 Treatment includes either a
single dose of oral albendazole 400 mg or
oral mebendazole 100 mg twice daily for 3
days. Treatment success ranges from 69%
to 92% depending on the regimen used.9
Concomitant iron therapy is necessary to
replace lost iron stores.5 v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
How to Cite this Article
Achanta CR. Image diagnosis: Gastric migration of
hookworms in a patient with anemia. Perm J 2016
Summer;20(3):15-201. DOI: http://dx.doi.org/
10.7812/TPP/15-201.
References
1. Chakma T, Rao PV, Tiwary RS. Prevalence of anaemia
and worm infestation in tribal areas of Madhya
Pradesh. J Indian Med Assoc 2000 Sep;98(9):567-71.
2. Mahajan M, Mathur M, Talwar V, Revathi G. Prevalence
of intestinal parasitic infestation in east Delhi. Indian J
Community Med 1993 Oct-Dec;18(4):177-80.
3. Pal D, Chattopadhyay UK, Sengupta G. A study on
the prevalence of hookworm infection in four districts
of West Bengal and its linkage with anaemia. Indian J
Pathol Microbiol 2007 Apr;50(2):449-52.
4. Haburchak DR, Dhawan VK, Watson CM,
Chandrasekar PH. Hookworm disease: background
[Internet]. New York, NY: WebMD LLC; 2014 May 12
[cited 2016 Jan 21]. Available from: http://emedicine.
medscape.com/article/218805-overview.
5. Feldman M, Friedman LS, Brandt LJ. Sleisenger
and Fordtran’s gastrointestinal and liver disease:
pathophysiology/diagnosis/management. 9th ed.
Philadelphia, PA: Saunders Elsevier; 2010.
6. Dumont A, Seferian V, Barbier P. Endoscopic
discovery and capture of Necator americanus in the
stomach. Endoscopy 1983 Mar;15(2):65-6. DOI:
http://dx.doi.org/10.1055/s-2007-1021467.
7. Boopathy V, Balasubramanian P, Phansalkar M,
Varghese RG. Endoscopic (video) demonstration of
hookworm infestation of the stomach. BMJ Case Rep
2014 May 30;2014. DOI: http://dx.doi.org/10.1136/
bcr-2014-204065.
8. Thomas V, Jose T, Harish K, Kumar S. Hookworm
infestation of antrum of stomach. Indian J
Gastroenterol 2006 May-Jun;25(3):154.
9. Steinmann P, Utzinger J, Du ZW, et al. Efficacy
of single-dose and triple-dose albendazole and
mebendazole against soil-transmitted helminths and
Taenia spp: a randomized controlled trial. PLoS One
2011;6(9):e25003. DOI: http://dx.doi.org/10.1371/
journal.pone.0025003.
Chalapathi Rao Achanta, MD, is a Gastroenterologist at Queen’s NRI
Hospital in Visakhapatnam, India. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-201
1
CLINICAL MEDICINE
Image Diagnosis: Encephalopathy Resulting
from Dural Arteriovenous Fistula
Ana Filipa Santos, MD; Célia Machado, MD; Sara Varanda, MD; João Pinho, MD;
Manuel Ribeiro, MD; Jaime Rocha, MD; Ricardo Maré, MD
E-pub: 07/08/2016 Perm J 2016 Summer;20(3):15-218
http://dx.doi.org/10.7812/TPP/15-218
CASE REPORT
A 69-year-old woman presented to the
Neurology Department with 2 months
of progressive psychomotor slowing, inability to concentrate, and periods of disorientation. Her past medical history was
unremarkable, and she was taking no medication. There was no history of trauma. On
neurologic examination she was alert but
taking a long time to answer, apathetic,
distractable, and hypophonic with right
visual and sensitive hemiextinction and left
hemiparesis. Montreal Cognitive Assessment Exam score was 11/30. A computed
tomography scan of the brain (Figure 1)
showed possible convexity subarachnoid
hemorrhage that the brain magnetic resonange imaging (MRI)/MRI angiography
(Figures 2 and 3) revealed to be engorged
cerebral vessels. Hyperintensity in the deep
white matter of the cerebral hemispheres
was also present. Cerebral angiography
(Figure 4) revealed a dural arteriovenous
fistula (DAVF) of the superior sagittal sinus
and torcula (Cognard classification IIb1).
The patient underwent endovascular
embolization, with combined transarterial
(n-butyl-cyanoacrylate) and transvenous
(coils) approach, resulting in proximal
occlusion of the superior sagital sinus,
torcula, and transverse sinus (Figure 5).
Posttreatment angiography revealed near
complete DAVF occlusion (Figure 6). Control MRI revealed a marked decrease of the
deep white matter hyperintensity and no
engorged cerebral veins (Figures 7 and 8).
The patient’s mental status improved post
procedure (Montreal Cognitive Assessment
Exam score, 20/30), and she progressively
came back to her baseline.
Figure 1. Computed tomography scan of the brain showing possible convexity subarachnoid hemorrhage.
Figure 2. Coronal-view T2-weighted magnetic
resonance image of the brain. The white arrows
indicate engorged cerebral veins visible over the
surfaces of the hemispheres bilaterally.
Figure 3. Axial-view T2-weighted magnetic resonance
image of the brain. The white crosses indicate the
increased signal that is diffusely present within the
deep white matter of the cerebral hemispheres.
Ana Filipa Santos, MD, is a Neurologist at Hospital de Braga in Braga, Portugal. E-mail: [email protected] Célia Machado, MD,
is a Neurologist at Hospital de Braga in Braga, Portugal. E-mail: [email protected]. Sara Varanda, MD, is a Neurologist at
Hospital de Braga in Braga, Portugal. E-mail: [email protected]. João Pinho, MD, is a Neurologist at Hospital de Braga in Braga,
Portugal. E-mail: [email protected]. Manuel Ribeiro, MD, is a Neuroradiologist at Centro Hospitalar de Vila Nova de Gaia-Espinho in
Gaia, Portugal. E-mail: [email protected]. Jaime Rocha, MD, is a Neuroradiologist at Hospital de Braga in Braga, Portugal. E-mail:
[email protected]. Ricardo Maré, MD, is a Neurologist at Hospital de Braga in Braga, Portugal. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-218
1
CLINICAL MEDICINE
Image Diagnosis: Encephalopathy Resulting from Dural Arteriovenous Fistula
Figure 4. Cerebral angiography performed before
endovascular embolization. The black arrowhead
indicates dural arteriovenous fistula of the superior
sagittal sinus. The black asterisk indicates dural
arteriovenous fistula of the torcula.
Figure 5. Cerebral angiography performed after
endovascular embolization. The black arrow
indicates transvenous coils.
DISCUSSION
acuity, seizures, Parkinsonism, cerebellar
symptoms, apathy, and dementia.2-4
DAVFs are abnormal arteriovenous connections within the dura, usually located
within the walls of a dural sinus or an adjacent cortical vein, and account for 10%
to 15% of all intracranial arteriovenous
lesions.2-4 The initiating events which lead
to their development are not clear, but the
literature reports association with trauma,
infection, recent surgery, and dural sinus
thrombosis.2-4 A wide variety of signs and
symptoms, which can vary because of lesion
location and pattern of venous drainage,
may arise from DAVFs, namely, pulsatile
tinnitus, ophthalmoplegia, proptosis, chemosis, retro-orbital pain, decreased visual
CONCLUSION
Our patient with DAVF presented with
encephalopathy with diffuse white matter
changes related to venous ischemia. Her
symptoms partially reverted with endovascular treatment.
DAVF should be considered in patients
with encephalopathy. This relatively nonspecific clinical picture may delay the diagnosis and result in further deterioration. A
high level of suspicion should be maintained
in patients who present in the context of unexplained intracranial hemorrhage without
Figure 6. Posttreatment cerebral angiography
shows near-complete occlusion of the dural
arteriovenous fistula.
significant risk factors (trauma, hypertension, or anticoagulation) or in possible subarachnoid hemorrhage in a nonaneurysmal
pattern. This should prompt imaging with
MRI and angiography, which are the gold
standard for diagnosis. DAVF recognition
is essential because these patients are potentially treatable. v
Disclosure Statement
The authors have no conflicts of interest to
disclose.
How to Cite this Article
Santos AF, Machado C, Varanda S, et al. Image
diagnosis: Encephalopathy resulting from dural
arteriovenous fistula. Perm J 2016 Summer;20(3):
15-218. DOI: http://dx.doi.org/10.7812/TPP/15-218.
References
Figure 7. Posttreatment magnetic resonance image
of the brain showing no engorged cerebral veins.
2
Figure 8. Posttreatment magnetic resonance image
of the brain. The white cross indicates a marked
decrease of the hyperintensity in the deep white
matter of the cerebral hemisphere.
1. Cognard C, Gobin YP, Pierot L, et al. Cerebral dural
arteriovenous fistulas: clinical and angiographic
correlation with a revised classification of venous
drainage. Radiology 1995 Mar;194(3):671-80. DOI:
http://dx.doi.org/10.1148/radiology.194.3.7862961.
2. Gandhi D, Chen J, Pearl M, Huang J, Gemmete JJ,
Kathuria S. Intracranial dural arteriovenous fistulas:
classification, imaging findings, and treatment. AJNR
Am J Neuroradiol 2012 Jun;33(6):1007-13. DOI:
http://dx.doi.org/10.3174/ajnr.A2798.
3. Oh JT, Chung SY, Lanzino G, et al. Treatment of
intracranial dural arteriovenous fistulas: clinical
characteristics and management based on location
and hemodynamics. J Cerebrovasc Endovasc
Neurosurg 2012 Sep;14(3):192-202. DOI:
http://dx.doi.org/10.7461/jcen.2012.14.3.192.
4. Vilela P, Goulão A. [Primary dural intracranial
arteriovenous lesions]. [Article in Portuguese].
Acta Med Port 2003 May-Jun;16(3):171-8.
The Permanente Journal/Perm J 2016 Summer;20(3):15-218
NURSING RESEARCH & PRACTICE
Future Challenges of Robotics and Artificial Intelligence in Nursing:
What Can We Learn from Monsters in Popular Culture?
Henrik Erikson, RNT, PhD; Martin Salzmann-Erikson, RN, MHN, PhD
Perm J 2016 Summer;20(3):15-243
E-pub: 07/15/2016 http://dx.doi.org/10.7812/TPP/15-243
ABSTRACT
It is highly likely that artificial intelligence (AI) will be implemented in nursing robotics
in various forms, both in medical and surgical robotic instruments, but also as different
types of droids and humanoids, physical reinforcements, and also animal/pet robots.
Exploring and discussing AI and robotics in nursing and health care before these tools
become commonplace is of great importance. We propose that monsters in popular
culture might be studied with the hope of learning about situations and relationships
that generate empathic capacities in their monstrous existences. The aim of the article
is to introduce the theoretical framework and assumptions behind this idea. Both robots
and monsters are posthuman creations. The knowledge we present here gives ideas
about how nursing science can address the postmodern, technologic, and global world
to come. Monsters therefore serve as an entrance to explore technologic innovations
such as AI. Analyzing when and why monsters step out of character can provide important insights into the conceptualization of caring and nursing as a science, which is
important for discussing these empathic protocols, as well as more general insight into
human knowledge. The relationship between caring, monsters, robotics, and AI is not
as farfetched as it might seem at first glance.
INTRODUCTION
It is highly likely that artificial intelligence (AI) will be implemented in medical technologic equipment for clinical
monitoring and decision making.1,2 This
change will probably happen rapidly and
on a global scale, because digitalization
and globalization are intensely connected
via the Internet.3,4 For this reason, the
ethics of robotics and AI must be well
developed for these posthuman creations
to make decisions within the frame of
acceptable human ethics and values of
nursing.5 One paradox is the question of
how we can understand and explore these
AIs before we must embrace them as facts
in everyday health care services.6-9
Monsters in popular culture could be
scrutinized with the hope of learning
about situations that generate empathic
capacities.10 If everyone who encounters
a fictional monster—in a book, play,
motion picture, or video game—and
who engages in caring activities reported
their observations, together these observations might show important patterns
relating to empathic abilities in posthuman creations. Cataloging and analyzing
situations in which monster characters
actually become nurturing and caring
can be important for understanding how
humans care as well as for understanding
care in relation to posthuman venues. Are
these situations of protection, sheltering,
or friendship? Questions about empathy
in relation to robotics and AI have been
addressed by researchers. Usually, this relationship is presented from the perspective of humans’ empathy for robots.11,12
However, the dimension we are interested
in is the reverse: the empathic capacities
that robotics and AI can demonstrate for
humans. The knowledge generated will
bring clues as to what the relationship is
between empathy and AI and will contribute to our understanding so that it
will be useful for a future where the impact of digitalization has to be taken into
account in nursing/caring theories. This
is one attempt to capture understanding
about empathic intelligences in virtual
creations, that is, robots, machines, and
cyborgs (empathic protocols). From
this perspective, we ask the question of
whether monsters can help us relate to
AI and to nursing robots.
LINK BETWEEN MONSTERS AND
ARTIFICIAL INTELLIGENCE
Monsters do relate to robotics and sometimes to “evil” machines that combine the
two into one appearance. One example in
popular culture is found in the Terminator film series, in which machines have
reached far beyond the point that is often
referred to as technologic singularity.13,14
Technologic singularity is a critical moment, a point when AI surpasses biological
intelligence. In the Terminator series, the
machines develop, improve, and reproduce
themselves without human involvement,
and their goal is to drive their creators—
the humans—to extinction.
However, in the 1940s, Isaac Asimov15
wrote Runaround, in which he developed
the Laws of Robotics:
1.A robot may not injure a human being,
or through inaction, allow a human being to come to harm
2.A robot must obey the orders given it by
human beings, except where such orders
would conflict with the First Law
3.A robot must protect its own existence as
long as such protection does not conflict
with the First or Second Law 15p44-5
4.(Added later, known as the zeroth law):
No robot may harm humanity or,
through inaction, allow humanity to
come to harm.16
We are entering an era when the vast
digitalization of health care in everyday
life and the fictional Laws of Robotics just
presented are discussed as reality.17 Health
care institutions and the nursing discipline
face paradigmatic changes that are related
to digital technology. For the discipline of
Henrik Erikson, RNT, PhD, is a Professor in Nursing at the Department of Nursing and Care at The
Swedish Red Cross University College in Stockholm, Sweden. E-mail: [email protected].
Martin Salzmann-Erikson, RN, MHN, PhD, is an Associate Professor in Nursing of Health and
Occupational Studies in the Department of Health and Caring Sciences at the University of Gävle
in Sweden. E-mail: [email protected].
The Permanente Journal/Perm J 2016 Summer;20(3):15-243
1
NURSING RESEARCH & PRACTICE
Future Challenges of Robotics and Artificial Intelligence in Nursing: What Can We Learn from Monsters in Popular Culture?
nursing, the relationship to technology and
AI is sparse, so these changes will represent
a giant leap. We argue that it is also highly
relevant and timely for nursing science to
monitor and to debate AI and Robotics
in the same fashion as other areas, such
as medicine.
The International Robot Fair 16 concluded with a World Robot Declaration
proposition that next-generation robots
will 1) be partners that coexist with human beings, 2) assist human beings both
physically and psychologically, and 3)
contribute to the realization of a safe
and peaceful society. Even though robots
equipped with AI in popular culture often
are portrayed as embodied monsters, this
might not be the reality in the near future.
However, and more importantly, AI is
developing rapidly, and several research
projects predict that technologic singularity is no more than 30 years away.18
Today’s robots are starting to be implemented in health care facilities, in forms
such as surgical robots19 and in nursing
homes.20 As posited in the World Robot
Declaration, next-generation robots assist
humans physically. One important aspect
of AI and robotics for nursing is that
nurses might be firsthand partners, working in nursing in institutions with robots
in the near future. Nurses might interact
with household robots in patients’ homes
rather than with the patients themselves.
CHALLENGES OF ROBOTICS AND
ARTIFICIAL INTELLIGENCE IN NURSING
Even if there is a connection between
monsters and robots, one does not ordinarily think of monsters and nursing in
the same framework, nor of robotics and
empathy. The relationship between caring monsters, robotics, and AI is not as
farfetched as it might seem at first glance.
Both robots and monsters are posthuman
creations.21 Just like the robot, monsters
are also connected to cultural and historic
contexts.22 Monsters represent our fears,
and they stand on the threshold of human becoming, always representing “the
other.”23-25 These representations suggest
that monsters ask us how we perceive
the world; they ask us to reevaluate our
cultural assumptions about ethnicity,
gender and sexuality, our perception
of difference, and our tolerance toward
2
expression.26 More generally, monsters ask
us why we created them.26 Maybe for that
reason, popular culture is full of monsters
in TV series, books, and movies.
ourselves and improving our understanding of AI and robotics.
What we can see in our project Caring Monsters34 so far is that monsters are
Monsters represent our fears, and they stand on the threshold
of human becoming, always representing “the other.” These
representations suggest that monsters ask us how we perceive
the world; they ask us to reevaluate our cultural assumptions
about ethnicity, gender and sexuality, our perception of
difference, and our tolerance toward expression
These representations in popular culture have the potential to contribute
to scholarly knowledge in relation to
the challenges we are facing in nursing
because of digitalization. Autonomous
personal robots for private use are entering the general market in 2016.27 Autonomous personal robots will have the
capability to recognize faces, take part
in conversations, adapt to new environments, and make their own decisions on
the basis of their own AI. AI has taken a
giant leap compared with mobile personal
assistants such as Siri (Apple, Cupertino,
CA) and Assistant (Speaktoit Inc, Palo
Alto, CA) or similar tools. Although the
robot may seem impressive and appears
to create safety, the robot is not in itself
particularly intelligent, which is why we
must distinguish between the robot as a
technical tool and its ability to make its
own decisions.28,29 Exploring and elaborating on robots and AI is highly relevant
and timely for nursing research.
IMPLICATIONS FOR NURSING PRACTICE
When various nursing robots become
common practice in institutional settings,
they will have a major impact on nursing
work, the nursing profession, and health
care in general.30,31 Nursing robots will
redefine ideas about nurses in general as
well as ideas about nursing attributes and
conceptual frameworks of comfort and
safety in particular.32,33 Staying abreast
of developments regarding redefinitions
of nursing and its underlying beliefs, values, and assumptions is relevant to also
understanding the implications of AI
and robots in health care. We therefore
state that we can turn to monsters and
their evolutionary existence for preparing
not doomed to uphold their monstrous
characters. They reshape their existence
and meaning over time. A monster as
“the other” is not a fixed position, nor
is the position unchangeable in relation
to humans. For example, our fear of
the power of science, as represented by
Frankenstein’s monster, has shifted over
nearly 200 years from being the epitome
of all monsters to the superhero.35 Our
fear of technology and AI as represented
in the Terminator film-series shows an
evolution from killing machine to conscientious protector.13 Fear of the collapse of a given society, as represented by
zombies in current popular culture, has
shifted in just a few decades from being
the problem to representing the solution
for humanity, as represented in the book
and film “Warm Bodies” and the British
TV series “In the Flesh.”36 The ability to
doubt is visualized and highlighted as
crucial when monsters step out of character in popular culture. The ability to
doubt seems to be a cornerstone when
giving caring attributes to the monsters.
We therefore assume that monsters do
not exist as separate entities in nature;
rather, they are socially constructed in,
for example, colloquial speech in everyday
conversations and manifested throughout
popular culture, where they are narrated
in texts or depicted in movies.
In the future of nursing robotics, questions of empathic protocols should be
explored further. Analyzing when and interpreting why monsters step out of character can provide important insight into
the conceptualization of caring and nursing as a science, insight that is important
for discussing these empathic protocols
and, more generally, human knowledge.20
The Permanente Journal/Perm J 2016 Summer;20(3):15-243
NURSING RESEARCH & PRACTICE
Future Challenges of Robotics and Artificial Intelligence in Nursing: What Can We Learn from Monsters in Popular Culture?
It is important to address the issue that
monsters are creations of storytellers and
writers who have their own ideas and messages about AI and robotics. However, the
storytellers’ motivations are not necessarily the same as the readers’ and viewers’
ideas, nor the larger social interpretations
that the monster itself creates. In other
words, the writers’ and creators’ motivations do not always match with the ideas
their work provokes. We can apply this
logic in the context of AI; the motivation
behind researchers creating AI might not
be the same as the interpretation of the
resulting AI itself. Monsters exist outside
and beyond storytellers’ and writers’ motivations. For this reason, we have chosen
to look at the monsters themselves, not
the creators’ motivations and intentions.
By stating this, we recognize the understanding of reality as the projection of an
ongoing construction and reconstruction
from the points of reference that we experience through life and that doubt and
self-negotiation are vital human values
that also seem to be crucial in the evolutionary history of monsters. v
Disclosure Statement
The author(s) have no conflicts of interest to
disclose.
How to Cite this Article
Erikson H, Salzmann-Erikson M. Future challenges
of robotics and artificial intelligence in nursing:
What can we learn from monsters in popular
culture? Perm J 2016 Summer;20(3):15-243.
DOI: http://dx.doi.org/10.7812/TPP/15-243.
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Feb 27-Mar 3; Genoa, Italy. Heverlee, Belgium:
EURON; 2006 [cited 2015 Sep 16]. Available
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ROBOETHICS%20ROADMAP%20Rel2.1.1.pdf.
17. Iosa M, Morone G, Cherubini A, Paolucci S. The
three laws of neurorobotics: a review on what
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18. Kurzweil R. The singularity is near: when humans
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19. Ashford H, Hunter A, Phung C, Coustasse A. Use
of robots on cardiac surgery [Internet]. Proceedings
of the AABRI International Conference; 2015
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University; 2015 [cited 2015 Oct 19]. Available
from: http://mds.marshall.edu/cgi/viewcontent.
cgi?article=1119&context=mgmt_faculty.
20. Robinson H, MacDonald B, Broadbent E. The role of
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of social robots: the benefits of collaborating
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3
Perm J 2016 Summer;20(3)
Physicians may earn up to 1 AMA PRA Category 1 CreditTM per article for reading and analyzing the designated CME articles published in each edition of TPJ. Each edition has four articles available for review. Other clinicians for whom CME
is acceptable in meeting educational requirements may report up to four hours of participation. The CME evaluation form
may be completed online or via mobile Web at www.tpjcme.org. The Certification of Credit will be e-mailed immediately
upon successful completion. Alternatively, this paper form may be completed and returned via fax or mail to the address
listed below. All Sections must be completed to receive credit. Certification of Credit will be mailed within two months of
receipt of the paper form. Completed forms will be accepted until November 2017.
To earn CME for reading each article designated for AMA PRA Category 1 Credit, you must:
• Score at least 50% in the posttest
• Complete the evaluation and provide your contact information
This form is also available online: www.thepermanentejournal.org
Summer 2016
CME Evaluation Program
Section A.
Article 1. (page 18) A Pharmacist-Staffed, Virtual Gout Management Clinic
for Achieving Target Serum Uric Acid Levels: A Randomized Clinical Trial
Article 3. (page 57) Evidence-Based Workflows for Thyroid and Parathyroid Surgery
What is the recommended goal for urate-lowering therapy in patients with chronic,
recurrent gout?
a. a serum uric acid level < 7.0 mg/dL
b. an allopurinol dose of 300 mg/d
c. a serum uric acid level < 6.8 mg/dL
d. a serum uric acid level < 6.0 mg/dL
When considering the risk stratification of a thyroid nodule by ultrasound, which nodule
should undergo a biopsy?
a. purely cystic or spongiform
b. < 1.5 cm nodule that is not suspicious
c. < 1 cm nodule that is suspicious and no high risk factors
d. > 1 cm nodule that is suspicious or any nodule > 1.5 cm
Which of the following statements is false about urate-lowering therapy in patients with gout?
a. adherence rates to urate-lowering therapy are low compared with many other
chronic conditions
b. physicians often fail to monitor and to appropriately escalate urate-lowering therapy
c. most gout patients are on appropriate urate-lowering therapy
d. flare prophylaxis with colchicine or a nonsteroidal anti-inflammatory drug is appropriate
in the first several months even after achieving the target level with allopurinol or other
urate-lowering treatments
When performing a preoperative voice assessment on a patient undergoing thyroid
or parathyroid surgery, in which of the following situations is documenting the quality
of the voice by using the diagnosis “Voice evaluation, normal” before surgery sufficient?
a. no previous neck surgery
b. previous neck surgery
c. previous chest surgery
d. patient with voice issues
Article 4. (page 107) You Are Not Alone:
Ten Strategies for Surviving a Malpractice Lawsuit
Article 2. (page 51) Improving Care in Older Patients with Diabetes:
A Focus on Glycemic Control
Which of the following statements is true?
a. our response to stress is hardwired and cannot be changed
b. you should never talk to anyone about how the lawsuit is affecting you
c. prescribing some diazepam for yourself is a good way to manage lawsuit-related stress
d. you can increase your resilience by writing down three good things that happen each day
What is the first-line therapy for treatment of glycemic control in older adults
with diabetes (assuming no contraindications to the medication)?
a. glipizide
b. glyburide
c. metformin
d. insulin
e. pioglitazone
Which of the following is a characteristic that does not help a physician manage
the stress of a lawsuit?
a. self-compassion
b. practicing mindfulness
c. being a perfectionist
d. practicing gratitude
What is an appropriate hemoglobin A1c range in a 74-year-old patient on glipizide
and metformin with comorbidities of hypertension and hyperlipidemia?
a. 5.5 to 5.9
b. 6.0 to 6.4
c. 6.5 to 6.9
d. 7.0 to 7.9
Section C.
Section B.
Referring to the CME articles, how likely is it that you will implement this learning to improve your practice within the next 3 months?
Objective 1
Objective 2
Integrate learned
knowledge and
increase competence/
confidence to support
improvement and
change in specific
practices, behaviors,
and performance.
Lead in further developing “PatientCentered Care” activities by acquiring
new skills and methods to overcome
barriers, improve physician/patient
relationships, better identify diagnosis
and treatment of clinical conditions,
as well as, efficiently stratify health
needs of varying patient populations.
Implement changes and
apply updates in services and
practice/policy guidelines,
incorporate systems and
quality improvements, and
effectively utilize evidencebased medicine to produce
better patient outcomes.
Article 1
5 4 3 2 1 0
5 4 3 2 1 0
5 4 3 2 1 0
Article 2
5 4 3 2 1 0
5 4 3 2 1 0
5 4 3 2 1 0
Article 3
5 4 3 2 1 0
5 4 3 2 1 0
5 4 3 2 1 0
Title _____________________________________________
Article 4
5 4 3 2 1 0
5 4 3 2 1 0
5 4 3 2 1 0
E-mail _____________________________________________
Key
5 = highly likely
4 = likely
3 = unsure
2 = unlikely
1 = highly unlikely
0 = I already did this
The Kaiser Permanente National CME Program is accredited by the
Accreditation Council for Continuing Medical Education (ACCME) to provide
continuing medical education for physicians.
The Kaiser Permanente National CME Program designates this journal-based
CME activity for 4 AMA PRA Category 1 Credits™. Physicians should claim
only the credit commensurate with the extent of their participation in the activity.
112
Objective 3
What other changes, if any, do you plan to make in your practice as
a result of reading these articles?
Mail or fax completed form to:
The Permanente Journal
500 NE Multnomah St, Suite 100
Portland, Oregon 97232
Phone: 503-813-3286
Fax: 503-813-2348
______________________________________________________
______________________________________________________
______________________________________________________
Section D. (Please print)
Name _____________________________________________
Physician
Non-Physician Address _____________________________________________
_____________________________________________
Signature _____________________________________________
Date _____________________________________________
The Permanente Journal/Perm J 2016 Summer;20(3)
BOOKS PUBLISHED BY
PERMANENTE AUTHORS:
Summer 2016/ Volume 20 No. 3
PermanenteJournal
The
Sponsored by the National Permanente
Medical Groups
Mission: The Permanente Journal advances
knowledge in scientific research, clinical
medicine, and innovative health care delivery.
Circulation: 25,000 print readers per
quarter, 6900 eTOC readers, and in 2015,
1.4 million page views on TPJ articles
in PubMed from a broad international
readership.
ON THE COVER:
Roman Stonemason
by Tom Janisse, MD, MBA
A Roman stonemason
works to repair the vulnerable corner of a 1000-yearold structure. He stands
sturdy in his fashionably
buckled black boots, blue
jeans with plaster-clouded
knees, and traditional
blue work coat with lapels.
Kneepads wait to support
his delicate work close to the ground, hammering
additional bits of marble, variously sized, to fit all filling
defects. He restores a historic work of masonry 30
generations after its construction and reconstruction,
done just like this in just this way, in a process first
learned during the transition from wood to stone.
Some hours into mixing mud, his dextrous hands with
precision and artistry carefully prep the faces for a final
fresh surface coat, smooth to the touch. When he is
done, the pads, hammer, slab, and bits all fit into his
metal pail, then into his bicycle basket for a ride home
through Roman traffic. He looks back to view with
pleasure and a sure sense of contribution his master
work of art.
Dr Janisse is the Editor-in-Chief of The Permanente
Journal and Publisher of The Permanente Press.
112
CME EVALUATION FORM
The Permanente Journal
500 NE Multnomah St, Suite 100
Portland, Oregon 97232
www.thepermanentejournal.org
ISSN 1552-5767
Follow @PermanenteJ
ORIGINAL RESEARCH
& CONTRIBUTIONS
4 Weight Loss and the Prevention of
Weight Regain: Evaluation of a Treatment Model of Exercise Self-Regulation
Generalizing to Controlled Eating.
James J Annesi, PhD, FAAHB, FTOS,
FAPA; Ping H Johnson, PhD;
Gisèle A Tennant, PhD; Kandice J Porter,
PhD; Kristin L McEwen
For decades behavioral weight-loss treatments have been unsuccessful beyond
the short term. In this study, women with
obesity were randomized into either a
comparison treatment that incorporated
a print manual plus telephone follow-ups
(n = 55) or into an experimental treatment
of The Coach Approach exercise-support
protocol followed after 2 months by group
nutrition sessions focused on generalizing
self-regulatory skills from an exercise
support to a controlled eating context
(n = 55). Improvements in all psychological
measures, physical activity, and fruit and
vegetable intake were significantly greater
in the experimental group. Change in
self-regulation best predicted weight loss,
whereas change in self-efficacy best predicted maintenance of lost weight.
18 A Pharmacist-Staffed, Virtual Gout
Management Clinic for Achieving
Target Serum Uric Acid Levels:
A Randomized Clinical Trial.
Robert Goldfien, MD; Alice Pressman,
PhD, MS; Alice Jacobson, MS; Michele Ng,
PharmD; Andrew Avins, MD, MPH
The authors conducted a parallel-group,
randomized, 26-week, controlled trial of a
pharmacist-staffed, telephone-based program for managing hyperuricemia vs usual
care. Among 37 participants randomized
to the intervention group, 13 (35%) had a
serum uric acid level (sUA) ≤ 6.0 mg/dL at
26 weeks vs 5 of 40 participants (13%) in
the control group (p = 0.03). A structured
pharmacist-staffed program was more effective than usual care for achieving target
sUA levels. These results suggest that
a structured program could significantly
improve gout management.
24 Exploring the Reality of Using Patient
Experience Data to Provide Resident
Feedback: A Qualitative Study of
Attending Physician Perspectives.
Steffanie Campbell, MD; Heather
Honoré Goltz, PhD, LMSW, MEd; Sarah
Njue, MPH; Bich Ngoc Dang, MD
From 7/2013 to 8/2013, in-depth, faceto-face, semistructured interviews were
conducted with 9 attending physicians
who precept residents in internal medicine
at 2 continuity clinics (75% of eligible attendings). Content analysis identified 6
potential barriers in using patient experience survey data: 1) perceived inability
of residents to learn or to incorporate
feedback, 2) punitive nature of feedback,
3) lack of training in the delivery of action-
able feedback, 4) lack of timeliness in the
delivery of feedback, 5) unclear benefit of
patient experience survey data as a tool for
providing resident feedback, and 6) lack of
individualized feedback.
31 Physicians Experiencing Intense
Emotions While Seeing Their Patients:
What Happens? Joana Vilela da Silva,
MD; Irene Carvalho, PhD
A self-report survey was completed by 127
physicians, with 52 (43%) reporting experiencing intense emotions frequently. Coping
strategies to deal with the emotion at the
moment included behavioral and cognitive
approaches. Choking-up/crying, touching, smiling, and providing support were
significantly associated with an immediate
positive impact on the physician-patient
relationship. Withdrawing from the situation, imposing, and defending oneself were
associated with a negative impact.
38 Difference in Effectiveness of
Medication Adherence Intervention
by Health Literacy Level. Ashli A
Owen-Smith, PhD, SM; David H Smith,
PhD, RPh; Cynthia S Rand, PhD; Jeffrey
O Tom, MD, MS; Reesa Laws; Amy
Waterbury, MPH; Andrew Williams,
PhD; William M Vollmer, PhD
Promoting Adherence to Improve Effectiveness of Cardiovascular Disease Therapies
(PATIENT) was a randomized clinical trial
designed to test the impact, compared
with usual care, of two technology-based
interventions that leveraged interactive
voice recognition to promote medication
adherence. The differences in intervention
effects for high vs low health literacy in this
exploratory analysis are consistent with
the hypothesis that individuals with lower
health literacy may derive greater benefit
from this type of intervention compared
with individuals with higher health literacy.
Your Guy’s Guide to Gynecology:
A Reference for Men and Women
Bruce Bekkar, MD; Uda Wahn, MD
ISBN-10: 0965506746
ISBN-13: 978-0965506748
East Sandwich, MA: North Star Publications
(Ant Hill Press); 2000.
Hardcover: 325 pages
$24.95
Picking up the Pieces:
What Everyone Needs to
Know When a Child Dies
Adrienne L Burnell, RN, MS, PhD;
George M Burnell, MD
ISBN-10: 1516859405
ISBN-13: 978-1516859405
createspace.com; 2015
Paperback: 206 pages
$26.45
If you are a Permanente author and would like your book cited here,
send an e-mail to [email protected].
45 Lifestyle and Self-Management by Those
Who Live It: Patients Engaging Patients
in a Chronic Disease Model. Michelle T
Jesse, PhD; Elizabeth Rubinstein; Anne
Eshelman, PhD, ABPP; Corinne Wee;
Mrunalini Tankasala; Jia Li, PhD; Marwan
Abouljoud, MD, CPE, MMM, FACS
Of 1862 patient satisfaction surveys, 823
were returned (44.2%). Patients and their
supports appreciated that the program
volunteer was a transplant recipient and
noted gratitude for the lifestyle information.
Five areas were associated with the success of Transplant Living Community: 1)
a “champion”; 2) a receptive health care
environment; 3) a high level of visibility
to physicians and staff; 4) a lifestyle plan
(“Play Your ACES” [Attitude, Compliance,
Support, and Exercise]), and 5) a strong
volunteer structure. It is feasible to integrate a sustainable patient-led lifestyle and
self-management educational group into
a busy tertiary care clinic for patients with
complex chronic illnesses.
The Permanente Journal/Perm J 2016 Summer:20(3)
For information and/or rates for placing an
announcement here, please contact [email protected].