Published Ahead of Print on November 5, 2012 as 10.1200/JCO.2012.45.9859 The latest version is at http://jco.ascopubs.org/cgi/doi/10.1200/JCO.2012.45.

9859

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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. Somereld, and Nancy E. Davidson Processed as a Rapid Communication manuscript
James L. Khatcheressian, Virginia Cancer Institute, Richmond; Patricia Hurley and Mark R. Somereld, 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 conicts 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

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 ve 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 rst 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]uorodeoxyglucosepositron 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 specic ndings 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.
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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 rst 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]uorodeoxyglucosepositron 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 specic ndings 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

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 nal 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 reect 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 Conicts of Interest The Update Committee was assembled in accordance with the ASCO Conicts 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 nancial 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 ndings. 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 identied in the review that specically 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 identied, 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 RECOMMENDED History/physical examination Recommendation

All women should have a careful history and physical examination every 3 to 6 mo for the rst 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 rst- or second-degree relatives; any rst-degree relative with a history of breast cancer diagnosed before the age of 50 yr; two or more rst- 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 rst post-treatment mammogram no earlier than 6 mo after denitive 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 ndings 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, 18F uorodeoxyglucosepositron emission tomography; MRI, magnetic resonance 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 specic 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 breast cancer, or a combination of breast cancer and other specic 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 physicianled follow-up. In general, the systematic reviews and meta-analyses were of varying quality and had signicant heterogeneity, particularly in terms of sample characteristics and study designs (Data Supplement Table DS3).
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Coordination of Care The literature search identied one systematic review and ve RCTs that compared various models of care for breast cancer surveillance (Data Supplement Table DS4). These studies and data were of mixed qualitywhich is important to consider in terms of the reliability and validity of the ndingsprimarily 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-benet 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 difcult 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 ASCOs recommendations. However, there are differences in recommended frequency and duration of surveillance.
GUIDELINE RECOMMENDATIONS

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 specic 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 benet 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 scientic evidence, weighing individual risks with potential harms and benets, 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 authors immediate family member(s) indicated a nancial 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 ASCOs conict of interest policy, please refer to the Author Disclosure Declaration and the Disclosures of Potential Conicts 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

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 ve key opportunities identied 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 neededparticularly RCTsto 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

AUTHOR CONTRIBUTIONS
Administrative support: Patricia Hurley, Mark R. Somereld Manuscript writing: All authors Final approval of manuscript: All authors
A systematic review. Plast Reconstr Surg 120:11251132, 2007 7. Houssami N, Ciatto S: Mammographic surveillance in women with a personal history of breast cancer: How accurate? How effective? Breast 19: 439-445, 2010 8. Pennant M, Takwoingi Y, Pennant L, et al: A systematic review of positron emission tomography (PET) and positron emission tomography/computed tomography (PET/CT) for the diagnosis of breast cancer recurrence. Health Technol Assess 14:1-103, 2010 9. Auguste P, Barton P, Hyde C, et al: An economic evaluation of positron emission tomography
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guidelines in the adjuvant setting. J Clin Oncol 24:5091-5097, 2006 4. US Preventive Services Task Force: Genetic risk assessment and BRCA mutation testing for breast and ovarian cancer susceptibility: Recommendation statement. Ann Intern Med 143:355-361, 2005 5. Morrow M, Waters J, Morris E: MRI for breast cancer screening, diagnosis, and treatment. Lancet 378:1804-1811, 2011 6. Barnsley GP, Grunfeld E, Coyle D, et al: Surveillance mammography following the treatment of primary breast cancer with breast reconstruction:

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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, 1-54, 2011 10. Lu WL, Jansen L, Post WJ, et al: Impact on survival of early detection of isolated breast recurrences after the primary treatment for breast cancer: A meta-analysis. Breast Cancer Res Treat 114: 403-412, 2009 11. Montgomery DA, Krupa K, Cooke TG: Follow-up in breast cancer: Does routine clinical examination improve outcome? A systematic review of the literature. Br J Cancer 97:1632-1641, 2007 12. Robertson C, Arcot Ragupathy SK, Boachie C, et al: The clinical effectiveness and costeffectiveness of different surveillance mammography regimens after the treatment for primary breast cancer: Systematic reviews registry database anal-

yses and economic evaluation. Health Technol Assess 15:v-vi, 1-322, 2011 13. Montgomery DA, Krupa K, Cooke TG: Alternative methods of follow up in breast cancer: A systematic review of the literature. Br J Cancer 96:1625-1632, 2007 14. Kimman ML, Bloebaum MM, Dirksen CD, et al: Patient satisfaction with nurse-led telephone follow-up after curative treatment for breast cancer. 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 cancer follow up: A randomised controlled trial comparing point of need access versus routine 6-monthly clinical review. Eur J Oncol Nurs 13:2-8, 2009

17. Oltra A, Santaballa A, Muna rriz B, et al: Costbenet analysis of a follow-up program in patients with breast cancer: A randomized prospective study. Breast J 13:571-574, 2007 18. Grunfeld E, Julian JA, Pond G, et al: Evaluating survivorship care plans: Results of a randomized, clinical trial of patients with breast cancer. J Clin Oncol 29:4755-4762, 2011 19. Schnipper LE, Smith TJ, Raghavan D, et al: American Society of Clinical Oncology identies ve key opportunities to improve care and reduce costs: The top ve list for oncology. J Clin Oncol 30:17151724, 2012 20. American Society of Clinical Oncology: Cancer treatment plan and summary resources. http://www.asco .org/ASCOv2/Practice%26Guidelines/QualityCare/ QualityMeasurement%26Improvement/Chemo therapyTreatmentPlanandSummary/Cancer TreatmentPlanandSummaryResources

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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 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 Nancy E. Davidson, MD, Co-Chair James L. Khatcheressian, MD, Co-Chair Elissa Bantug, MHS Laura J. Esserman, MD, MBA 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 Afliation 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

Abbreviation: UPMC, University of Pittsburgh Medical Center.

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