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Published Ahead of Print on November 5, 2012 as 10.1200/JCO.2012.45.9859
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JOURNAL OF CLINICAL ONCOLOGY
A S C O
S P E C I A L
A R T I C L E
Breast Cancer Follow-Up and Management After Primary
Treatment: American Society of Clinical Oncology Clinical
Practice Guideline Update
James L. Khatcheressian, Patricia Hurley, Elissa Bantug, Laura J. Esserman, Eva Grunfeld, Francine Halberg,
Alexander Hantel, N. Lynn Henry, Hyman B. Muss, Thomas J. Smith, Victor G. Vogel, Antonio C. Wolff,
Mark R. Somerfield, and Nancy E. Davidson
Processed as a Rapid Communication manuscript
James L. Khatcheressian, Virginia Cancer
Institute, Richmond; Patricia Hurley and
Mark R. Somerfield, American Society of
Clinical Oncology, Alexandria, VA; Elissa
Bantug, Thomas J. Smith, and Antonio C.
Wolff, Johns Hopkins Medicine and Sidney
Kimmel Comprehensive Cancer Center,
Baltimore, MD; Laura J. Esserman, Carol
Franc Buck Breast Care Center and Helen
Diller Family Comprehensive Cancer
Center, University of California at San Francisco, San Francisco; Francine Halberg,
Marin Cancer Institute, Greenbrae, CA; Eva
Grunfeld, University of Toronto and Ontario
Institute for Cancer Research, Toronto,
Ontario, Canada; Alexander Hantel, Edward
Cancer Centers, Naperville, IL; N. Lynn
Henry, University of Michigan Comprehensive Cancer Center, Ann Arbor, MI; Hyman
B. Muss, Lineberger Comprehensive
Cancer Center, University of North Carolina
at Chapel Hill, Chapel Hill, NC; Victor G.
Vogel, Geisinger Medical Center, Danville;
and Nancy E. Davidson, University of Pittsburgh Cancer Institute and University of
Pittsburgh Medical Center Cancer Center,
Pittsburgh, PA.
Submitted August 7, 2012; accepted
September 24, 2012; published online
ahead of print at www.jco.org on
November 5, 2012.
Copyright © 2012 American Society of
Clinical Oncology. All rights reserved. No
part of this document may be reproduced
or transmitted in any form or by any
means, electronic or mechanical, including
photocopy, recording, or any information
storage and retrieval system, without written permission by the American Society of
Clinical Oncology.
Authors’ disclosures of potential conflicts
of interest and author contributions are
found at the end of this article.
Corresponding author: American Society of
Clinical Oncology, 2318 Mill Rd, Suite 800,
Alexandria, VA 22314; e-mail: guidelines@
asco.org.
© 2012 by American Society of Clinical
Oncology
0732-183X/12/3099-1/$20.00
DOI: 10.1200/JCO.2012.45.9859
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Purpose
To provide recommendations on the follow-up and management of patients with breast cancer
who have completed primary therapy with curative intent.
Methods
To update the 2006 guideline of the American Society of Clinical Oncology (ASCO), a systematic
review of the literature published from March 2006 through March 2012 was completed using
MEDLINE and the Cochrane Collaboration Library. An Update Committee reviewed the evidence
to determine whether the recommendations were in need of updating.
Results
There were 14 new publications that met inclusion criteria: nine systematic reviews (three
included meta-analyses) and five randomized controlled trials. After its review and analysis of the
evidence, the Update Committee concluded that no revisions to the existing ASCO recommendations were warranted.
Recommendations
Regular history, physical examination, and mammography are recommended for breast cancer
follow-up. Physical examinations should be performed every 3 to 6 months for the first 3 years,
every 6 to 12 months for years 4 and 5, and annually thereafter. For women who have undergone
breast-conserving surgery, a post-treatment mammogram should be obtained 1 year after the
initial mammogram and at least 6 months after completion of radiation therapy. Thereafter, unless
otherwise indicated, a yearly mammographic evaluation should be performed. The use of
complete blood counts, chemistry panels, bone scans, chest radiographs, liver ultrasounds, pelvic
ultrasounds, computed tomography scans, [18F]fluorodeoxyglucose–positron emission tomography scans, magnetic resonance imaging, and/or tumor markers (carcinoembryonic antigen, CA
15-3, and CA 27.29) is not recommended for routine follow-up in an otherwise asymptomatic
patient with no specific findings on clinical examination.
J Clin Oncol 30. © 2012 by American Society of Clinical Oncology
INTRODUCTION
In 1997, the American Society of Clinical Oncology
(ASCO) published an evidence-based clinical practice
guideline on breast cancer follow-up and management
in asymptomatic patients after primary, curative therapy.1 ASCO guidelines are updated periodically by a
subset of the original expert panel. The guideline was
updated and published in 19992 and again in 2006.3 In
March 2012, the Update Committee reviewed the
results of a systematic review of the literature to
determine whether the ASCO guideline recommendations needed additional updating.
This clinical practice guideline addresses three
overarching clinical questions: (1) What guidance
around follow-up and management should be available to women who have been previously treated for
breast cancer? (2) What testing is recommended for
the detection of breast cancer recurrence in the adjuvant setting after curative-intent primary therapy?
(3) What is the optimal frequency of monitoring?
Table 1 summarizes the guideline recommendations. A Data Supplement, a patient guide,
and other clinical tools and resources to help clinicians implement this guideline are available at
http://www.asco.org/guidelines/breastfollowup.
© 2012 by American Society of Clinical Oncology
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1
Khatcheressian et al
METHODS
The Update Committee included academic and community practitioners,
medical oncologists, a surgical oncologist, a radiation oncologist, hematologic
oncologists, a gynecologic oncologist, a primary care physician, and a patient
advocate (Appendix Table A1, online only). A Working Group of the Update
Committee completed a review and analysis of evidence published between
March 2006 and March 2012 to determine whether the recommendations
THE BOTTOM LINE
ASCO GUIDELINE UPDATE
Breast Cancer Follow-Up and Management After
Primary Treatment: American Society of Clinical
Oncology Clinical Practice Guideline Update
Intervention
● Modes of surveillance for patients with breast cancer who
have completed primary therapy with curative intent
Target Audience
● Medical oncologists, primary care providers, oncology
nurses, surgical oncologists, pathologists, and nuclear medicine specialists
Key Recommendations
● Regular history, physical examination, and mammography
are recommended
● Examinations should be performed every 3 to 6 months for
the first 3 years, every 6 to 12 months for years 4 and 5, and
annually thereafter
● For women who have undergone breast-conserving surgery,
a post-treatment mammogram should be obtained 1 year
after the initial mammogram and at least 6 months after
completion of radiation therapy; thereafter, unless otherwise
indicated, a yearly mammographic evaluation should be
performed
● Use of CBCs, chemistry panels, bone scans, chest radiographs, liver ultrasounds, computed tomography scans,
[18F]fluorodeoxyglucose–positron emission tomography
scanning, magnetic resonance imaging, or tumor markers
(carcinoembryonic antigen, CA 15-3, and CA 27.29) is not
recommended for routine breast cancer follow-up in an
otherwise asymptomatic patient with no specific findings on
clinical examination
Methods
● A comprehensive systematic review of the literature was
conducted, and an Update Committee was convened to review the evidence and develop guideline recommendations
A Data Supplement (including evidence tables) and clinical tools and
resources can be found at http://www.asco.org/guidelines/
breastfollowup
2
© 2012 by American Society of Clinical Oncology
needed to be updated. The Working Group drafted the guideline update and
circulated it to the full Update Committee for review and approval. The ASCO
Clinical Practice Guidelines Committee leadership reviewed and approved the
final document.
Details of the literature search strategy and the inclusion and exclusion
criteria are provided in the Data Supplement (http://www.asco.org/guidelines/
breastfollowup). In brief, studies were included if their primary objective
was the follow-up and management of patients with breast cancer who had
completed primary therapy with curative intent. The outcomes of interest
were disease-free survival, overall survival, health-related quality of life,
reduced toxicity, and cost effectiveness. The searches were limited to
randomized controlled trials (RCTs), systematic reviews (with or without
meta-analyses), and clinical practice guidelines. However, for the search on
tumor markers, both randomized and nonrandomized studies were eligible if they directly addressed the clinical utility of one or more tumor
markers (ie, carcinoembryonic antigen, CA 15-3, and CA 27.29) by comparing the outcomes of interest for a group of patients monitored with one
or more of the listed tumor markers with a group of patients who were not
monitored with any tumor marker.
Guideline Policy
The practice guideline is not intended to substitute for the independent
professional judgment of the treating physician. Practice guidelines do not
account for individual variation among patients and may not reflect the most
recent evidence. This guideline does not recommend any particular product or
course of medical treatment. Use of the practice guideline is voluntary.
Guideline and Conflicts of Interest
The Update Committee was assembled in accordance with the ASCO
Conflicts of Interest Management Procedures for Clinical Practice Guidelines
(summarized at http://www.asco.org/guidelinescoi). Members of the Update
Committee completed a disclosure form, which requires disclosure of financial and other interests that are relevant to the subject matter of the guideline,
including relationships with commercial entities that are reasonably likely to
experience direct regulatory or commercial impact as a result of promulgation
of the guideline. Categories for disclosure include employment relationships,
consulting arrangements, stock ownership, honoraria, research funding, and
expert testimony. In accordance with these procedures, the majority of the
members of the Update Committee did not disclose any such relationships.
RESULTS
A QUOROM diagram in the Data Supplement reports the results of
the literature search. Data were extracted from 14 articles in total. Data
Supplement Tables DS3 and DS4 summarize the characteristics of the
studies included in the literature review and analysis, along with their
findings. These tables, and other clinical tools and resources, can be
found at http://www.asco.org/guidelines/breastfollowup.
There were no new RCTs, systematic reviews, or meta-analyses
identified in the review that specifically examined history or physical
examination, breast self-examination, patient education regarding
symptoms of recurrence, or referral for genetic counseling. Additionally, there were no systematic reviews, meta-analyses, RCTs, or observational studies that met the inclusion criteria for breast cancer tumor
marker testing.
Breast Imaging
There were no RCTs of breast imaging that met the inclusion
criteria. Several systematic reviews on breast imaging were identified,
including one systematic review5 that evaluated the sensitivity of
breast magnetic resonance imaging to detect tumor recurrence and
two systematic reviews6,7 of the effectiveness of mammography for
breast cancer surveillance. Additionally, one meta-analysis8 examined
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ASCO Breast Cancer Surveillance Guideline Update
Table 1. Recommendations for Breast Cancer Follow-Up and Management in the Adjuvant Setting
Mode of Surveillance
Recommendationⴱ
RECOMMENDED
History/physical examination
All women should have a careful history and physical examination every 3 to 6 mo for the first 3 yr after primary therapy,
then every 6 to 12 mo for the next 2 yr, and then annually.
The history and physical examination should be performed by a physician† experienced in the surveillance of patients with
cancer and in breast examination.
Patient education regarding
Physicians should counsel patients about the symptoms of recurrence including new lumps, bone pain, chest pain,
symptoms of recurrence
dyspnea, abdominal pain, or persistent headaches. Helpful Web sites for patient education include www.cancer.net and
www.cancer.org.
Referral for genetic counseling Women at high risk for familial breast cancer syndromes should be referred for genetic counseling in accordance with
clinical guidelines recommended by the US Preventive Services Task Force.19 Criteria to recommend referral include the
following: Ashkenazi Jewish heritage; history of ovarian cancer at any age in the patient or any first- or second-degree
relatives; any first-degree relative with a history of breast cancer diagnosed before the age of 50 yr; two or more first- or
second-degree relatives diagnosed with breast cancer at any age; patient or relative with diagnosis of bilateral breast
cancer; and history of breast cancer in a male relative.‡
Breast self-examination
All women should be counseled to perform monthly breast self-examination.
Mammography
Women treated with breast-conserving therapy should have their first post-treatment mammogram no earlier than 6 mo
after definitive radiation therapy. Subsequent mammograms should be obtained every 6 to 12 mo for surveillance of
abnormalities. Mammography should be performed yearly if stability of mammographic findings is achieved after
completion of locoregional therapy.
Pelvic examination
Regular gynecologic follow-up is recommended for all women. Patients who receive tamoxifen therapy are at increased risk
for developing endometrial cancer and should be advised to report any vaginal bleeding to their physicians. Longer followup intervals may be appropriate for women who have had a total hysterectomy and oophorectomy.
Coordination of care
The risk of breast cancer recurrence continues through 15 yr after primary treatment and beyond. Continuity of care for
patients with breast cancer is recommended and should be performed by a physician experienced in the surveillance of
patients with cancer and in breast examination, including the examination of irradiated breasts. Follow-up by a PCP
seems to lead to the same health outcomes as specialist follow-up with good patient satisfaction.
If a patient with early-stage breast cancer (tumor ⬍5 cm and ⬍4 positive nodes) desires follow-up exclusively by a PCP,
care may be transferred to the PCP approximately 1 yr after diagnosis. If care is transferred to a PCP, both the PCP and
the patient should be informed of the appropriate follow-up and management strategy. Re-referral for further oncology
assessment may be considered, as needed, especially for patients who are receiving adjuvant endocrine therapy.
NOT RECOMMENDED
Routine blood tests
CBC testing is not recommended for routine breast cancer surveillance.
Automated chemistry studies are not recommended for routine breast cancer surveillance.
Imaging studies
Chest x-rays are not recommended for routine breast cancer surveillance.
Bone scans are not recommended for routine breast cancer surveillance.
Ultrasound of the liver is not recommended for routine breast cancer surveillance.
CT scanning is not recommended for routine breast cancer surveillance.
FDG-PET scanning is not recommended for routine breast cancer surveillance.
Breast MRI is not recommended for routine breast cancer surveillance.
The use of CA 15-3 or CA 27.29 is not recommended for routine surveillance of patients with breast cancer after primary
Breast cancer tumor marker
testing
therapy.
CEA testing is not recommended for routine surveillance of patients with breast cancer after primary therapy.
Abbreviations: CBC, complete blood count; CEA, carcinoembryonic antigen; FDG-PET, 关18F兴 fluorodeoxyglucose–positron emission tomography; MRI, magnetic
resonance imaging; PCP, primary care physician.
ⴱ
All recommendations remain the same as those published in 2006.3 The Panel concluded that there was no new evidence that warranted changing any of the
recommendations. The 2006 guideline provides a detailed discussion and rationale for the recommendations.
†Although the evidence is lacking, it seems likely that history as well as physical and breast exams may also be conducted by experienced non-physician providers
(eg, Nurse Practitioners, Physician Assistants) under the supervision of an experienced physician.
‡Expert consensus-based recommendations are available with criteria specific to patients with cancer (eg, from the National Comprehensive Cancer Network
关www.nccn.org兴). These recommendations include similar criteria as those from the USPSTF as well as other criteria such as diagnosis of triple negative breast
cancer, or a combination of breast cancer and other specific cancers.
the sensitivity of positron emission tomography (PET) and PET–
computed tomography (CT) to detect tumor recurrence, and one
systematic review9 evaluated the cost effectiveness of PET and PET-CT
in breast cancer surveillance.
There were two meta-analyses10,11 and one systematic review12
that addressed multiple modes of surveillance within their reviews and
analyses, including ultrasound, mammography, CT scans, magnetic
resonance imaging, clinical examinations, frequency of follow-up, or
specialist-led or primary care physician–led follow-up.
In general, the systematic reviews and meta-analyses were of
varying quality and had significant heterogeneity, particularly in terms
of sample characteristics and study designs (Data Supplement Table DS3).
www.jco.org
Coordination of Care
The literature search identified one systematic review and five
RCTs that compared various models of care for breast cancer surveillance (Data Supplement Table DS4). These studies and data were of
mixed quality—which is important to consider in terms of the reliability and validity of the findings—primarily because of inadequate sample sizes, limited follow-up periods, variations in protocols, and
protocol violations. The systematic review examined alternatives
to clinical follow-up and frequency or duration of follow-up.13
Three RCTs evaluated reduced follow-up strategies, including
nurse-led telephone follow-up compared with traditional hospitalbased follow-up14,15 and point-of-need access to specialist care
compared with routine hospital-based clinical review.16 In general, the
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Khatcheressian et al
studies found that reduced follow-up strategies did not negatively
affect patient-reported outcomes or early detection of recurrence.
Another RCT17 performed a cost-benefit analysis of standard clinical
follow-up compared with more intensive follow-up with additional
imaging and laboratory tests and concluded that more-intensive
follow-up was associated with higher costs without differences in early
detection of relapses. However, the analytic methods were not described in the report, and therefore, the validity of this conclusion is
difficult to ascertain. Results from one additional RCT18 found no
evidence that survivorship care plans improve patient-reported outcomes, including cancer-related distress and coordination of care,
when outcomes of Canadian women randomly assigned to receive a
survivorship care plan were compared with those of women who did
not receive a comprehensive survivorship care plan. Both groups had
follow-up transferred to primary care physicians, which was considered an important strategy to meet the demand for scarce oncology resources.
Clinical practice guidelines for surveillance of breast cancer are
available from many national and international organizations other
than ASCO. A list of some key guidelines is provided in the Data
Supplement (Data Supplement Table DS5). In general, the recommended modes of surveillance are comparable to ASCO’s recommendations. However, there are differences in recommended frequency
and duration of surveillance.
GUIDELINE RECOMMENDATIONS
After their review and analysis of the evidence for the various
modes of surveillance for breast cancer, the Update Committee
concluded that the evidence was not compelling enough to warrant
changes to any of the 2006 guideline recommendations.3 Table 1
provides a summary of the guideline recommendations. These recommendations are congruent with the five key opportunities identified by ASCO to improve cancer care and reduce costs.19
CONCLUSION AND FUTURE RESEARCH
After a systematic review and analysis of the literature for the
follow-up and management of patients with breast cancer, the Update
Committee concluded that there was no new evidence compelling
enough to warrant changes to any of the guideline recommendations.
Further research is needed—particularly RCTs—to determine the
comparative effectiveness of different modes of breast cancer surveillance and the ideal frequency and duration of follow-up. Research is
also needed to establish the clinical utility of breast cancer tumor
REFERENCES
1. Recommended breast cancer surveillance
guidelines: American Society of Clinical Oncology.
J Clin Oncol 15:2149-2156, 1997
2. Smith TJ, Davidson NE, Schapira DV, et al:
American Society of Clinical Oncology 1998 update
of recommended breast cancer surveillance guidelines. J Clin Oncol 17:1080-1082, 1999
3. Khatcheressian JL, Wolff AC, Smith TJ, et al:
American Society of Clinical Oncology 2006 update
of the breast cancer follow-up and management
4
© 2012 by American Society of Clinical Oncology
marker testing for the follow-up and management of breast cancer
and ultimately to develop clinical practice guidelines for tumor
marker testing that are risk based and/or specific to tumor subtypes
(eg, triple-negative breast cancer). More research is also needed to
evaluate the effectiveness and quality of different models of survivorship care and to identify subsets of patients who would benefit from
the various models of care.
In the meantime, the Update Committee encourages health care
providers to have an open dialogue with patients as part of a comprehensive treatment planning process. A useful way to approach treatment planning and ensure a coordinated cancer care plan is through
the ASCO Cancer Treatment Plans and Summary templates, available
online.20 The treatment planning discussion should include consideration of scientific evidence, weighing individual risks with potential
harms and benefits, and patient preferences. The Update Committee
will continue to monitor the literature for new evidence that may
warrant revisiting the recommendations for the follow-up and management of breast cancer after primary treatment.
ADDITIONAL RESOURCES
A Data Supplement and clinical tools and resources can be found at
http://www.asco.org/guidelines/breastfollowup. Patient information
is also available there and at http://www.cancer.net.
AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF
INTEREST
Although all authors completed the disclosure declaration, the following
author(s) and/or an author’s immediate family member(s) indicated a
financial or other interest that is relevant to the subject matter under
consideration in this article. Certain relationships marked with a “U” are
those for which no compensation was received; those relationships marked
with a “C” were compensated. For a detailed description of the disclosure
categories, or for more information about ASCO’s conflict of interest policy,
please refer to the Author Disclosure Declaration and the Disclosures of
Potential Conflicts of Interest section in Information for Contributors.
Employment or Leadership Position: None Consultant or Advisory
Role: N. Lynn Henry, GE Healthcare (C) Stock Ownership: None
Honoraria: None Research Funding: None Expert Testimony: None
Other Remuneration: None
AUTHOR CONTRIBUTIONS
Administrative support: Patricia Hurley, Mark R. Somerfield
Manuscript writing: All authors
Final approval of manuscript: All authors
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tomography (PET/CT) for the diagnosis of breast cancer recurrence. Health Technol Assess 14:1-103, 2010
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ASCO Breast Cancer Surveillance Guideline Update
(PET) and positron emission tomography/computed
tomography (PET/CT) for the diagnosis of breast
cancer recurrence. Health Technol Assess 15:iii-iv,
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10. Lu WL, Jansen L, Post WJ, et al: Impact on
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403-412, 2009
11. Montgomery DA, Krupa K, Cooke TG:
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13. Montgomery DA, Krupa K, Cooke TG: Alternative methods of follow up in breast cancer: A
systematic review of the literature. Br J Cancer
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14. Kimman ML, Bloebaum MM, Dirksen CD, et
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BMC Cancer 10:174, 2010
15. Beaver K, Tysver-Robinson D, Campbell M, et
al: Comparing hospital and telephone follow-up after
treatment for breast cancer: Randomised equivalence trial. BMJ 338:a3147, 2009
16. Sheppard C, Higgins B, Wise M, et al: Breast
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17. Oltra A, Santaballa A, Munárriz B, et al: Costbenefit analysis of a follow-up program in patients
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18. Grunfeld E, Julian JA, Pond G, et al: Evaluating
survivorship care plans: Results of a randomized,
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19. Schnipper LE, Smith TJ, Raghavan D, et al:
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key opportunities to improve care and reduce costs:
The top five list for oncology. J Clin Oncol 30:17151724, 2012
20. American Society of Clinical Oncology: Cancer
treatment plan and summary resources. http://www.asco
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■ ■ ■
www.jco.org
© 2012 by American Society of Clinical Oncology
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5
Khatcheressian et al
Acknowledgment
The Update Committee wishes to thank the American Society of Clinical Oncology Clinical Practice Guidelines Committee leadership and
the reviewers for Journal of Clinical Oncology for their thoughtful reviews of earlier drafts of the guideline update.
Appendix
Table A1. Guideline Update Committee Members
Update Committee Member
Affiliation
Nancy E. Davidson, MD, Co-Chair
James L. Khatcheressian, MD, Co-Chair
Elissa Bantug, MHS
Laura J. Esserman, MD, MBA
University of Pittsburgh Cancer Institute and UPMC Cancer Center, Pittsburgh, PA
Virginia Cancer Institute, Richmond, VA
Johns Hopkins Medicine and Sidney Kimmel Comprehensive Cancer Center, Baltimore, MD
Carol Franc Buck Breast Care Center and Helen Diller Family Comprehensive Cancer Center, University of California
at San Francisco, San Francisco, CA
University of Toronto and Ontario Institute for Cancer Research, Toronto, Ontario, Canada
Marin Cancer Institute, Greenbrae, CA
Edward Cancer Centers, Naperville, IL
University of Michigan Comprehensive Cancer Center, Ann Arbor, MI
Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC
Johns Hopkins Medicine and Sidney Kimmel Comprehensive Cancer Center, Baltimore, MD
Geisinger Medical Center, Danville, PA
Johns Hopkins Medicine and Sidney Kimmel Comprehensive Cancer Center, Baltimore, MD
Eva Grunfeld, MD, DPhil
Francine Halberg, MD
Alexander Hantel, MD
N. Lynn Henry, MD, PhD
Hyman B. Muss, MD
Thomas J. Smith, MD
Victor G. Vogel, MD
Antonio C. Wolff, MD
Abbreviation: UPMC, University of Pittsburgh Medical Center.
6
© 2012 by American Society of Clinical Oncology
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