Heidi D. Nelson, MD, MPH; Miranda Pappas, MA; Amy Cantor, MD, MPH; Jessica Griffin, MS; Monica Daeges, BA; Linda Humphrey, MD, MPH
Disclaimer: The findings and conclusions in this article are those of the authors, who are responsible for its content, and do not necessarily represent the views of the AHRQ. No statement in this report should be construed as an official position of the AHRQ or the U.S. Department of Health and Human Services.
Acknowledgment: The authors thank Andrew Hamilton, MLS, MS, for conducting literature searches and Spencer Dandy, BS, for assisting with manuscript preparation at the Pacific Northwest Evidence-based Practice Center at Oregon Health & Science University; Alison Conlin, MD, MPH, and Michael Neuman, MD, at the Providence Cancer Center at Providence Health and Services Oregon, and Arpana Naik, MD, at Oregon Health & Science University for providing medical expertise; Jennifer Croswell, MD, MPH, at the AHRQ; and USPSTF members Linda Baumann, PhD, RN, Kirsten Bibbins-Domingo, PhD, MD, MAS, Mark Ebell, MD, MS, Jessica Herzstein, MD, MPH, Michael LeFevre, MD, MSPH, and Douglas Owens, MD, MS.
Financial Support: By the AHRQ (contract 290-2012-00015-I, Task Order 2), Rockville, Maryland.
Disclosures: Drs. Nelson, Cantor, and Humphrey; Ms. Pappas; Ms. Griffin; and Ms. Daeges report grants from AHRQ during the conduct of this study. Forms can be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M15-0970.
Editors' Disclosures: Christine Laine, MD, MPH, Editor in Chief, reports that she has no financial relationships or interests to disclose. Darren B. Taichman, MD, PhD, Executive Deputy Editor, reports that he has no financial relationships or interests to disclose. Cynthia D. Mulrow, MD, MSc, Senior Deputy Editor, reports that she has no relationships or interests to disclose. Deborah Cotton, MD, MPH, Deputy Editor, reports that she has no financial relationships or interest to disclose. Jaya K. Rao, MD, MHS, Deputy Editor, reports that she has stock holdings/options in Eli Lilly and Pfizer. Sankey V. Williams, MD, Deputy Editor, reports that he has no financial relationships or interests to disclose. Catharine B. Stack, PhD, MS, Deputy Editor for Statistics, reports that she has stock holdings in Pfizer.
Requests for Single Reprints: Heidi D. Nelson, MD, MPH, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Mail Code BICC, Portland, OR 97239; e-mail, firstname.lastname@example.org.
Current Author Addresses: Drs. Nelson, Cantor, and Humphrey; Ms. Pappas; Ms. Griffin; and Ms. Daeges: Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Mail Code BICC, Portland, OR 97239.
Author Contributions: Conception and design: H.D. Nelson, M. Pappas, A. Cantor, L. Humphrey.
Analysis and interpretation of the data: H.D. Nelson, M. Pappas, A. Cantor, J. Griffin, M. Daeges, L. Humphrey.
Drafting of the article: H.D. Nelson, M. Pappas, A. Cantor, L. Humphrey.
Critical revision of the article for important intellectual content: H.D. Nelson, A. Cantor, L. Humphrey.
Final approval of the article: H.D. Nelson, M. Pappas, A. Cantor, J. Griffin, M. Daeges, L. Humphrey.
Provision of study materials or patients: H.D. Nelson, M. Daeges.
Obtaining of funding: H.D. Nelson.
Administrative, technical, or logistic support: H.D. Nelson, M. Pappas, A. Cantor, M. Daeges.
Collection and assembly of data: H.D. Nelson, M. Pappas, A. Cantor, J. Griffin, M. Daeges, L. Humphrey.
Nelson HD, Pappas M, Cantor A, Griffin J, Daeges M, Humphrey L. Harms of Breast Cancer Screening: Systematic Review to Update the 2009 U.S. Preventive Services Task Force Recommendation. Ann Intern Med. 2016;164:256-267. doi: 10.7326/M15-0970
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Published: Ann Intern Med. 2016;164(4):256-267.
Published at www.annals.org on 12 January 2016
In 2009, the U.S. Preventive Services Task Force recommended biennial mammography screening for women aged 50 to 74 years and selective screening for those aged 40 to 49 years.
To review studies of screening in average-risk women with mammography, magnetic resonance imaging, or ultrasonography that reported on false-positive results, overdiagnosis, anxiety, pain, and radiation exposure.
MEDLINE and Cochrane databases through December 2014.
English-language systematic reviews, randomized trials, and observational studies of screening.
Investigators extracted and confirmed data from studies and dual-rated study quality. Discrepancies were resolved through consensus.
Based on 2 studies of U.S. data, 10-year cumulative rates of false-positive mammography results and biopsies were higher with annual than biennial screening (61% vs. 42% and 7% vs. 5%, respectively) and for women aged 40 to 49 years, those with dense breasts, and those using combination hormone therapy. Twenty-nine studies using different methods reported overdiagnosis rates of 0% to 54%; rates from randomized trials were 11% to 22%. Women with false-positive results reported more anxiety, distress, and breast cancer–specific worry, although results varied across 80 observational studies. Thirty-nine observational studies indicated that some women reported pain during mammography (1% to 77%); of these, 11% to 46% declined future screening. Models estimated 2 to 11 screening-related deaths from radiation-induced cancer per 100 000 women using digital mammography, depending on age and screening interval. Five observational studies of tomosynthesis and mammography indicated increased biopsies but reduced recalls compared with mammography alone.
Studies of overdiagnosis were highly heterogeneous, and estimates varied depending on the analytic approach. Studies of anxiety and pain used different outcome measures. Radiation exposure was based on models.
False-positive results are common and are higher for annual screening, younger women, and women with dense breasts. Although overdiagnosis, anxiety, pain, and radiation exposure may cause harm, their effects on individual women are difficult to estimate and vary widely.
Agency for Healthcare Research and Quality.
Analytic framework and key questions.
KQ = key question.
* Excludes women with preexisting breast cancer; clinically significant BRCA1 or BRCA2 mutations, Li-Fraumeni syndrome, Cowden syndrome, hereditary diffuse gastric cancer, or other familial breast cancer syndrome; high-risk lesions (ductal carcinoma in situ, lobular carcinoma in situ, atypical ductal hyperplasia, or atypical lobular hyperplasia); or previous large doses of chest radiation (≥20 Gy) before age 30 y.
† False-positive and false-negative mammography results, biopsy recommendations due to false-positive mammography results, overdiagnosis and resulting overtreatment, anxiety, pain, and radiation exposure.
‡ Family history; breast density; race/ethnicity; menopausal status; current use of menopausal hormone therapy or oral contraceptives; prior benign breast biopsy; and, for women aged >50 y, body mass index.
§ Mammography (film, digital, or tomosynthesis), magnetic resonance imaging, ultrasonography, and clinical breast examination (alone or in combination).
Summary of evidence search and selection.
RCT = randomized, controlled trial.
* Cochrane Central Register of Controlled Trials and Cochrane Database of Systematic Reviews.
Appendix Table 1. U.S. Studies of Cumulative False-Positive Mammography and Biopsy Results
Appendix Table 2. Studies of Overdiagnosis With Breast Cancer Screening
Appendix Table 2–Continued
Table 1. Systematic Reviews of Psychological Harms of Breast Cancer Screening
Table 2. Results of New Studies of Psychological Harms of Breast Cancer Screening
Appendix Table 3. Systematic Reviews of Pain With Mammography
Appendix Table 4. Models of Radiation Exposure With Screening, Breast Cancer Incidence, and Death
Appendix Table 5. Studies of Harms of Breast Cancer Screening With Different Modalities
Table 3. Summary of Evidence
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Hematology/Oncology, Breast Cancer, Cancer Screening/Prevention, Prevention/Screening.
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