This systematic evidence review is an update of evidence for the U.S. Preventive Services Task Force (USPSTF) recommendation on breast cancer screening for average-risk women (1). In 2002, on the basis of results of a previous review (2, 3), the USPSTF recommended mammography screening, with or without clinical breast examination (CBE), every 1 to 2 years for women aged 40 years or older. They concluded that the evidence was insufficient to recommend for or against routine CBE alone and for or against teaching or performing routine breast self-examination (BSE). Breast cancer is the most frequently diagnosed noncutaneous cancer and the second leading cause of cancer deaths among women in the United States (4). In 2008, an estimated 182460 cases of invasive and 67770 cases of noninvasive breast cancer were diagnosed, and 40480 women died of breast cancer (4). Incidence increases with age, and the probability of a woman developing breast cancer is 1 in 69 in her 40s, 1 in 38 in her 50s, and 1 in 27 in her 60s (5). Data suggest that incidence has stabilized in recent years (68) and mortality has decreased since 1990 (9, 10) because of many factors, including screening (11). In 2005, 68% of women aged 40 to 65 years had screening mammography within the previous 2 years in the United States (4). Breast cancer is known to have an asymptomatic phase that can be detected with mammography. Mammography screening is sensitive (77% to 95%), specific (94% to 97%), and acceptable to most women (2). It is done by using either plain film or digital technologies, although the shift to digital is ongoing. Contrast-enhanced magnetic resonance imaging (MRI) has traditionally been used to evaluate women who have already received a diagnosis of breast cancer. Recommendations for its use in screening pertain to certain high-risk groups only (12). If a woman has an abnormal mammographic finding on screening or a concerning finding on physical examination, additional imaging and biopsy may be recommended. Additional imaging may consist of diagnostic mammography or mammography done with additional or special views, targeted breast ultrasonography, or breast MRI (13, 14). Additional imaging may help classify the lesion as a benign or suspicious finding to determine the need for biopsy. Biopsy techniques vary in the level of invasiveness and amount of tissue acquired, which affects yield and patient experience. We focus on new studies and evidence gaps that were unresolved at the time of the 2002 USPSTF recommendation. These include the effectiveness of mammography screening in decreasing breast cancer mortality among average-risk women aged 40 to 49 years and 70 years or older; the effectiveness of CBE and BSE in decreasing breast cancer mortality among women of any age; and the magnitude of harms of screening with mammography, CBE, and BSE. Methods The USPSTF and Agency for Healthcare Research and Quality (AHRQ) developed the key questions that guided our update. Investigators created an analytic framework incorporating the key questions and outlining the patient population, interventions, outcomes, and harms of the screening process (Appendix Figure 1). The target population includes women without preexisting breast cancer and not considered to be at high risk for breast cancer on the basis of extensive family history of breast or ovarian cancer or other personal risk factors, such as abnormal breast pathology or deleterious genetic mutations. Harms include radiation exposure, pain during procedures, patient anxiety and other psychological responses, consequences of false-positive and false-negative test results, and overdiagnosis. Overdiagnosis refers to women receiving a diagnosis of invasive or noninvasive breast cancer who had abnormal lesions that were unlikely to become clinically evident during their lifetimes in the absence of screening (15). Overdiagnosis may have a greater effect on women with shorter life expectancies because of age or comorbid conditions. Appendix Figure 1. Analytic framework and key questions. BSE = breast self-examination; CBE = clinical breast examination; MRI = magnetic resonance imaging. *Includes radiation exposure, pain, psychological responses, false-positive and false-negative test results, and overdiagnosis. Data Sources and Searches We searched the Cochrane Central Register of Controlled Trials and Cochrane Database of Systematic Reviews (through the fourth quarter of 2008) and MEDLINE (1 January 2001 to 1 December 2008) for relevant studies and meta-analyses (16). We also conducted secondary referencing by manually reviewing reference lists of key articles and searching citations by using Web of Science (17). Appendix Figure 2 shows our search results. Appendix Figure 2. Literature search and selection. BSE = breast self-examination; CBE = clinical breast examination; SR = systematic review; USPSTF = U.S. Preventive Services Task Force. *Cochrane databases include the Cochrane Central Register of Controlled Trials and the Cochrane Database of Systematic Reviews. Other sources include reference lists and studies suggested by experts. Some articles are included for more than 1 key question. Study Selection We selected studies on the basis of inclusion and exclusion criteria developed for each key question (16). To determine the effectiveness of screening, we included randomized, controlled trials (RCTs) and updates to previously published trials of screening with mammography (film and digital), MRI, CBE, or BSE with breast cancer mortality outcomes published since 2001. One trial was translated into English from Russian for this update (18). We also reviewed meta-analyses that included studies with mortality data. We excluded studies other than controlled trials and systematic reviews or those without breast cancer mortality as an outcome. We determined harms of screening by using evidence from several study designs and data sources. For mammography, we focused our searches on recently published systematic reviews and meta-analyses of the harms previously described. We also conducted specific searches for primary studies published more recently than the included systematic reviews and meta-analyses. In addition, we evaluated data from the Breast Cancer Surveillance Consortium (BCSC), which is a collaborative network of 5 mammography registries and 2 affiliated sites with linkages to pathology and tumor registries across the United States that is sponsored by the National Cancer Institute (19, 20). These data draw from community samples that are representative of the larger, national population and may be more applicable to current practice in the United States than other published sources. Data include a mix of film and digital mammography. For harms of CBE and BSE, we reviewed screening trials of these procedures that reported potential adverse effects, used recently published systematic reviews, and conducted focused searches. Data Extraction and Quality Assessment We extracted details about the patient population, study design, analysis, follow-up, and results. By using predefined criteria developed by the USPSTF (21), 2 investigators rated the quality of each study as good, fair, or poor and resolved discrepancies by consensus. We included only systematic reviews rated as good quality in the report and RCTs rated as fair or good quality in the meta-analysis. Data Synthesis and Analysis Meta-analysis of Mammography Trials We updated the 2002 meta-analysis to include new findings from published trials of mammography screening compared with control participants for women aged 40 to 49 years that reported relative risk (RR) reduction in breast cancer mortality. We conducted similar updates for other age groups for context. We used breast cancer mortality results from trials to estimate the pooled RR. We calculated estimates from a random-effects model under the Bayesian data analytic framework by using the RBugs package in R (22, 23), the same model as that used in the previous report (2). The Appendix provides additional details. We used funnel plots to assess publication bias and L'Abb plots to assess heterogeneity. Analysis of BCSC Data We obtained data from 600830 women aged 40 years or older undergoing routine mammography screening from 2000 to 2005 at the BCSC sites from the BCSC Statistical Coordinating Center and stratified the data by age in decades. Routine screening was defined as having at least 1 mammogram within the previous 2 years, which is consistent with current USPSTF recommendations. For women who had several mammograms during the study, 1 result was randomly selected to be included in the calculations. These data constitute selected BCSC data intended to represent the experience of a cohort of regularly screened women without preexisting breast cancer or abnormal physical findings. Variables include the numbers of positive and negative mammography results and, of these, the number of true-negative and false-negative results based on follow-up data within 1 year of mammography screening. A positive mammography result was defined according to standardized terminology and assessments of the American College of Radiology Breast Imaging Reporting and Data System (BI-RADS) manual used by the BCSC (24). These include 4 categories: needs additional evaluation (category 0), probably benign with a recommendation for immediate follow-up (category 3), suspicious (category 4), or highly suggestive of cancer (category 5) (25). For women who had a positive screening mammography result, additional data included the number of women undergoing additional imaging and biopsy; diagnoses, including invasive cancer and ductal carcinoma in situ; and negative results. We considered additional imaging procedures and biopsies done within 60 days of the screening mammography to be related to screening. From these data, we calculated age-specific rates (numbers per 1000 women per round) of invasive brea
[1]
J. Habbema,et al.
Age-specific reduction in breast cancer mortality by screening: an analysis of the results of the Health Insurance Plan of Greater New York study.
,
1986,
Journal of the National Cancer Institute.
[2]
L. Tabár,et al.
Efficacy of breast cancer screening by age. New results swedish two‐county trial
,
1995,
Cancer.
[3]
K. Kerlikowske,et al.
Breast Cancer Surveillance Consortium: a national mammography screening and outcomes database.
,
1997,
AJR. American journal of roentgenology.
[4]
I. Olivotto,et al.
False positive rate of screening mammography.
,
1998,
The New England journal of medicine.
[5]
A. Mushlin,et al.
Estimating the accuracy of screening mammography: a meta-analysis.
,
1998,
American journal of preventive medicine.
[6]
Ten-year risk of false positive screening mammograms and clinical breast examinations.
,
1998,
Journal of nurse-midwifery.
[7]
J. Elmore,et al.
Ten-year risk of false positive screening mammograms and clinical breast examinations.
,
1998,
The New England journal of medicine.
[8]
V. Semiglazov,et al.
[Interim results of a prospective randomized study of self-examination for early detection of breast cancer (Russia/St.Petersburg/WHO)].
,
1999,
Voprosy onkologii.
[9]
L. Smeeth,et al.
Numbers needed to treat derived from meta-analyses—sometimes informative, usually misleading
,
1999,
BMJ.
[10]
A. Miller,et al.
Canadian National Breast Screening Study-2: 13-year results of a randomized trial in women aged 50-59 years.
,
2000,
Journal of the National Cancer Institute.
[11]
L. Tabár,et al.
The Swedish Two-County Trial twenty years later. Updated mortality results and new insights from long-term follow-up.
,
2000,
Radiologic clinics of North America.
[12]
N. Baxter.
Preventive health care, 2001 update: should women be routinely taught breast self-examination to screen for breast cancer?
,
2001,
CMAJ : Canadian Medical Association journal = journal de l'Association medicale canadienne.
[13]
C. Drossaert,et al.
Does mammographic screening and a negative result affect attitudes towards future breast screening?
,
2001,
Journal of medical screening.
[14]
C. Mulrow,et al.
Current methods of the US Preventive Services Task Force: a review of the process.
,
2001,
American journal of preventive medicine.
[15]
Roberta M Ray,et al.
Randomized trial of breast self-examination in Shanghai: final results.
,
2002,
Journal of the National Cancer Institute.
[16]
A. Berg,et al.
Screening for Breast Cancer: Recommendations and Rationale
,
2002,
Annals of Internal Medicine.
[17]
T. To,et al.
The Canadian National Breast Screening Study-1: Breast Cancer Mortality after 11 to 16 Years of Follow-up: A Randomized Screening Trial of Mammography in Women Age 40 to 49 Years
,
2002,
Annals of Internal Medicine.
[18]
S. Woolf,et al.
Breast Cancer Screening: A Summary of the Evidence for the U.S. Preventive Services Task Force
,
2002,
Annals of Internal Medicine.
[19]
Ingvar Andersson,et al.
Long-term effects of mammography screening: updated overview of the Swedish randomised trials
,
2002,
The Lancet.
[20]
Evis Sala,et al.
The Gothenburg Breast Screening Trial
,
2003,
Cancer.
[21]
Alfons G H Kessels,et al.
The additional diagnostic value of ultrasonography in the diagnosis of breast cancer.
,
2003,
Archives of internal medicine.
[22]
E. A. Paul,et al.
Breast self-examination and death from breast cancer: a meta-analysis
,
2003,
British Journal of Cancer.
[23]
L. Tabár,et al.
Quantifying the potential problem of overdiagnosis of ductal carcinoma in situ in breast cancer screening.
,
2003,
European journal of cancer.
[24]
Isabelle Bedrosian,et al.
Changes in the surgical management of patients with breast carcinoma based on preoperative magnetic resonance imaging
,
2003,
Cancer.
[25]
Karla Kerlikowske,et al.
Comparison of screening mammography in the United States and the United kingdom.
,
2003,
JAMA.
[26]
V. Semiglazov,et al.
[Results of a prospective randomized investigation [Russia (St.Petersburg)/WHO] to evaluate the significance of self-examination for the early detection of breast cancer].
,
2003,
Voprosy onkologii.
[27]
Solveig Hofvind,et al.
The cumulative risk of a false‐positive recall in the Norwegian Breast Cancer Screening Program
,
2004,
Cancer.
[28]
Jan Mæhlen,et al.
Incidence of breast cancer in Norway and Sweden during introduction of nationwide screening: prospective cohort study
,
2004,
BMJ : British Medical Journal.
[29]
V. Semiglazov,et al.
The role of breast self-examination in early breast cancer detection (results of the 5-years USSR/WHO randomized study in Leningrad)
,
1992,
European Journal of Epidemiology.
[30]
L. Tabár,et al.
Overdiagnosis and overtreatment of breast cancer: Estimates of overdiagnosis from two trials of mammographic screening for breast cancer
,
2005,
Breast Cancer Research.
[31]
H. D. de Koning,et al.
Overdiagnosis and overtreatment of breast cancer: Microsimulation modelling estimates based on observed screen and clinical data
,
2005,
Breast Cancer Research.
[32]
D. Berry,et al.
Effect of screening and adjuvant therapy on mortality from breast cancer
,
2005
.
[33]
J. Austoker,et al.
The psychological impact of mammographic screening. A systematic review
,
2005,
Psycho-oncology.
[34]
Deborah Schrag,et al.
Annual report to the nation on the status of cancer, 1975-2002, featuring population-based trends in cancer treatment.
,
2005,
Journal of the National Cancer Institute.
[35]
N. Day.
Overdiagnosis and breast cancer screening
,
2005,
Breast Cancer Research.
[36]
S. Moss.
Overdiagnosis and overtreatment of breast cancer: Overdiagnosis in randomised controlled trials of breast cancer screening
,
2005,
Breast Cancer Research.
[37]
D. Tripathy.
Targeted Therapies in Breast Cancer
,
2005,
The breast journal.
[38]
Gary R Cutter,et al.
Association between mammography timing and measures of screening performance in the United States.
,
2005,
Radiology.
[39]
A. Miller,et al.
Breast screening in the emerging world: high prevalence of breast cancer in Cairo.
,
2005,
Breast.
[40]
E. Feuer,et al.
SEER Cancer Statistics Review, 1975-2003
,
2006
.
[41]
Ingvar Andersson,et al.
Rate of over-diagnosis of breast cancer 15 years after end of Malmö mammographic screening trial: follow-up study
,
2006,
BMJ : British Medical Journal.
[42]
Michael Waller,et al.
Effect of mammographic screening from age 40 years on breast cancer mortality at 10 years' follow-up: a randomised controlled trial
,
2006,
The Lancet.
[43]
S. Rosso,et al.
Estimate of overdiagnosis of breast cancer due to mammography after adjustment for lead time. A service screening study in Italy
,
2006,
Breast Cancer Research.
[44]
Paola Pisani,et al.
Outcome of screening by clinical examination of the breast in a trial in the Philippines
,
2006,
International journal of cancer.
[45]
Karla Kerlikowske,et al.
Performance benchmarks for screening mammography.
,
2006,
Radiology.
[46]
S. Duffy,et al.
Overdiagnosis, Sojourn Time, and Sensitivity in the Copenhagen Mammography Screening Program
,
2006,
The breast journal.
[47]
J. Elmore,et al.
Breast self-examination: self-reported frequency, quality, and associated outcomes.
,
2006,
Journal of cancer education : the official journal of the American Association for Cancer Education.
[48]
A. Whittemore,et al.
Medical radiation exposure and breast cancer risk: Findings from the Breast Cancer Family Registry
,
2007,
International journal of cancer.
[49]
D. Miglioretti,et al.
Declines in invasive breast cancer and use of postmenopausal hormone therapy in a screening mammography population.
,
2007,
Journal of the National Cancer Institute.
[50]
Eric J Feuer,et al.
The decrease in breast-cancer incidence in 2003 in the United States.
,
2007,
The New England journal of medicine.
[51]
Noel T Brewer,et al.
Systematic Review: The Long-Term Effects of False-Positive Mammograms
,
2007,
Annals of Internal Medicine.
[52]
Manfred S. Green,et al.
Routine screening mammography in women older than 74 years: a review of the available data.
,
2007,
Maturitas.
[53]
Sankey V. Williams,et al.
Screening Mammography in Women 40 to 49 Years of Age: A Systematic Review for the American College of Physicians
,
2007,
Annals of Internal Medicine.
[54]
K. McMasters,et al.
Trends in mammography and clinical breast examination: a population-based study.
,
2007,
The Journal of surgical research.
[55]
M. Yaffe,et al.
American Cancer Society Guidelines for Breast Screening with MRI as an Adjunct to Mammography
,
2007
.
[56]
G. Hortobagyi,et al.
Mammography before diagnosis among women age 80 years and older with breast cancer.
,
2008,
Journal of clinical oncology : official journal of the American Society of Clinical Oncology.
[57]
J. Bertino.
The Journal of Clinical Oncology: The Initial Years
,
2008
.
[58]
S. Jones.
Regular self-examination or clinical examination for early detection of breast cancer.
,
2008,
International journal of epidemiology.
[59]
H. Nelson,et al.
Screening for Breast Cancer: Systematic Evidence Review Update for the U. S. Preventive Services Task Force
,
2009
.