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Reviews | 
Heidi D. Nelson, MD, MPH; Miranda Pappas, MA; Amy Cantor, MD, MPH; Jessica Griffin, MS; Monica Daeges, BA; and Linda Humphrey, MD, MPH
Background: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. Purpose: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. Data Sources:MEDLINE and Cochrane databases through December 2014. Study Selection:English-language systematic reviews, randomized trials, and observational studies of screening. Data Extraction:Investigators extracted and confirmed data from studies and dual-rated study quality. Discrepancies were resolved through consensus. Data Synthesis: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. Limitations: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. Conclusion: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. Primary Funding Source:Agency for Healthcare Research and Quality.
Topics: mammography, pain, breast cancer, breast neoplasm screening, false-positive results, overdiagnosis, biopsy, anxiety, radiation exposure
Original Research | 
Heidi D. Nelson, MD, MPH; Ellen S. O'Meara, PhD; Karla Kerlikowske, MD, MPH; Steven Balch, MA, MBA; and Diana Miglioretti, PhD
Background:Women screened with digital mammography may receive false-positive and false-negative results and subsequent imaging and biopsies. How these outcomes vary by age, time since the last screening, and individual risk factors is unclear. Objective:To determine factors associated with false-positive and false-negative digital mammography results, additional imaging, and biopsies among a general population of women screened for breast cancer. Design:Analysis of registry data. Setting:Participating facilities at 5 U.S. Breast Cancer Surveillance Consortium breast imaging registries with linkages to pathology databases and tumor registries. Patients:405 191 women aged 40 to 89 years screened with digital mammography between 2003 and 2011. A total of 2963 were diagnosed with invasive cancer or ductal carcinoma in situ within 12 months of screening. Measurements:Rates of false-positive and false-negative results and recommendations for additional imaging and biopsies from a single screening round; comparisons by age, time since the last screening, and risk factors. Results:Rates of false-positive results (121.2 per 1000 women [95% CI, 105.6 to 138.7]) and recommendations for additional imaging (124.9 per 1000 women [CI, 109.3 to 142.3]) were highest among women aged 40 to 49 years and decreased with increasing age. Rates of false-negative results (1.0 to 1.5 per 1000 women) and recommendations for biopsy (15.6 to 17.5 per 1000 women) did not differ greatly by age. Results did not differ by time since the last screening. False-positive rates were higher for women with risk factors, particularly family history of breast cancer; previous benign breast biopsy result; high breast density; and, for younger women, low body mass index. Limitations:Confounding by variation in patient-level characteristics and outcomes across registries and regions may have been present. Some factors, such as numbers of first- and second-degree relatives with breast cancer and diagnoses associated with previous benign biopsy results, were not examined. Conclusion:False-positive mammography results and additional imaging are common, particularly for younger women and those with risk factors, whereas biopsies occur less often. Rates of false-negative results are low. Primary Funding Source:Agency for Healthcare Research and Quality and National Cancer Institute.
Topics: biopsy, mammography, diagnostic imaging, mammography, digital, false-positive results, false-negative results, breast density, breast cancer
Reviews | 
Joy Melnikow, MD, MPH; Joshua J. Fenton, MD, MPH; Evelyn P. Whitlock, MD, MPH; Diana L. Miglioretti, PhD; Meghan S. Weyrich, MPH; Jamie H. Thompson, MPH; and Kunal Shah
Background:Screening mammography has lower sensitivity and specificity in women with dense breasts, who experience higher breast cancer risk. Purpose:To perform a systematic review of reproducibility of Breast Imaging Reporting and Data System (BI-RADS) density categorization and test performance and clinical outcomes of supplemental screening with breast ultrasonography, magnetic resonance imaging (MRI), and digital breast tomosynthesis (DBT) in women with dense breasts and negative mammography results. Data Sources:MEDLINE, PubMed, EMBASE, and Cochrane database from January 2000 to July 2015. Study Selection:Studies reporting BI-RADS density reproducibility or supplemental screening results for women with dense breasts. Data Extraction:Quality assessment and abstraction of 24 studies from 7 countries; 6 studies were good-quality. Data Synthesis:Three good-quality studies reported reproducibility of BI-RADS density; 13% to 19% of women were recategorized between “dense” and “nondense” at subsequent screening. Two good-quality studies reported that sensitivity of ultrasonography for women with negative mammography results ranged from 80% to 83%; specificity, from 86% to 94%; and positive predictive value (PPV), from 3% to 8%. The sensitivity of MRI ranged from 75% to 100%; specificity, from 78% to 94%; and PPV, from 3% to 33% (3 studies). Rates of additional cancer detection with ultrasonography were 4.4 per 1000 examinations (89% to 93% invasive); recall rates were 14%. Use of MRI detected 3.5 to 28.6 additional cancer cases per 1000 examinations (34% to 86% invasive); recall rates were 12% to 24%. Rates of cancer detection with DBT increased by 1.4 to 2.5 per 1000 examinations compared with mammography alone (3 studies). Recall rates ranged from 7% to 11%, compared with 7% to 17% with mammography alone. No studies examined breast cancer outcomes. Limitations:Good-quality evidence was sparse. Studies were small and CIs were wide. Definitions of recall were absent or inconsistent. Conclusion:Density ratings may be recategorized on serial screening mammography. Supplemental screening of women with dense breasts finds additional breast cancer but increases false-positive results. Use of DBT may reduce recall rates. Effects of supplemental screening on breast cancer outcomes remain unclear. Primary Funding Source:Agency for Healthcare Research and Quality.
Topics: breast, breast cancer, breast neoplasm screening, breast density, breast imaging reporting and data system, magnetic resonance imaging, cancer, mammography
Clinical Guidelines | 
Albert L. Siu, MD, MSPH, on behalf of the U.S. Preventive Services Task Force
Description:Update of the 2009 U.S. Preventive Services Task Force (USPSTF) recommendation on screening for breast cancer. Methods:The USPSTF reviewed the evidence on the following: effectiveness of breast cancer screening in reducing breast cancer–specific and all-cause mortality, as well as the incidence of advanced breast cancer and treatment-related morbidity; harms of breast cancer screening; test performance characteristics of digital breast tomosynthesis as a primary screening strategy; and adjunctive screening in women with increased breast density. In addition, the USPSTF reviewed comparative decision models on optimal starting and stopping ages and intervals for screening mammography; how breast density, breast cancer risk, and comorbidity level affect the balance of benefit and harms of screening mammography; and the number of radiation-induced breast cancer cases and deaths associated with different screening mammography strategies over the course of a woman's lifetime. Population:This reccommendation applies to asymptomatic women aged 40 years or older who do not have preexisting breast cancer or a previously diagnosed high-risk breast lesion and who are not at high risk for breast cancer because of a known underlying genetic mutation (such as a BRCA1 or BRCA2 gene mutation or other familial breast cancer syndrome) or a history of chest radiation at a young age. Recommendations:The USPSTF recommends biennial screening mammography for women aged 50 to 74 years. (B recommendation)The decision to start screening mammography in women prior to age 50 years should be an individual one. Women who place a higher value on the potential benefit than the potential harms may choose to begin biennial screening between the ages of 40 and 49 years. (C recommendation)The USPSTF concludes that the current evidence is insufficient to assess the balance of benefits and harms of screening mammography in women aged 75 years or older. (I statement)The USPSTF concludes that the current evidence is insufficient to assess the benefits and harms of digital breast tomosynthesis (DBT) as a primary screening method for breast cancer. (I statement)The USPSTF concludes that the current evidence is insufficient to assess the balance of benefits and harms of adjunctive screening for breast cancer using breast ultrasonography, magnetic resonance imaging (MRI), DBT, or other methods in women identified to have dense breasts on an otherwise negative screening mammogram. (I statement)
Topics: mammography, breast cancer, breast neoplasm screening, breast
Melnikow and colleagues summarize evidence about the benefits and harms of supplemental screening with ultrasonography, magnetic resonance imaging, or digital breast tomosynthesis in women with dense breasts and negative results on mammography. The editorialist argues that we should not wait for randomized trials that evaluate mortality outcomes. Rather, we should offer supplemental screening in settings that collect data that will enable careful observational studies of outcomes in women who do and do not have supplemental tests.
Topics: breast, breast neoplasm screening, mammography, breast cancer, ultrasonography, magnetic resonance imaging
Editorials | 
Christine Laine, MD, MPH; Kay Dickersin, PhD; and Cynthia Mulrow, MD, MSc
This issue includes recommendations from the U.S. Preventive Services Task Force on screening for breast cancer in average-risk women. The editorialists discuss the recommendation as well as the firestorm after the 2009 recommendation. They emphasize that we must turn attention and resources to gathering evidence to fill important gaps in knowledge about breast cancer so that women, along with their health care providers, can make the best decisions to reduce risk for disease-related morbidity and mortality.
Topics: breast neoplasm screening, breast cancer
Editorials | 
Albert L. Siu, MD, MSPH; Kirsten Bibbins-Domingo, PhD, MD, MAS; David C. Grossman, MD, MPH; Michael L. LeFevre, MD, MSPH, on behalf of the U.S. Preventive Services Task Force
This issue includes updated recommendations from the U.S. Preventive Services Task Force on screening mammography for breast cancer. Task Force members discuss the recommendation statement and the strong emerging convergence among groups who have recently issued evidence-based guidelines, which should give the public confidence in the science that supports mammography screening.
Topics: breast neoplasm screening
Original Research | 
Jeanette Birnbaum, PhD, MPH; Vijayakrishna K. Gadi, MD, PhD; Elan Markowitz; and Ruth Etzioni, PhD
Background:Mammography trials, which are the primary sources of evidence for screening benefit, were conducted decades ago. Whether advances in systemic therapies have rendered previously observed benefits of screening less significant is unknown. Objective:To compare the outcomes of breast cancer screening trials had they been conducted using contemporary systemic treatments with outcomes of trials conducted with previously used treatments. Design:Computer simulation model of 3 virtual screening trials with similar reductions in advanced-stage cancer cases but reflecting treatment patterns in 1975 (prechemotherapy era), 1999, or 2015 (treatment according to receptor status). Data Sources:Meta-analyses of screening and treatment trials; study of dissemination of primary systemic treatments; SEER (Surveillance, Epidemiology, and End Results) registry. Target Population:U.S. women aged 50 to 74 years. Time Horizon:10 and 25 years. Perspective:Population. Intervention:Mammography, chemotherapy, tamoxifen, aromatase inhibitors, and trastuzumab. Outcome Measures:Breast cancer mortality rate ratio (MRR) and absolute risk reduction (ARR) obtained by the difference in cumulative breast cancer mortality between control and screening groups. Results of Base-Case Analysis:At 10 years, screening in a 1975 trial yielded an MRR of 90% and an ARR of 5 deaths per 10 000 women. A 2015 screening trial yielded a 10-year MRR of 90% and an ARR of 3 deaths per 10 000 women. Results of Sensitivity Analysis:Greater reductions in advanced-stage disease yielded a greater screening effect, but MRRs remained similar across trials. However, ARRs were consistently lower under contemporary treatments. When contemporary treatments were available only for early-stage cases, the MRR was 88%. Limitation:Disease models simplify reality and cannot capture all breast cancer subtypes. Conclusion:Advances in systemic therapies for breast cancer have not substantively reduced the relative benefits of screening but have likely reduced the absolute benefits because of their positive effect on breast cancer survival. Primary Funding Source:University of Washington and National Cancer Institute.
Topics: mortality, breast cancer, breast neoplasm screening, mammography, sensitivity analysis, chemotherapy regimen
Original Research | 
Diana L. Miglioretti, PhD; Jane Lange, PhD; Jeroen J. van den Broek, MSc; Christoph I. Lee, MD, MSHS; Nicolien T. van Ravesteyn, PhD; Dominique Ritley, MPH; Karla Kerlikowske, MD; Joshua J. Fenton, MD, MPH; Joy Melnikow, MD, MPH; Harry J. de Koning, PhD; and Rebecca A. Hubbard, PhD
Includes: Supplemental Content
Background:Estimates of risk for radiation-induced breast cancer from mammography screening have not considered variation in dose exposure or diagnostic work-up after abnormal screening results. Objective:To estimate distributions of radiation-induced breast cancer incidence and mortality from digital mammography screening while considering exposure from screening and diagnostic mammography and dose variation among women. Design:2 simulation-modeling approaches. Setting:U.S. population. Patients:Women aged 40 to 74 years. Intervention:Annual or biennial digital mammography screening from age 40, 45, or 50 years until age 74 years. Measurements:Lifetime breast cancer deaths averted (benefits) and radiation-induced breast cancer incidence and mortality (harms) per 100 000 women screened. Results:Annual screening of 100 000 women aged 40 to 74 years was projected to induce 125 breast cancer cases (95% CI, 88 to 178) leading to 16 deaths (CI, 11 to 23), relative to 968 breast cancer deaths averted by early detection from screening. Women exposed at the 95th percentile were projected to develop 246 cases of radiation-induced breast cancer leading to 32 deaths per 100 000 women. Women with large breasts requiring extra views for complete examination (8% of population) were projected to have greater radiation-induced breast cancer risk (266 cancer cases and 35 deaths per 100 000 women) than other women (113 cancer cases and 15 deaths per 100 000 women). Biennial screening starting at age 50 years reduced risk for radiation-induced cancer 5-fold. Limitation:Life-years lost from radiation-induced breast cancer could not be estimated. Conclusion:Radiation-induced breast cancer incidence and mortality from digital mammography screening are affected by dose variability from screening, resultant diagnostic work-up, initiation age, and screening frequency. Women with large breasts may have a greater risk for radiation-induced breast cancer. Primary Funding Source:Agency for Healthcare Research and Quality, U.S. Preventive Services Task Force, National Cancer Institute.
Topics: breast cancer, mammography, digital, breast, mortality
Original Research | 
Jeanne S. Mandelblatt, MD, MPH; Natasha K. Stout, PhD; Clyde B. Schechter, MA, MD; Jeroen J. van den Broek, MS; Diana L. Miglioretti, PhD; Martin Krapcho, BS; Amy Trentham-Dietz, PhD, MS; Diego Munoz, PhD, MS; Sandra J. Lee, ScD; Donald A. Berry, PhD; Nicolien T. van Ravesteyn, PhD; Oguzhan Alagoz, PhD; Karla Kerlikowske, MD; Anna N.A. Tosteson, ScD; Aimee M. Near, MPH; Amanda Hoeffken, MPH; Yaojen Chang, DrPH, MS, MPH; Eveline A. Heijnsdijk, PhD; Gary Chisholm, MS; Xuelin Huang, PhD; Hui Huang, MS; Mehmet Ali Ergun, MSc; Ronald Gangnon, PhD; Brian L. Sprague, PhD; Sylvia Plevritis, PhD; Eric Feuer, PhD; Harry J. de Koning, MD, PhD; and Kathleen A. Cronin, PhD, MPH
Background:Controversy persists about optimal mammography screening strategies. Objective:To evaluate screening outcomes, taking into account advances in mammography and treatment of breast cancer. Design:Collaboration of 6 simulation models using national data on incidence, digital mammography performance, treatment effects, and other-cause mortality. Setting:United States. Patients:Average-risk US female population and subgroups with varying risk, breast density, or comorbidity. Intervention:Eight strategies differing by age at which screening starts (40, 45, or 50 years) and screening interval (annual, biennial, and hybrid [annual for women in their 40s and biennial thereafter]). All strategies assumed 100% adherence and stopped at age 74 years. Measurements:Benefits (breast cancer–specific mortality reduction, breast cancer deaths averted, life-years, and quality-adjusted life-years); number of mammograms used; harms (false-positive results, benign biopsies, and overdiagnosis); and ratios of harms (or use) and benefits (efficiency) per 1000 screens. Results:Biennial strategies were consistently the most efficient for average-risk women. Biennial screening from age 50 to 74 years avoided a median of 7 breast cancer deaths versus no screening; annual screening from age 40 to 74 years avoided an additional 3 deaths, but yielded 1988 more false-positive results and 11 more overdiagnoses per 1000 women screened. Annual screening from age 50 to 74 years was inefficient (similar benefits, but more harms than other strategies). For groups with a 2- to 4-fold increased risk, annual screening from age 40 years had similar harms and benefits as screening average-risk women biennially from 50 to 74 years. For groups with moderate or severe comorbidity, screening could stop at age 66 to 68 years. Limitation:Other imaging technologies, polygenic risk, and nonadherence were not considered. Conclusion:Biennial screening for breast cancer is efficient for average-risk populations. Decisions about starting ages and intervals will depend on population characteristics and the decision makers' weight given to the harms and benefits of screening. Primary Funding Source:National Institutes of Health.
Topics: mammography, breast cancer, breast neoplasm screening, breast density, mammography, digital, cancer, mortality, comorbidity
In this issue, Birnbaum and colleagues evaluate whether the availability of efficient adjuvant and chemotherapy treatments would have changed reductions in the risk for breast cancer death reported by randomized trials on breast cancer screening. The editorialist discusses these results and the implications for women having breast cancer screening.
Topics: breast neoplasm screening, breast cancer
Topics: breast neoplasm screening
Ideas and Opinions | 
Mosoka Fallah, PhD, MPH; Bernice Dahn, MD, MPH; Tolbert G. Nyenswah, Esq, MPH; Moses Massaquoi, MD, MPH; Laura A. Skrip, MPH; Dan Yamin, PhD; Martial Ndeffo Mbah, PhD; Netty Joe, MD; Siedoh Freeman, MD; Thomas Harris, BA; Zinnah Benson, BBA; and Alison P. Galvani, PhD
In Liberia, programs based on community engagement were effective in controlling the Ebola virus disease epidemic.
Topics: ebola virus disease, liberia, community
Ideas and Opinions | 
David U. Himmelstein, MD; and Russell S. Phillips, MD
Should asymptomatic patients schedule annual visits with their physicians? Many experts and some professional organizations say no and cite evidence-based studies as the reason why. This article examines those studies and reaches more nuanced conclusions.
Topics: primary care physicians, health evaluation, primary health care, elderly, evidence-based practice, cochrane collaboration, health disparity, professional organizations, multiphasic screening, add-on code, physician-patient relations, mortality, angiotensin-converting enzyme inhibitors, screening test, inspection, laboratory test finding, asymptomatic diseases, breast cancer, manual pelvic examination, visual acuity testing, exertional dyspnea, sexually transmitted diseases, spirometry, tonometry, urinalysis, vaginal smears, audiometry, follow-up, laboratory techniques and procedures, mammography, melanoma, myopia, pain, electrocardiogram, statins, edema, diagnostic radiologic examination, chest pain, blood test, headache
Letters | 
Eirion Slade, MPhys; Henry Drysdale, BSc; Ben Goldacre, MBBS, on behalf of the COMPare Team
Members of the Centre for Evidence-Based Medicine Outcome Monitoring Project (COMPare) express their concerns about switched or incompletely reported outcomes in 2 trials published in Annals. In the accompanying response, the Editors describe their procedures for reviewing reports of clinical trials and potential reasons for the discrepancies noted by COMPare.
Letters | 
The Editors
Members of the Centre for Evidence-Based Medicine Outcome Monitoring Project (COMPare) express their concerns about switched or incompletely reported outcomes in 2 trials published in Annals. In the accompanying response, the Editors describe their procedures for reviewing reports of clinical trials and potential reasons for the discrepancies noted by COMPare.
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