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Breast Cancer Follow-Up and Management After PrimaryTreatment: American Society of Clinical Oncology ClinicalPractice Guideline UpdateJames 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 Fran-

cisco, 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 Comprehen-

sive 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 Pitts-

burgh 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 writ-

ten 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

A B S T R A C T

PurposeTo provide recommendations on the follow-up and management of patients with breast cancerwho have completed primary therapy with curative intent.

MethodsTo update the 2006 guideline of the American Society of Clinical Oncology (ASCO), a systematicreview of the literature published from March 2006 through March 2012 was completed usingMEDLINE and the Cochrane Collaboration Library. An Update Committee reviewed the evidenceto determine whether the recommendations were in need of updating.

ResultsThere were 14 new publications that met inclusion criteria: nine systematic reviews (threeincluded meta-analyses) and five randomized controlled trials. After its review and analysis of theevidence, the Update Committee concluded that no revisions to the existing ASCO recommen-dations were warranted.

RecommendationsRegular history, physical examination, and mammography are recommended for breast cancerfollow-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 undergonebreast-conserving surgery, a post-treatment mammogram should be obtained 1 year after theinitial mammogram and at least 6 months after completion of radiation therapy. Thereafter, unlessotherwise indicated, a yearly mammographic evaluation should be performed. The use ofcomplete blood counts, chemistry panels, bone scans, chest radiographs, liver ultrasounds, pelvicultrasounds, computed tomography scans, [18F]fluorodeoxyglucosepositron emission tomogra-phy scans, magnetic resonance imaging, and/or tumor markers (carcinoembryonic antigen, CA15-3, and CA 27.29) is not recommended for routine follow-up in an otherwise asymptomaticpatient 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

guidelineonbreastcancer follow-upand management

in asymptomatic patients after primary, curative ther-

apy.1 ASCO guidelines are updated periodically by a

subset of the original expert panel. The guideline was

updated andpublished in19992and 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 recommen-

dations needed additional updating.

This clinical practice guideline addresses three

overarching clinical questions: (1) What guidancearound follow-up and management should be avail-

able to women whohave been previously treated for

breast cancer? (2) What testing is recommended for

the detection of breast cancer recurrence in the ad-

juvant setting after curative-intentprimary therapy?

(3) What is the optimal frequency of monitoring?

Table 1 summarizes the guideline recom-

mendations. A Data Supplement, a patient guide,

and other clinical tools and resources to help cli-

nicians implement this guideline are available at

http://www.asco.org/guidelines/breastfollowup.

JOURNAL OF CLINICAL ONCOLOGY A S C O S P E C I A L A R T I C L E

2012 by American Society of Clinical Oncology 1

http://jco.ascopubs.org/cgi/doi/10.1200/JCO.2012.45.9859The latest version is atPublished Ahead of Print on November 5, 2012 as 10.1200/JCO.2012.45.9859

Copyright 2012 by American Society of Clinical OncologyDownloaded from jco.ascopubs.org on January 30, 2014. For personal use only. No other uses without permission.

Copyright 2012 American Society of Clinical Oncology. All rights reserved.
http://www.asco.org/guidelines/breastfollowuphttp://jco.ascopubs.org/cgi/doi/10.1200/JCO.2012.45.9859http://jco.ascopubs.org/cgi/doi/10.1200/JCO.2012.45.9859http://jco.ascopubs.org/cgi/doi/10.1200/JCO.2012.45.9859http://jco.ascopubs.org/cgi/doi/10.1200/JCO.2012.45.9859http://www.asco.org/guidelines/breastfollowup

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METHODS

The Update Committee included academic and community practitioners,medicaloncologists,a surgicaloncologist,a radiation oncologist, hematologiconcologists, a gynecologic oncologist, a primary care physician, and a patientadvocate (AppendixTableA1, online only). A Working Group of the UpdateCommittee completed a review and analysis of evidence published betweenMarch 2006 and March 2012 to determine whether the recommendations

needed to be updated. The Working Group drafted the guideline update andcirculated it to thefullUpdateCommitteeforreview andapproval. TheASCOClinical PracticeGuidelinesCommitteeleadershipreviewed andapprovedthefinal document.

Details of the literature search strategy and the inclusion and exclusioncriteriaare providedin theDataSupplement (http://www.asco.org/guidelines/breastfollowup). In brief, studies were included if their primary objectivewasthe follow-upand managementof patients with breast cancerwho hadcompleted primary therapy with curative intent. The outcomes of interestwere disease-free survival, overall survival, health-related quality of life,reduced toxicity, and cost effectiveness. The searches were limited torandomized controlled trials (RCTs), systematic reviews (with or withoutmeta-analyses),and clinicalpracticeguidelines. However,for the search ontumor markers, both randomized and nonrandomized studies were eligi-ble if they directly addressed the clinical utility of one or more tumormarkers (ie, carcinoembryonic antigen, CA 15-3, and CA 27.29) by com-paringthe outcomes of interest fora group of patients monitoredwith oneor more ofthe listed tumor markers with a group ofpatients who were notmonitored with any tumor marker.

Guideline PolicyThe practice guideline is not intended to substitute for the independent

professional judgment of the treating physician. Practice guidelines do notaccount for individual variation among patients andmay not reflect the mostrecent evidence. Thisguidelinedoes notrecommendany particularproductorcourse of medical treatment. Use of the practice guideline is voluntary.

Guideline and Conflicts of InterestThe 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 UpdateCommittee completed a disclosure form, which requires disclosure of finan-cial and other interests that are relevant to the subject matter of the guideline,including relationships with commercial entities that are reasonably likely toexperience direct regulatory or commercial impactas a result of promulgationof the guideline. Categories for disclosure include employment relationships,consulting arrangements, stock ownership, honoraria, research funding, andexpert 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

theliterature search.Datawere extracted from14 articlesin total. Data

Supplement Tables DS3and 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. Addition-ally, there were no systematic reviews, meta-analyses, RCTs, or obser-

vationalstudies thatmet 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

THE BOTTOM LINE

ASCO GUIDELINE UPDATE

Breast Cancer Follow-Up and Management After

Primary Treatment: American Society of ClinicalOncology Clinical Practice Guideline Update

Intervention

Modes of surveillance for patients with breast cancer whohave completed primary therapy with curative intent

Target Audience

Medical oncologists, primary care providers, oncology

nurses, surgical oncologists, pathologists, and nuclear medi-

cine 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 radio-

graphs, liver ultrasounds, computed tomography scans,

[18F]fluorodeoxyglucosepositron 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 anotherwise 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 re-

view 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

Khatcheressian et al

2 2012 by American Society of Clinical Oncology JOURNAL OF CLINICAL ONCOLOGY

Downloaded from jco.ascopubs.org on January 30, 2014. For personal use only. No other uses without permission.Copyright 2012 American Society of Clinical Oncology. All rights reserved.
http://www.asco.org/guidelines/breastfollowuphttp://www.asco.org/guidelines/breastfollowuphttp://www.asco.org/guidelines/breastfollowuphttp://www.asco.org/guidelines/breastfollowup

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the sensitivity of positron emission tomography (PET) and PET

computed tomography (CT) to detect tumor recurrence, and one

systematic review9evaluated thecost effectivenessof PETand PET-CT

in breast cancer surveillance.

There were two meta-analyses10,11 and one systematic review12

thataddressed multiple modes of surveillancewithintheir reviewsand

analyses, including ultrasound, mammography, CT scans, magnetic

resonance imaging, clinical examinations, frequency of follow-up, or

specialist-led or primary care physicianled follow-up.

In general, the systematic reviews and meta-analyses were of

varying qualityand hadsignificant heterogeneity, particularly in terms

of sample characteristics and study designs (Data Supplement Ta-

ble DS3).

Coordination of Care

The literature search identified one systematic review and five

RCTs that compared various models of care for breast cancer surveil-

lance (Data Supplement Table DS4). These studies and data were of

mixed qualitywhichis important to considerin terms of thereliabil-

ity and validity of the findingsprimarily becauseof inadequate sam-

ple 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-upcompared withtraditional hospital-

based follow-up14,15 and point-of-need access to specialist care

comparedwith routinehospital-basedclinical review.16 Ingeneral,the

Table 1. Recommendations for Breast Cancer Follow-Up and Management in the Adjuvant Setting

Mode of Surveillance Recommendation

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 withcancer and in breast examination.

Patient education regarding

symptoms of recurrence

Physicians should counsel patients about the symptoms of recurrence including new lumps, bone pain, chest pain,

dyspnea, abdominal pain, or persistent headaches. Helpful Web sites for patient education include www.cancer.net andwww.cancer.org.

Referral for genetic counseling Women at high risk for familial breast cancer syndromes should be referred for genetic counseling in accordance withclinical guidelines recommended by the US Preventive Services Task Force.19 Criteria to recommend referral include thefollowing: Ashkenazi Jewish heritage; history of ovarian cancer at any age in the patient or any first- or second-degreerelatives; any first-degree relative with a history of breast cancer diagnosed before the age of 50 yr; two or more first- orsecond-degree relatives diagnosed with breast cancer at any age; patient or relative with diagnosis of bilateral breastcancer; 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 moafter definitive radiation therapy. Subsequent mammograms should be obtained every 6 to 12 mo for surveillance ofabnormalities. Mammography should be performed yearly if stability of mammographic findings is achieved aftercompletion of locoregional therapy.

Pelvic examination Regular gynecologic follow-up is recommended for all women. Patients who receive tamoxifen therapy are at increased riskfor developing endometrial cancer and should be advised to report any vaginal bleeding to their physicians. Longer follow-up 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 ofpatients with cancer and in breast examination, including the examination of irradiated breasts. Follow-up by a PCPseems to lead to the same health outcomes as specialist follow-up with good patient satisfaction.

If a patient with early-stage breast cancer (tumor5 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 andthe patient should be informed of the appropriate follow-up and management strategy. Re-referral for further oncologyassessment 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.

Breast cancer tumor markertesting

The use of CA 15-3 or CA 27.29is not recommended for routine surveillance of patients with breast cancer after primarytherapy.

CEAtesting is not recommended for routine surveillance of patients with breast cancer after primary therapy.

Abbreviations: CBC, complete blood count; CEA, carcinoembryonic antigen; FDG-PET, 18F fluorodeoxyglucosepositron emission tomography; MRI, magneticresonance imaging; PCP, primary care physician.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

www.nccn.org). These recommendations include similar criteria as those from the USPSTF as well as other criteria such as diagnosis of triple negative breastcancer, or a combination of breast cancer and other specific cancers.

ASCO Breast Cancer Surveillance Guideline Update

www.jco.org 2012 by American Society of Clinical Oncology 3


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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 wasassociated with higher costs withoutdifferencesin early

detection of relapses. However, the analytic methods were not de-

scribed 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 out-

comes, 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 consid-

ered an important strategy to meet the demand for scarce oncolo-

gy 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 recom-mended modes of surveillance are comparableto ASCOs recommen-

dations. 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

concludedthat theevidencewas notcompelling enoughto warrant

changes to any of the 2006 guideline recommendations.3 Table 1

provides a summary of the guideline recommendations. These rec-

ommendations are congruent with the five key opportunities identi-fied 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 patientswith breast cancer, theUpdate

Committee concluded that there was no new evidence compelling

enoughto warrant changes to anyof the guideline recommendations.

Further research is neededparticularly RCTsto determine the

comparative effectiveness of different modes of breast cancer surveil-

lance and the ideal frequency and duration of follow-up. Research is

also needed to establish the clinical utility of breast cancer tumor

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 survivor-

ship 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 compre-

hensive treatment planning process. A useful way to approach treat-

ment planning and ensure a coordinated cancer care plan is through

the ASCOCancer Treatment Plans and Summary templates, available

online.20 The treatment planning discussion should include consider-

ation 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 man-

agement 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 OFINTEREST

Although all authors completed the disclosure declaration, the followingauthor(s) and/or an authors immediate family member(s) indicated a

financial or other interest that is relevant to the subject matter underconsideration in this article. Certain relationships marked with a U arethose for which no compensation was received; those relationships markedwith a C were compensated. For a detailed description of the disclosurecategories, or for more information about ASCOs conflict of interest policy,

please refer to the Author Disclosure Declaration and the Disclosures ofPotential Conflicts of Interest section in Information for Contributors.Employment or Leadership Position: None Consultant or AdvisoryRole:N. Lynn Henry, GE Healthcare (C)Stock Ownership:NoneHonoraria:NoneResearch Funding:NoneExpert Testimony:NoneOther Remuneration: None

AUTHOR CONTRIBUTIONS

Administrative support:Patricia Hurley, Mark R. SomerfieldManuscript writing:All authors

Final approval of manuscript: All authors

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ASCO Breast Cancer Surveillance Guideline Update

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Acknowledgment

The Update Committee wishes to thank the American Society of Clinical Oncology Clinical Practice Guidelines Committee leadership and

the reviewers forJournal of Clinical Oncologyfor 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 University of Pittsburgh Cancer Institute and UPMC Cancer Center, Pittsburgh, PA

James L. Khatcheressian, MD, Co-Chair Virginia Cancer Institute, Richmond, VA

Elissa Bantug, MHS Johns Hopkins Medicine and Sidney Kimmel Comprehensive Cancer Center, Baltimore, MD

Laura J. Esserman, MD, MBA Carol Franc Buck Breast Care Center and Helen Diller Family Comprehensive Cancer Center, University of Californiaat San Francisco, San Francisco, CA

Eva Grunfeld, MD, DPhil University of Toronto and Ontario Institute for Cancer Research, Toronto, Ontario, Canada

Francine Halberg, MD Marin Cancer Institute, Greenbrae, CA

Alexander Hantel, MD Edward Cancer Centers, Napervil le, IL

N. Lynn Henry, MD, PhD University of Michigan Comprehensive Cancer Center, Ann Arbor, MI

Hyman B. Muss, MD Lineberger Comprehensive Cancer Center, University of North Carolina at Chapel Hill, Chapel Hill, NC

Thomas J. Smith, MD Johns Hopkins Medicine and Sidney Kimmel Comprehensive Cancer Center, Baltimore, MD

Victor G. Vogel, MD Geisinger Medical Center, Danville, PA

Antonio C. Wolff, MD Johns Hopkins Medicine and Sidney Kimmel Comprehensive Cancer Center, Baltimore, MD

Abbreviation: UPMC, University of Pittsburgh Medical Center.




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