Paper
Screening for Breast Cancer: An Update for the U.S. Preventive Services Task Force
Published Nov 17, 2009 ·
Annals of Internal Medicine
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Abstract
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
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