Download Quality of Care of Patients With Non–Small

Special Report
Quality of Care of Patients With Non–Small-Cell Lung Cancer:
A Report of a Performance Improvement Initiative
Fred R. Hirsch, MD, PhD, Robert M. Jotte, MD, PhD, Carolyn A. Berry, PhD,
William A. Mencia, MD, Stephanie A. Stowell, MPhil, and Allison J. Gardner, PhD
Background: Lung cancer is the leading cause of cancer deaths in the United States. In recent years, significant
advancements have been made in the molecular characterization of tumors, and the availability of new agents
to treat non–small-cell lung cancer has increased. Despite these achievements, optimal care of patients with this
condition remains less than ideal. Although national quality measures and guideline recommendations provide
the necessary framework for patient care, routine self-assessment of adherence to these measures is required for
physician practice improvement. To this end, a performance improvement initiative that met national continuing
medical education standards was designed.
Methods: Focusing on non–small-cell lung cancer patient care, oncologists underwent a three-step process that
included a self-assessment of predetermined performance measures, the development and implementation of
an actionable plan for improvement, and a second round of assessment to measure practice change.
Results: A total of 440 unique patient charts were reviewed by 22 practicing oncologists. Participants demonstrated
high baseline performance levels of established quality measures, such as inclusion of the patient’s pathology report
and assessment of smoking history. Significant gains were observed in the areas of supportive care, including
assessment of the patient’s emotional well-being and the use of molecular markers in diagnostic and treatment
decision making.
Conclusions: Data from this study support the value of performance improvement initiatives to help increase
physician delivery of evidence-based care to patients.
Introduction
Lung cancer is highly prevalent and often fatal. More
than 225,000 new cases are diagnosed each year in the
United States, 85% to 90% of which are non–smallcell lung cancer (NSCLC).1 Lung cancer is the leading
cause of cancer-related mortality, accounting for approximately 28% of cancer-related deaths.1,2 Contributing to the poor prognosis of lung cancer is the fact
that it often goes undetected until it has progressed
to advanced-stage disease.1
In addition to the high prevalence of NSCLC,
contemporary management is becoming increasingly
complex due to the identification of key biomarkers
that influence optimal treatment selection and the development of targeted therapies. Appropriate patient
care also requires the coordination of oncologists,
From the University of Colorado Cancer Center (FRH), Aurora,
CO, Rocky Mountain Cancer Centers (RMJ), Denver, CO, Langone
School of Medicine (CAB) at the New York University, New York,
NY, and Med-IQ (WAM, SAS, AJG), Baltimore, MD.
Submitted May 8, 2012; accepted January 9, 2013.
Address correspondence to Stephanie A. Stowell, MPhil, Med-IQ,
5523 Research Park Drive, Suite 210, Baltimore, MD 21228.
E-mail: [email protected]
This initiative was supported by an unrestricted educational
grant from Lilly USA, LLC. The funding source had no role in the
execution, analysis, or development of the resulting manuscript
associated with this initiative.
90 Cancer Control
pathologists, nurses, and other specialists. Given these
factors, efforts focusing on enhancing quality patient
care are necessary to improve clinical outcomes and
reduce the human and financial toll of lung cancer.
The development and implementation of qualitybased performance measures have the potential to
improve outcomes for patients with cancer. Practicebased education that integrates measures focusing on
specific clinical decisions and processes can provide a
more personalized approach to improving knowledge
when compared with more traditional educational
platforms. Through the use of self-assessments, clinicians are provided a realistic view of their practices,
which allows for more conscientious efforts to align
behavioral and systems-related goals.
Quality improvement in oncology has been a
growing focus of attention over the last 15 years. The
National Cancer Policy Board (NCPB) was established
by the Institute of Medicine and the National Research
Council in an effort to assess the quality of cancer
prevention, control, diagnosis, treatment, and palliation.3 In an ensuing report, the NCPB concluded that
wide disparities exist in the quality of cancer care in
the United States, thereby highlighting the need for
performance measures to improve clinical outcomes.4
The American Society of Clinical Oncology (ASCO)
responded to this call for quality improvement by deJanuary 2014, Vol. 21, No. 1
veloping the National Initiative on Cancer Care Quality (NICCQ) in 2000. In 2002, the Quality Oncology
Practice Initiative (QOPI) was designed as a quality improvement program specifically for ASCO members.5-8
These programs initially focused on two of the most
prevalent cancers in the United States — breast and
colorectal cancers — and established a model for the
comprehensive assessment of community oncologist
practice patterns, which has since been expanded to
address multiple cancer types, including NSCLC.
In addition to these programs, the American Board
of Medical Specialties and the American Medical Association (AMA)–convened Physician Consortium for
Performance Improvement created validated performance measures and developed a nationally standardized continuing medical education (CME) format to
improve patient care.9,10 Specifically, AMA performance
improvement (PI) is a nationally standardized CME
model that allows participants to earn up to 20 AMA
Physician’s Recognition Award category 1 credits™
through the completion of a 3-step process of selfassessment, improvement, and reassessment.
Informed by existing lung cancer performance
measures, current evidence-based NSCLC treatment
guidelines, and previous experience in designing a
PI initiative focused on colorectal cancer care, an Accreditation Council for Continuing Medical Education–accredited provider of CME collaborated with
2 expert lung cancer faculty members to develop
a complementary, first-of-its-kind NSCLC-specific
PI initiative for community oncologists.11 Using the
performance measures as a tool to evaluate practice
patterns, participating oncologists assessed the quality
of patient care delivered at baseline, formulated and
applied a PI strategy specific to the needs of their
practice, and reevaluated the quality of patient care
following this period of improvement to optimize the
implementation of evidence-based practice patterns
and, ultimately, outcomes for patients with NSCLC.
Methods
Process of AMA PI
The NSCLC PI initiative was structured according to
the standardized AMA PI CME model.9 Prior to entering stage A, participants completed a self-assessment
questionnaire addressing current practice processes
and procedures. This was used as a means to prompt
participants to reflect on potential areas of educational
need and facilitate the development of a meaningful
improvement plan. In stage A, participants conducted
a self-assessment based on a set of predetermined
performance measures through a retrospective review of eligible patient charts. These performance
measures focused on key processes of care, such as
diagnostic procedures, staging, supportive care, and
evidence-based treatment decisions. Individuals’ pracJanuary 2014, Vol. 21, No. 1
tice patterns were compared with those of their peers
participating in the initiative and clinical guideline
recommendations, when applicable. The results of
this self-evaluation process served as the basis for the
development of an individualized plan for improving
practice performance in the second step (stage B) of
the initiative.
Participants implemented their individual plans
over a period of active improvement. During this
time, participants accessed a CME-certified publication, which provided a comprehensive review of
evidence-based NSCLC management strategies and
the clinical data supporting these recommendations,
as well as applicable tools designed to aid in PI (eg, a
staging checklist, a patient distress thermometer and
checklist, an algorithm for the first-line treatment of
advanced NSCLC). At the end of the active period of
improvement, participants entered the final step of the
initiative (stage C), in which they conducted a second
round of self-evaluation using unique charts from
patients whose disease had been diagnosed during
each participant’s period of active improvement. Each
participant’s performance in stage C was subsequently
compared with his or her own baseline performance
in stage A, the performance of their peers in stage C,
and national standards, as applicable.
Performance Measure Selection
Performance measures for this PI initiative were developed based on the NSCLC-specific measures included in the ASCO QOPI program, as well as national
evidence-based guideline recommendations for quality
patient care in NSCLC, and reflected best practices for
the management of all stages of NSCLC at the time of
initiative planning (November 2009; Table 1).12-22 The
majority of the performance measures were worded
such that responses could be coded in simple terms of
“yes,” “no,” or “N/A” (not applicable) and were assessed
for ease of abstraction from medical oncology records.
Medical Record Selection
Each participant was asked to submit information
from the charts of 10 patients with a primary diagnosis of NSCLC in stages A and C, for a total of 20
charts. Patients who had been diagnosed with NSCLC
within 1 year of the last office visit were eligible,
and patients with any stage small-cell lung cancer or
non-primary lung tumors were excluded. Participants
were instructed to review different patient charts in
stage A and stage C; therefore, data were considered
to be unlinked.
Confidentiality and Exemption From Consent
Institutional review board approval was not sought
for this initiative. According to the US Department of
Health and Human Services, research is exempt from
Cancer Control 91
institutional review board evaluation if the research
involves the collection or study of existing data, documents, and records and “if the information is recorded
by the investigator in such a manner that the subjects
cannot be identified directly, or through identifiers
linked to the subjects.”23 To ensure compliance with
these requirements, patient data were collected in a
de-identified format.
Table 1. — Evidence-Based Performance Measures
Statistical Analysis
Analyses were conducted at the patient chart level.
Responses to individual questions that were marked
as “N/A” or unanswered were omitted from the analysis. Pearson’s chi-square tests were used to compare
individual performance measures between stage A
and stage C unless otherwise noted. When statistically
appropriate, Wilcoxon rank-sum and Fisher 2-tailed
exact tests of significance were used. Results were
considered statistically significant if the resulting
probability value was less than .05.
Evaluation and Staging
Imaging techniques ordered for clinical staging of patient with
suspected lung cancer
Head CT or MRI brain imaging performed for patients with
stage III or IV disease
Copy of surgical pathology report included in patient’s chart
Number of lymph nodes resected for patients with stage I, II,
or IIIA disease who underwent surgery
Referral for surgical evaluation documented for patients with
stage I, II, or IIIA disease who did not undergo surgery
Core biopsy or bronchoscopy performed if surgery was
not performed
Histological confirmation of isolated metastatic disease
documented for appropriate patients
Proper stage assigned per the 7th edition of the IASLC TNM
Classification of Malignant Tumors based on pathology results
Further tumor characterization sought for specimens
designated “NSCLC NOS”
Performance status assessed and documented at the time
of diagnosis
Performance status assessed and documented at the last
office visit
Surveillance and Supportive Care
Follow-up chest CT scan performed within 6 months after surgery
for patients with nonmetastatic disease who underwent surgical
resection
Smoking history established and documented
Current smoking status documented at the last office visit
Smoking cessation counseling recommended and documented
for active smokers
Cancer-related distress (ie, psychological, social, spiritual)
documented
Treatment
Adjuvant chemotherapy recommended for patients with
stage IA disease (overuse measure)
Adjuvant chemotherapy recommended for patients with
stage IB disease
Adjuvant chemotherapy recommended for patients with
resectable stage II or III disease
Reason documented if a patient with resectable stage II or III disease received adjuvant chemotherapy that was not cisplatin-based
Nonsquamous cell histology documented for patients with
unresectable stage III or IV disease who received bevacizumab
or pemetrexed
EGFR and/or KRAS mutation testing performed prior to
treatment for patients with advanced adenocarcinoma who
received an EGFR TKI
Concurrent chemoradiation recommended for patients with
unresectable stage III disease and good performance status
Immediate course of maintenance treatment recommended for
patients with advanced NSCLC who were in remission or had
stable disease after completion of first-line therapy
Data were derived from references 12-22. CT = computed tomography, EGFR = epidermal growth factor receptor, IASLC = International
Association for the Study of Lung Cancer, MRI = magnetic resonance
imaging, NOS = not otherwise specified, NSCLC = non–small-cell lung
cancer, TKI = tyrosine kinase inhibitor, TNM = tumor, node, metastasis.
92 Cancer Control
Results
Participant Demographics
A total of 22 physicians completed the PI initiative
between January 2010 and August 2011. Demographic
information for this group is presented in Table 2.
Forty-one percent of participants reported practicing
in a group setting, and nearly one-quarter reported
practicing in a community-based oncology center.
Most physicians had been practicing between 6 and
10 years. The average number of patients with NSCLC
who were reported to be seen each month by participants was 25 (range, 2–75), approximately 5 of
whom were presenting for a first visit (range, 1–25).
Patient Demographics
A total of 440 patient charts were submitted by PI
participants: 220 in stage A and 220 in stage C. Most of
Table 2. — Participant Demographics (N = 22)
Practice Type
Academic medical center
Community-based oncology center
Community-based hospital
Group practice
Solo practice
Other
14%
23%
14%
41%
5%
5%
Years in Practice
<1
1–5
6–10
11–20
> 20
0%
14%
36%
27%
23%
Average number of patients with NSCLC (per month)
25
Average number of first-visit patients with NSCLC
(per month)
5
NSCLC = non–small-cell lung cancer.
Because of rounding, percentages do not total 100.
January 2014, Vol. 21, No. 1
Table 3. — Patient Cancer Staging According to
Participant Performance Improvement Stage
Performance Improvement
Cancer Stage
Stage A
n (%)a
Stage C
n (%)
I
45 (20)
49 (22)
II
23 (10)
43 (20)
III
67 (30)
50 (23)
IV
85 (39)
78 (35)
a
Because of rounding, percentage does not total 100.
the patients with NSCLC whose charts were reviewed
as part of this initiative were classified as having stage
III or IV disease (Table 3).
smoking history was nearly universally established
for all patients upon diagnosis, rates of performing
routine reassessment of current smoking status and
incorporating recommendations for smoking cessation counseling were less than ideal in stage A. After
completing the PI process, the percentage of participants who documented a patient’s current smoking
status increased from 89% to 99% (P < .001), and the
percentage of those who referred current smokers
to cessation counseling increased from 86% to 98%
(P = .001; Fig 2). Participants assessed emotional wellbeing and cancer-related distress in 90% of their
patients in stage C, representing a 30% increase over
baseline from stage A (P < .001).
With regard to evidence-based treatment measures,
notable changes in clinician performance were observed (Fig 3). The documentation of nonsquamous
histology in the charts of patients with unresectable
stage III or IV disease who were treated with bevacizumab or pemetrexed significantly increased from 83%
to 99% upon completion of the activity (P = .002). EGFR
mutation testing was also more likely to be performed
on patients with advanced adenocarcinoma prior to
treatment with an epidermal growth factor receptor
(EGFR) tyrosine kinase inhibitor (48% in stage A to 88%
in stage C; P < .001). A total of 88% of patients who
had advanced NSCLC and stable disease immediately
following the completion of first-line therapy were offered maintenance therapy in stage C, an increase of
19% from the stage A baseline level (P = .007).
No. of Patients (%)
Performance Gains
Several significant improvements were observed in
the staging and characterization of NSCLC at the conclusion of the activity. Participants were more likely
to use chest radiography in addition to computed
tomography scans of the chest and 18F-fluorodeoxyglucose–positron emission tomography scans to aid
in the clinical staging of patients with suspected
lung cancer (50% to 74% from stage A to stage C,
respectively; P < .001). Although surgical pathology
reports, including proper stage assignment according
to the seventh edition of the International Association
for the Study of Lung Cancer (IASLC) Tumor Node
Metastasis (TNM) Classification
of Malignant Tumors, were inStage A
Stage C
cluded with 100% of the patient
charts in both stages A and C
100
(data not shown), the proportion of participants who sought
90
further characterization of tumors designated to be NSCLC
not otherwise specified (“NOS”)
80
increased from 78% in stage A to
92% in stage C (P = .028; Fig 1).
70
In addition, multiple aspects
of patient evaluation improved
over the course of the PI process
60
(Fig 1). Despite a high baseline
level in the assessment of per50
formance status at the time of
diagnosis and at the last office
40
visit, significant improvement
Chest
Further
PS at
PS at
was observed in stage C for
Radiography
Characterization
Diagnosis
Last Visit
both measures (performance
of NOS
status at diagnosis: 96% in stage
n = 220 n = 220
n = 64 n = 63
n = 220 n = 220 n = 187 n = 188
A to 99% in stage C, P = .033;
performance status at the last Fig 1. — Participant performance gains from stages A to C. Chest radiograph order for clinical staging,
P < .001. Further characterization of NSCLC tumors designated “not otherwise stated” (NOS), P = .028.
visit: 80% in stage A to 100% Performance status (PS) assessed at the time of diagnosis, P = .033. PS assessed at the last office visit of
in stage C, P < .001). Although patients with at least 1 office visit, P < .001.
January 2014, Vol. 21, No. 1
Cancer Control 93
Discussion
initial self-evaluation and engagement in a period
of planned improvement, participant data revealed
a significant improvement in the incorporation of
histological and genetic features into management
decisions for appropriate patients.
Research published in the
last 7 years has illustrated the
Stage A
Stage C
key role of histology in deter100
mining optimal treatment courses for advanced NSCLC. Recent
evidence suggests that histologi90
cal subtype is related to median
survival, drug toxicities, and the
potential for specific genetic
80
abnormalities.24-26 For instance,
patients with squamous cell car70
cinoma have an increased risk
of bleeding and are more likely
to experience life-threatening
60
or fatal hemoptysis if treated
with bevacizumab, and clinical
50
evidence fails to demonstrate a
significant therapeutic benefit
with pemetrexed in this subset
40
of NSCLC patients.27,28 FurtherEmotional
Current
Smoking
Smoking
Well-Being
History
Smoking Status
Cessation
more, neither agent is approved
n = 220 n = 220 n = 220 n = 220 n = 134 n = 151 n = 110 n = 108
by the US Food and Drug Administration (FDA) for use in
Fig 2. — Participant performance gains from stages A to C. Assessment of emotional well-being, P < .001;
patients with this histological
smoking history, P = 1.000; current smoking status of active smokers, P < .001; smoking cessation counseling recommended to active smokers, P = .001.
subtype. However, patients
with nonsquamous pathology
who receive these therapies
are more likely to respond to
Stage A
Stage C
treatment and avoid potentially
100
fatal adverse events. Therefore,
accurate tumor subtyping and
90
effective communication between oncologists and pathologists are essential components
80
of high-quality care of patients
with NSCLC.21,22,29
70
At the completion of this
activity, oncologists more proactively pursued “NOS” pathology
60
designations to discern more specific tumor characteristics; since
50
accurate tumor subtyping can
guide therapeutic decisions and
prevent inappropriate treatment
40
choices for this patient populaMaintenance
Nonsquamous
EGFR
Therapy
Histology
Mutation Testing
tion, this improvement may have
n = 74 n = 66
n = 220 n = 220
n = 46 n = 33
a clinically relevant impact. In
addition, the appropriate use of
Fig 3. — Participant performance gains from stages A to C. Nonsquamous cell histology documented for
proven treatment regimens in
patients with resectable stage III or IV disease who received bevacizumab or pemetrexed, P =.002; EGFR
patients with unresectable stage
and/or mutation testing performed prior to treatment, P < .001; maintenance therapy recommended for
patients with advanced NSCLC in remission or with stable disease after first-line therapy, P = .007.
III or stage IV disease with docuNo. of Patients (%)
No. of Patients (%)
This NSCLC-focused PI initiative demonstrated that
oncologists can improve clinical skills relevant to the
evaluation, staging, supportive care, and evidencebased treatment of patients with NSCLC. After an
94 Cancer Control
January 2014, Vol. 21, No. 1
mented nonsquamous cell histology increased among
physicians participating in this initiative.
Clinical advancements surrounding key molecular
biomarkers and the development of targeted therapies are also of particular importance to the management of NSCLC because it is estimated that more than
one-half of these tumors have an identifiable mutation.30 Data from several trials, including the IRESSA
Pan-Asia Study, First-SIGNAL, OPTIMAL, EURTAC,
and those from the North-East Japan and West Japan
Study Groups, demonstrate that newly diagnosed patients with advanced-stage NSCLC and a known EGFRactivating tyrosine kinase domain mutation may benefit from first-line targeted chemotherapy.31-36 Prompted
by clinical evidence that supports the importance of
determining EGFR mutation status on optimal treatment decisions, the FDA formally approved erlotinib
for the first-line treatment of patients with metastatic
NSCLC and exon 19 deletions or exon 21 L858R substitution mutations in the EGFR gene as determined
by a companion diagnostic test in May 2013.37 In addition, ASCO and the National Comprehensive Cancer
Network (NCCN) updated their NSCLC clinical practice guidelines to formally incorporate into treatment
recommendations this new indication as well as data
from studies examining novel targeted agents directed
against tumors harboring anaplastic lymphoma kinase
(ALK) gene rearrangements.29,34,38-40 The PI initiative
was developed before the ALK-specific inhibitor became available outside of a clinical trial, so evaluation
of the ALK gene rearrangement was not included as a
performance measure in this activity. However, EGFR
mutation testing for appropriate patients increased
by 40% from baseline level; because mutation testing
results are poised to guide the selection of individualized treatment strategies that have the maximal impact
on disease progression and patient survival rates, this
40% improvement is of clinical significance.
Another noted change regarding evidenced-based
treatment performance among PI participants was the
increase in the recommendation of maintenance therapy for patients with advanced disease. Maintenance
therapy is a relatively new concept in NSCLC, and it
has been a subject of intensive clinical investigation
and controversy over the last decade. When the PI activity was launched in January 2010, only pemetrexed
and bevacizumab (if initially given with chemotherapy)
were recommended by guidelines from the NCCN for
maintenance therapy in patients with tumor response or
stable disease after first-line therapy.14 However, based
on the results of multiple large-scale trials with various
maintenance protocols that have illustrated significant
improvements in progression-free survival, and overall survival rates to a lesser extent, guidelines from
both ASCO and the NCCN expanded treatment options
and added additional agents in this setting, includJanuary 2014, Vol. 21, No. 1
ing erlotinib, cetuximab, and gemcitabine.22,24,29,37,41-43
This approach exemplifies a shift in care for patients
with cancer. Although evidence is still accumulating
regarding the exact benefits and limitations of maintenance therapy, more oncologists are considering this
therapeutic strategy for select patient populations.
In the area of supportive care, physician participants were 30% more likely to assess cancer-related
distress in patients during stage C of the PI activity.
Increasingly, emotional well-being is recognized as an
essential component of care for patients with cancer.44
Evidence suggests that up to 40% of patients with
cancer experience significant distress associated with
their disease; however, estimates of the proportion of
these patients who receive or are referred to counseling or psychological treatment are low, ranging from
10% to 50%.44-46 The need for recognition of psychological distress is of particular importance to busy,
community-based oncology practitioners, for whom
psychosocial resources may be limited.44
To address suboptimal identification and management of emotional and psychological distress among
patients in oncology clinics, the Commission on Cancer introduced a new performance standard requiring
psychosocial distress screening to be performed at
pivotal time points, such as diagnosis and treatment
transitions, and will require physicians to document
provision of psychosocial care and follow-up of identified individuals.47 As more standards concerning patient emotional well-being are adopted, oncologists
will need to expand their competencies to include
the varying aspects of psychosocial care.
In addition to increased awareness of psychological distress, physician participants improved the
regular reassessment of their patients’ smoking status and recommendation of cessation counseling to
active smokers. Evidence suggests that up to 83%
of patients who are current smokers at the time of
diagnosis continue to smoke.48 Smoking not only
increases the risk of metachronous tumors, reduces
treatment efficacy, and increases treatment toxicity,
but also nearly doubles the risk of death in patients
who continue to smoke after a diagnosis of earlystage lung cancer.49,50 Furthermore, the risk of death
from other smoking-related conditions, such as coronary heart disease and chronic obstructive pulmonary
disorder, is also a significant concern for patients with
potentially curable disease.18,51
Although the routine assessment of patient performance status at each office visit was relatively high at
baseline among participating physicians, the observed
improvement in the execution of this measure was
significant. Evaluating performance status at every
visit is crucial for monitoring the impact of disease,
revising treatment plans when necessary, and managing overall patient health.
Cancer Control 95
There are several limitations of this PI study. First,
the study is limited by small sample sizes. A larger
number of participants and a richer pool of patient
chart data would likely provide a clearer picture of
the impact of PI in NSCLC patient care. Second, no
restrictions on disease stage were present, which further limited the sampling of questions surrounding
evidence-based treatment. Third, optimal patient care
is an individualized and complex process that cannot
necessarily be accurately captured through the generalities of performance measures. Additional limitations
were typical of those associated with other reported
PI activities.11,52-54 The integrity of the data was reliant
on the participants and may have been affected by
biases with patient chart selection, self-reporting of
performance measures, and the inability to differentiate between improvements in charting and execution
of care processes. However, the objective of PI CME
is to catalyze change in physician behavior; therefore,
participant biases would be self-defeating in nature.
PI CME is a method to promote positive changes
in physician behavior. Although the educational materials that supported the activity were important to
enhance participant knowledge, the opportunity for
individual performance change and commitment to
that change are the keys to its success. Participants
reviewed how evidence-based standards were employed in their practices and developed personalized
strategies to attain patient care goals. In turn, this may
also have increased the likelihood for changes to be
adopted over the long term.
Conclusions
After completing this initiative focused on patient care
for those with non–small-cell lung cancer, participants
demonstrated significant gains in applying knowledge
from recent scientific advancements in tumor characterization based on histological and genetic features
to appropriately classify and treat their patients. Furthermore, notable gains were made in the area of
supportive care through the improved assessment
of current smoking status and emotional well-being,
as well as referral to smoking cessation counseling,
which has traditionally been outside the role of the
practicing oncologist. With regard to both areas of
improvement, these changes are important, fundamental steps toward providing improved comprehensive patient care that more appropriately addresses
the physical disease as well as its psychological and
lifestyle implications.
Appreciation is expressed to Whitney Stevens Dollar for
project management and Beth Wills for participant recruitment. They also thank Rebecca Julian, Sara Miller, and
Rachel Karcher for editorial assistance, Kenny Khoo for data
management, Amy Sison for outcomes management, and
Liza King for data analysis.
96 Cancer Control
References
1. American Cancer Society. Lung cancer (non-small cell). http://www.
cancer.org/Cancer/LungCancer-Non-SmallCell/DetailedGuide/non-smallcell-lung-cancer-key-statistics. Accessed July 15, 2013.
2. US Cancer Statistics Working Group. United States Cancer Statistics: 1999–2007 Incidence and Mortality Web-based Report. Atlanta, GA:
Department of Health and Human Services, Centers for Disease Control and
Prevention, and National Cancer Institute; 2010. http://www.cdc.gov/uscs. Accessed July 15, 2013.
3. Hewitt M, Simone JV. Ensuring Quality Cancer Care. Washington,
DC: National Academy Press; 1999. http://www.nap.edu/catalog.php?record_
id=6467. Accessed July 15, 2013.
4. Institute of Medicine. National Cancer Policy Board. http://www.iom.
edu/About-IOM/Leadership-Staff/Boards/National-Cancer-Policy-Board.
aspx. Accessed August 20, 2013.
5. Malin JL, Schneider EC, Epstein AM, et al. Results of the National
Initiative for Cancer Care Quality: how can we improve the quality of cancer
care in the United States? J Clin Oncol. 2006;24(4):626-634.
6. Schneider EC, Malin JL, Kahn KL, et al. Developing a system to assess the quality of cancer care: ASCO’s national initiative on cancer care
quality. J Clin Oncol. 2004;22(15):2985-2991.
7. Neuss MN, Desch CE, McNiff KK, et al. A process for measuring the
quality of cancer care: the Quality Oncology Practice Initiative. J Clin Oncol.
2005;23(25):6233-6239.
8. Simone JV. Origins of the quality oncology practice initiative. J Oncol
Pract. 2009;5(6):269-720.
9. American Medical Association. Physician Consortium for Performance
Improvement. http://www.ama-assn.org/ama/pub/physician-resources/physicianconsortium-performance-improvement.page. Accessed July 13, 2013.
10. American Board of Medical Specialties. Maintenance of certification.
http://www.abms.org/Maintenance_of_Certification/ABMS_MOC.aspx. Accessed July 15, 2013.
11. Marshall JL, Cartwright TH, Berry CA, et al. Implementation of a
performance improvement initiative in colorectal cancer care. J Oncol Pract.
2012;8(5):309-314.
12. Quality Oncology Practice Initiative. Summary of measures, Fall
2009. http://qopi.asco.org/Documents/QOPIFall2009MeasuresSummary.pdf.
Accessed August 9, 2013.
13. Rivera MP, Mehta AC, American College of Chest Physicians. Initial
diagnosis of lung cancer: ACCP evidence-based clinical practice guidelines
(2nd ed). Chest. 2007;132(3 suppl):131S-148S.
14. National Comprehensive Cancer Network. NCCN clinical practice
guidelines in oncology: non-small cell lung cancer. v.2.2009.
15. Silvestri GA, Gould MK, Margolis ML, et al; American College of
Chest Physicians. Noninvasive staging of non-small cell lung cancer: ACCP
evidenced based clinical practice guidelines (2nd ed). Chest. 2007;132(3
suppl):178S-201S.
16. Detterbeck FC, Jantz MA, Wallace M, et al, American College of
Chest Physicians. Invasive mediastinal staging of lung cancer: ACCP
evidence-based clinical practice guidelines (2nd ed). Chest. 2007;132(3
suppl):202S-220S.
17. National Comprehensive Cancer Network. NCCN clinical practice
guidelines in oncology: distress management. v.2.2009.
18. US Department of Health and Human Services. Treating tobacco
use and dependence: 2008 update. http://www.surgeongeneral.gov/tobacco/
treating_tobacco_use08.pdf. Accessed July 15, 2013.
19. Scott WJ, Howington J, Feigenberg S, et al; American College of
Chest Physicians. Treatment of non-small cell lung cancer stage I and
stage II: ACCP evidence-based clinical practice guidelines (2nd ed). Chest.
2007;132(3 suppl):234S-242S.
20. Pisters KM, Evans WK, Azzoli CG, et al; Cancer Care Ontario; American Society of Clinical Oncology. Adjuvant chemotherapy and adjuvant radiation therapy for stages II/IIA resectable non small-cell lung cancer guideline.
J Clin Oncol. 2007;25(34):5506-5518.
21. International Association for the Study of Lung Cancer. Staging Manual in Thoracic Oncology. Orange Park, FL: Editorial Rx Press; 2009.
22. Azzoli CG, Baker S Jr, Temin S, et al. American Society of Clinical
Oncology Clinical Practice Guideline update on chemotherapy for stage IV
non-small-cell lung cancer. J Clin Oncol. 2009;27(26):6251-6266.
23. Code of Federal Regulations, Title 45: Public Welfare, Department of Health and Human Services, Part 46: Protection of Human Subjects, Revised January 15, 2009. http://www.hhs.gov/ohrp/humansubjects/
guidance/45cfr46.html. Accessed July 15, 2013.
24. Ciuleanu T, Brodowicz T, Zielinski C, et al. Maintenance pemetrexed
plus best supportive care versus placebo plus best supportive care for nonsmall cell lung cancer: a randomized, double-blind, phase 3 study. Lancet.
2009;374(9699):1432-1440.
25. Sandler A, Gray R, Perry MC, et al. Paclitaxel-carboplatin alone
or with bevacizumab for non-small cell lung cancer. N Engl J Med.
2006;355(4):2542-2550.
26. Scagliotti GV, Parikh P, von Pawel J, et al. Phase III study comparing
cisplatin plus gemcitabine with cisplatin plus pemetrexed in chemotherapyJanuary 2014, Vol. 21, No. 1
naïve patients with advanced-stage non-small cell lung cancer. J Clin Oncol.
2008;26(21):3543-3551.
27. Johnson DH, Fehrenbacher L, Novotny WF, et al. Randomized phase
II trial comparing bevacizumab plus carboplatin and paclitaxel with carboplatin and paclitaxel alone in previously untreated locally advanced or metastatic
non-small-cell lung cancer. J Clin Oncol. 2004;22(11):2184-2191.
28. Joerger M, Omlin A, Cerny T, et al. The role of pemetrexed in advanced non small-cell lung cancer: special focus on pharmacology and
mechanism of action. Curr Drug Targets. 2010;11(1):37-47.
29. National Comprehensive Cancer Network. NCCN clinical practice
guidelines in oncology: non-small cell lung cancer. v.2.2013.
30. Kris MG, Johnson BE, Kwiatkowski DJ, et al. Identification of driver
mutations in tumor specimens from 1,000 patients with lung adenocarcinoma: the NCI’s Lung Cancer Mutation Consortium (LCMC). J Clin Oncol. 2011 ASCO Annual Meeting Proceedings (Post-Meeting Edition).
2011;29:18(June 20 suppl):CRA7506. Abstract.
31. Mok TS, Wu YL, Thongprasert S, et al. Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med. 2009;361(10):947-957.
32. Lee JS, Park K, Kim SW, et al. A randomized phase III study of gefitinib (IRESSA) versus standard chemotherapy (gemcitabine plus cisplatin)
as a first-line treatment for never-smokers with advanced or metastatic adenocarcinoma of the lung. J Thoracic Oncol. 2009;4(suppl 1):S283.
33. Zhou C, Wu YL, Chen G, et al. Erlotinib versus chemotherapy as
first-line treatment for patients with advanced EGFR mutation-positive nonsmall-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label,
randomised, phase 3 study. Lancet Oncol. 2011;12(8):735-742.
34. Rosell R, Carcereny E, Gervais R, et al. Erlotinib versus standard
chemotherapy as first-line treatment for European patients with advanced
EGFR mutation-positive non-small-cell lung cancer (EURTAC): a multicentre,
open-label, randomised phase 3 trial. Lancet Oncol. 2012;13(3):239-246.
35. Maemondo M, Inoue A, Kobayashi K, et al. Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med.
2010;362(25):2380-2388.
36. Mitsudomi T, Morita S, Yatabe Y, et al. Gefitinib versus cisplatin plus
docetaxel in patients with non-small-cell lung cancer harbouring mutations
of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol. 2010;11(2):121-128.
37. US Food and Drug Administration. Erlotinib. http://www.fda.gov/
Drugs/InformationOnDrugs/ApprovedDrugs/ucm352317.htm. Accessed July
26, 2013.
38. Cappuzzo F, Ciuleanu T, Stelmakh L, et al; SATURN Investigators.
Erlotinib as maintenance treatment in advanced non-small-cell lung cancer:
a muticentre, randomized, placebo-controlled phase 3 study. Lancet Oncol.
2010;11(6):521-529.
39. Kwak EL, Bang Y-J, Camidge R, et al. Anaplastic lymphoma kinase
inhibition in non-small-cell lung cancer. N Engl J Med. 2010;363(18):16931703.
40. Keedy VL, Temin S, Somerfield MR, et al. Epidermal growth factor
receptor (EGFR) mutation testing for patients with advanced non-small cell
lung cancer considering first-line EGFR tyrosine kinase inhibitor therapy. J
Clin Oncol. 2011;29(15):2121-2127.
41. Paz-Ares LG, De Marinis F, Dediu M, et al. PARAMOUNT: final overall
survival results of the phase III study of maintenance pemetrexed versus
placebo immediately after induction treatment with pemetrexed plus cisplatin for advanced nonsquamous non-small-cell lung cancer. J Clin Oncol.
2013;31(23):2895-2902.
42. Zhang L, Ma S, Song X, et al. Gefitinib versus placebo as maintenance therapy in patients with locally advanced or metastatic non-small-cell
lung cancer (INFORM; C-TONG 0804): a multicentre, double-blind randomised phase 3 trial. Lancet Oncol. 2012;13(5):466-475.
43. Patel J, Socinski MA, Garon EB, et al. A randomized, open-label, phase
3, superiority study of pemetrexed (Pem)+carboplatin (Cb)+bevacizumab (B)
followed by maintenance Pem+B versus paclitaxel (Pac)+Cb+B followed by
maintenance B in patients (pts) with stage IIIB or IV non-squamous nonsmall cell lung cancer (NS-NSCLC). J Thorac Oncol. 2012;7:LBPL1. Abstract.
44. National Comprehensive Cancer Network. NCCN clinical practice
guidelines in oncology: distress management. v.2.2013.
45. Kadan-Lottick NS, Vanderwerker LC, Block SD, et al. Psychiatric disorders and mental health service use in patients with advanced cancer: a
report from the coping with cancer study. Cancer. 2005;104(12):2872-2881.
46. Jacobsen PB, Shibata D, Siegel EM, et al. Evaluating the quality of
psychosocial care in outpatient medical oncology settings using performance
indicators. Psychooncology. 2011;20(11):1221-1227.
47. Commission on Cancer. Cancer Program Standards 2012: Ensuring
Patient-Centered Care. V1.0. 2012.
48. Cataldo JK, Dubey S, Prochaska JJ. Smoking cessation: an integral
part of lung cancer treatment. Oncology. 2010;78(5-6):289-301.
49. Waller LL, Weaver KE, Petty WJ, et al. Effects of continued tobacco use during treatment of lung cancer. Expert Rev Anticancer Ther.
2010;10(10):1569-1575.
50. Parsons A, Daley A, Begh R, et al. Influence of smoking cessation
after diagnosis of early stage lung cancer on prognosis: systematic review of
observational studies with meta-analysis. BMJ. 2010;340:b5569.
January 2014, Vol. 21, No. 1
51. Rubins J, Unger M, Colice GL; American College of Chest Physicians.
Followup and surveillance of the lung cancer patient following curative intent
therapy: ACCP evidence-based clinical practice guideline (2nd ed). Chest.
2007;132(3 suppl):355S-367S.
52. Cannon CP, Hoekstra JW, Larson DM, et al. Individual quality improvement in acute coronary syndromes: A performance improvement initiative. Crit Pathw Cardiol. 2009;8(1):43-48.
53. Stowell SA, Karcher RB, Bartel RC, et al. Results of a performance
improvement initiative in diabetes care. CE Measure. 2010;4(2):34-39.
54. Sekeres MA, Stowell SA, Berry CA, et al. Improving the diagnosis
and treatment of patients with myelodysplastic syndromes through a performance improvement initiative. Leuk Res. 2013;37(4):422-426.
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