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Clinical Guidelines |

Screening Mammography in Women 40 to 49 Years of Age: A Systematic Review for the American College of Physicians FREE

Katrina Armstrong, MD, MSCE; Elizabeth Moye, BA; Sankey Williams, MD; Jesse A. Berlin, ScD; and Eileen E. Reynolds, MD
[+] Article and Author Information

From the University of Pennsylvania, Philadelphia, Pennsylvania; Johnson & Johnson Pharmaceutical Research & Development, Raritan, New Jersey; and Beth Israel Deaconess Medical Center, Boston, Massachusetts.


Acknowledgments: The authors thank Faun Carter and Melani Sherman, who provided valuable administrative assistance.

Potential Financial Conflicts of Interest: Employment: J.A. Berlin (Johnson & Johnson Pharmaceutical Research & Development); Stock ownership or options (other than mutual funds): J.A. Berlin (Johnson & Johnson Pharmaceutical Research & Development).

Requests for Single Reprints: Katrina Armstrong, MD, MSCE, University of Pennsylvania, 1204 Blockley Hall, 423 Guardian Drive, Philadelphia, PA 19104.

Current Author Addresses: Dr. Armstrong: University of Pennsylvania, 1204 Blockley Hall, 423 Guardian Drive, Philadelphia, PA 19104.

Ms. Moye: 435 East 30th Street, #518, New York, NY 10016.

Dr. Williams: University of Pennsylvania, 1220 Blockley Hall, 423 Guardian Drive, Philadelphia, PA 19104-6021.

Dr. Berlin: 1125 Trenton-Harbourton Road, P.O. Box 200, M/S 67, Titusville, NJ 08560.

Dr. Reynolds: Beth Israel Deaconess Medical Center, 330 Brookline Avenue, Boston, MA 02215.


Ann Intern Med. 2007;146(7):516-526. doi:10.7326/0003-4819-146-7-200704030-00008
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Background: The risks and benefits of mammography screening among women 40 to 49 years of age remain an important issue for clinical practice.

Purpose: To evaluate the evidence about the risks and benefits of mammography screening for women 40 to 49 years of age.

Data Sources: English-language publications in MEDLINE (1966–2005), Pre-MEDLINE, and the Cochrane Central Register of Controlled Trials and references of selected studies through May 2005.

Study Selection: Previous systematic reviews; randomized, controlled trials; and observational studies.

Data Extraction: Two independent reviewers.

Data Synthesis: In addition to publications from the original mammography trials, 117 studies were included in the review. Meta-analyses of randomized, controlled trials demonstrate a 7% to 23% reduction in breast cancer mortality rates with screening mammography in women 40 to 49 years of age. Screening mammography is associated with an increased risk for mastectomy but a decreased risk for adjuvant chemotherapy and hormone therapy. The risk for death due to breast cancer from the radiation exposure involved in mammography screening is small and is outweighed by a reduction in breast cancer mortality rates from early detection. Rates of false-positive results are high (20% to 56% after 10 mammograms), but false-positive results have little effect on psychological health or subsequent mammography adherence. Although many women report pain at the time of the mammography, few see pain as a deterrent to future screening. Evidence about the effect of negative screening mammography on psychological well-being or the subsequent clinical presentation of breast cancer is insufficient.

Limitations: Few randomized, controlled trials assessed the risks of screening, and the literature search was completed in 2005.

Conclusions: Although few women 50 years of age or older have risks from mammography that outweigh the benefits, the evidence suggests that more women 40 to 49 years of age have such risks.

Key Summary Points

Meta-analyses of randomized, controlled trials demonstrate a 7% to 23% reduction in breast cancer mortality rates from screening mammography in women 40 to 49 years of age.

Screening mammography is associated with an increased risk for mastectomy but a decreased risk for adjuvant chemotherapy and hormone therapy.

The risk for radiation is small (30 to 200 breast cancer deaths occurred in an annual screening of 100 000 women 40 to 49 years of age).

Rates of false-positive mammograms are high (20% to 56% after 10 mammograms), but false-positive results have little effect on psychological health or subsequent mammography adherence.

Although many women report pain at the time of mammography, few see pain as a deterrent to future screening.

Breast cancer risk varies among women in their 40s and affects the absolute reduction in rates of breast cancer mortality and the absolute risk for false-positive results on screening mammography.

Several decades after the first guidelines for breast cancer screening were published, the routine use of mammography among asymptomatic women remains a topic of considerable debate (12). This debate surfaces occasionally on screening women 50 years of age or older but persists regularly for screening women in their 40s (34). The persistence of this controversy suggests a level of unease with our current understanding of the benefits and risks of mammography and with how this understanding has been translated into screening recommendations.

Understanding the risks and benefits of screening mammography among women in their 40s is important because of the critical position that breast cancer holds in that age group. In the United States, breast cancer is one of the most common causes of death for women in their 40s. In 2002, almost 5000 women between 40 and 49 years of age died of breast cancer, compared with the 6800 women who died of heart disease or 1500 women who died of HIV (5). However, despite the relative importance of breast cancer in this age group, the burden of breast cancer among women in their 40s is low for a population-based screening program. More than 98% of women will not develop breast cancer between 40 and 50 years of age, but they will be subject to the risks of population-based screening. Of the 44 000 women who die of breast cancer each year, fewer than one fifth received their diagnoses between the ages of 40 and 49 years (67).

We describe the results of a systematic review of the benefits and risks for screening mammography among women 40 to 49 years of age. Currently, 8 published meta-analyses discuss the effect of mammography screening in women 40 to 49 years of age on breast cancer mortality rates (816). All but 1 demonstrate a reduction in mortality rates from screening mammography. Thus, we did not perform another meta-analysis of the effect of screening mammography on breast cancer mortality rates, but we reviewed briefly the benefits of mammography screening derived from published screening trials and meta-analyses. In addition, we focused on 2 areas that are less well-studied but may affect recommendations about screening mammography among women in this age group: 1) risks of mammography screening and 2) variation in the risks and benefits of mammography according to an individual woman's characteristics.

Data Sources

We created a framework of the potential risks and benefits of screening mammography to guide the literature search (Figure). On the basis of the framework, we searched MEDLINE, Pre-MEDLINE, and the Cochrane Central Register of Controlled Trials for English-language publications. We conducted the initial searches in spring 2004 and updated them in May 2005. General search strategies included Medical Subject Headings (MeSH) terms mammography or breast neoplasms and mass screening, as well as the keywords mammography, screening, and breast cancer. We conducted additional searches for each individual risk or benefit by using appropriate keywords and MeSH terms. We reviewed the references of all selected articles to identify additional relevant articles.

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Figure.
Risks and benefits of screening mammography.

Numbers correspond to the risks and benefits outlined in the Table.

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Study Selection

Although previous systematic reviews have largely focused on randomized, controlled trials of mammography screening to quantify the benefit of screening on breast cancer mortality rates, most evidence about risks and other benefits of mammography is derived from observational studies, primarily prospective cohort studies (Table). Thus, we included a wide range of study designs in our review, with the included studies depending on the question and the available evidence. We used meta-analyses to assess the effect of mammography screening on breast cancer mortality rates and the risk for a false-positive mammogram at a single screening; randomized, controlled trials and prospective cohort studies to assess the effect of mammography on breast cancer treatment and the cumulative risk for a false-positive mammogram; and both prospective and cross-sectional observational studies to assess the other risks of mammography. We excluded case series and ecological designs for all risks except for ductal carcinoma in situ (DCIS), because most published data on DCIS outcomes are derived from these study designs. In addition, we reviewed the available publications from the 8 original mammography trials and the published simulation models of the effect of radiation from mammography screening. When possible, we focused on evidence from studies of screening mammography in women in their 40s or analyses of this age group within larger cohorts. When this was not possible, we used studies of screening mammography in older women. In the case of multiple publications from the same study, we included only the most recent publication in our analysis.

Table Jump PlaceholderTable.  Risks and Benefits of Screening Mammography

For study selection, a study investigator reviewed abstracts of all primary research articles to determine whether the full-text article should be retrieved. We retrieved 873 full-text articles, and 2 investigators reviewed them. In addition to the publications from the original trials, 117 of these articles met inclusion criteria.

Data Extraction and Quality Assessment

Two investigators abstracted information about the study design, setting, study sample, measures, analysis, and results. When needed, we contacted authors to clarify questions about study design or results. We evaluated study quality by using the approach proposed by the Centre for Evidence-Based Medicine (http://www.cebm.net/levels_of_evidence.asp) (Appendix Table 1). The lead investigator adjudicated any disagreements between the reviewers about article content and quality.

Table Jump PlaceholderAppendix Table 1.  Evidence-Based Medicine Review Score: Criteria Used to Assess Study Quality*
Role of the Funding Source

The review was conducted under contract with the American College of Physicians. The funding source had no role in the collection, analysis, or interpretation of the data or in the decision to submit the article for publication.

Benefits
Breast Cancer Mortality

Many meta-analyses have combined the results of major mammography screening trials to assess the effect of screening on breast cancer mortality rates. The latest meta-analysis demonstrated that screening mammography every 1 to 2 years in women 40 to 49 years of age results in a 15% decrease in breast cancer mortality after 14 years of follow-up (relative risk, 0.85 [95% CI, 0.73 to 0.99]) (12). This effect size is very similar to that reported by most previous meta-analyses of women 40 to 49 years of age (8, 10, 1314, 16). It is smaller than the 22% reduction seen among women 50 years of age or older (relative risk, 0.78 [CI, 0.70 to 0.87]) (12). The meta-analysis did not include the recently published results of the United Kingdom trial of annual mammography screening in 160 921 women in their 40s (relative risk, 0.83 [CI, 0.66 to 1.04]) (17). However, this estimate is so similar to the results of the meta-analyses that the findings are unlikely to substantively change. Nevertheless, the effect of mammography screening on breast cancer mortality rates for women in their 40s remains controversial for several reasons. These reasons include concern about the quality of the trials that found mammography to have the largest benefit, the interval until the mortality rate reduction began, and the validity of death due to breast cancer as the primary end point (2). We review each issue in the following sections.

Study quality is important because high-quality studies are more likely to provide accurate estimates of the effect size. However, judging study quality is difficult because of imperfect reporting and lack of consensus on criteria for evaluating studies. Furthermore, high-quality studies are relatively uncommon. In the setting of screening mammography for women 40 to 49 years of age, previous meta-analyses differ in their assessment of study quality and study inclusion. The Cochrane meta-analysis (2) excluded all but 2 of the 8 trials that provided information about this age group (the Canadian trial and the Malmö trial). The most recent meta-analysis, which was from the U.S. Preventive Services Task Force (12), included all trials but the Edinburgh trial. Other meta-analyses have included all 8 trials (1011, 1314, 16). To a great extent, these differences arise from different levels of concern about inadequate or inconsistent information in study publications, including variation in the numbers of participants in sequential reports; differences in baseline characteristics among groups; and lack of information about randomization procedures, date of trial entry, and other study characteristics. Although many of these concerns cannot be fully resolved, recent analyses and critical reviews support the argument that none of the trials is sufficiently biased to necessitate exclusion from meta-analyses, with the possible exception of the Edinburgh trial, for which substantive evidence of failure of randomization persists (1821).

The reduction in breast cancer mortality rates with mammography screening does not begin for some time after initiation of screening. This delay occurs because breast cancer is not immediately fatal and women who do not undergo screening must begin to die of cancer before a reduction in mortality rates can be seen. For women 40 to 49 years of age at the initiation of screening, the reduction in breast cancer mortality rates can be measured after 6 years of follow-up and the effect size increases over time (8, 12). Thus, some women who begin screening in their 40s are older than 50 years of age when the reduction in breast cancer mortality rate begins. Although the precise contributions of screening in women 40 to 49 years of age and screening after a woman turned 50 years of age are difficult to determine, several analyses suggest that the most benefit is attributable to screening when women are between 40 and 49 years of age (8, 12).

Concern has been raised about the validity of death due to breast cancer as the primary end point in screening trials. Because differential misclassification of cause of death may bias study results and breast cancer treatment may increase rates of cardiovascular mortality, some investigators have suggested that overall death should be the primary end point (2). However, because the relative reduction in overall mortality rates with mammography will be much smaller than that in breast cancer mortality rates, trials of more than 1 million women would be necessary to detect a difference in overall mortality rates. Existing screening trials use strategies for minimizing misclassification of cause of death, including blinded review of deaths and sensitivity analyses using alternative sources for death classification (19).

The existing mammography screening trials have several other potential limitations for estimating the effect of mammography in community practice (22). Some biases may have resulted in an underestimate of the benefit of current screening programs, whereas others may have led to an overestimate. Mammography technology has improved since the 1960s, when the first trial was begun. However, differences in technology among trials have not been shown to be associated with the magnitude of benefit, and some of the larger estimates come from the earliest trials. Screening intervals and techniques were often less intensive in the trials than those that are currently recommended in the United States. Because most trials tested the effect of an invitation to screening rather than screening itself, many women in the intervention group did not undergo screening. In addition, some women in the control group had screening outside of the study protocol. This crossover biases the results of the trials toward showing no benefit of screening. Case–control studies, which measure the actual use of screening, and observational studies of screening programs generally find higher estimates of the benefit of mammography (2324). Women in the intervention group may have been more likely to undergo treatment at referral centers because these centers were connected to the screening programs, which may have led to improved treatment outcomes.

In summary, the body of evidence indicates that women who undergo screening mammography between 40 and 49 years of age are less likely to die of breast cancer than women who do not undergo screening mammography, although the magnitude of the effect is smaller than that among women 50 years of age or older. The mortality benefit is unlikely to be completely explained by biases in mammography screening trials or the effects of screening after the age of 49 years.

Breast Cancer Treatment Morbidity

Early detection may reduce the morbidity associated with breast cancer treatment by enabling the use of less aggressive therapies, for example, lumpectomy instead of mastectomy. However, more cases of cancer are detected in women who undergo screening than in women who do not undergo screening. Thus, the absolute effect of screening on breast cancer treatment is uncertain.

Five of the 8 screening trials reported data about breast cancer treatment in intervention and control groups (2529). In addition, 9 other studies assessed the effect of screening on breast cancer treatment (3039). Overall, these studies demonstrate that, because screening detects earlier-stage cancer, screen-detected cancer is more likely to be eligible for breast-conserving surgery and is less likely to be eligible for adjuvant chemotherapy and hormone therapy than cancer that is detected in some other way. However, differences in eligibility for breast-conserving surgery or chemotherapy do not always translate into differences in treatment (24, 3839). In addition, when considering the overall population of women who undergo screening, invitation to mammography screening is associated with absolute increases in the probabilities of mastectomy, lumpectomy, and radiation therapy because more cases of cancer are found (15). For example, in the Malmö trial, women in the screening group were 25% more likely to have a mastectomy and 24% more likely to have radiation therapy than women in the control group (15). However, rates of chemotherapy and hormone therapy remain lower in the screening group than in the control group.

Reassurance

Although clinical experience suggests that many women perceive the reassurance provided by a negative mammogram as a substantial benefit, we found few empirical data to support this effect. Studies exploring the overall psychological impact of screening generally found relatively little effect across the population, with a few studies suggesting improved psychological well-being after screening (4043).

Risks
Radiation

No studies directly measure the risk for cancer caused by radiation exposure from mammography screening. Any effect of screening radiation on breast cancer incidence is small and is difficult to separate from the effect of screening on breast cancer detection. Estimates of the risk for radiation from mammography are derived from cohort studies of other forms of radiation exposure, including high-dose exposures (over a short or prolonged period of time) and low-dose exposures from other sources (4468). In general, studies of low-dose exposures have been inconclusive, with some demonstrating a small increase in risk and others finding no association (44, 47, 54, 57). However, studies of high-dose exposures have found that women who were exposed to high levels of radiation have a statistically significantly increased risk for breast cancer, with relative risks ranging from 1.33 to 11.39 for exposures of 0.3 to 43.4 Gy (46, 52, 55, 59, 65, 6768). High-dose exposures that have been studied include radiation treatment, diagnostic radiography, and atomic bombs. The increase in risk seems to be larger with higher doses of exposure, younger age at exposure, and longer follow-up.

The mean glandular dose from 2-view mammography is approximately 4 to 5 mGy. A recent analysis of radiation dose in the United Kingdom trial of mammography screening in women 40 to 48 years of age found a mean glandular dose of 2.5 mGy for an oblique film and 2.0 mGy for a craniocaudal film (69). However, dosage varies among facilities and increases with breast density. If women 40 to 49 years of age are screened every year and an estimated 20% experience a false-positive test result requiring additional radiographies, the average cumulative exposure from screening during the decade will be around 60 mGy.

Appendix Table 2 details evidence from these studies on the risk for radiation.

Overdiagnosis

Overdiagnosis occurs when screening identifies cancer that would not have become clinically evident during a patient's lifetime. Although some proportion of invasive cancer diagnosed by mammography may never have presented clinically, the proportion is likely to be very small for women 40 to 49 years of age. Thus, concern about overdiagnosis from mammography screening focuses on the possibility that some proportion of DCIS detected by mammography would not have progressed to clinically evident invasive carcinoma within the life expectancy of a woman 40 to 49 years of age. Because we found no studies that evaluated this question directly, we examined 3 embedded questions: 1) Does the use of screening mammography increase the probability of a DCIS diagnosis? 2) What proportion of DCIS will progress to clinically evident invasive cancer, and over what period? 3) What are the clinical and quality-of-life consequences of a DCIS diagnosis?

The use of mammography screening has been associated with the incidence of DCIS in ecological and other analyses (7073). The identification of DCIS increased 7-fold from 1980 (when screening mammography programs were introduced) to 2001 (70). More than 25% of cases of cancer diagnosed among women in their 40s are DCIS, and 86% of DCIS cases are detected by screening (71).

Relatively few studies have examined the natural history of DCIS. Although some older studies suggest that approximately 40% of women who had a local excision or no treatment for DCIS may develop breast cancer in the same breast, these studies provide little information to evaluate study quality and generally included very few women (7481). The largest series of 80 women with untreated DCIS found that 14% had a cancer diagnosis after several decades of follow-up (75). Studies of women with treated DCIS have found that 3% to 8% had invasive breast cancer at 5 years and 2% had died of breast cancer at 10 to 15 years (82).

The diagnosis of DCIS has significant clinical consequences. Small cross-sectional studies suggest that women diagnosed with DCIS experience some emotional duress, such as sleeplessness and anxiety (8384), but how long these symptoms persist or their effect on overall quality of life is not known. In 1999, 28% of U.S. women diagnosed with DCIS had mastectomy, 64% had lumpectomy, and 52% of those who had lumpectomy had radiation (85).

Appendix Table 3 details evidence from these studies on the risk for overdiagnosis.

Table Jump PlaceholderAppendix Table 3.  Overdiagnosis*
False-Positive Test Results

Women who undergo screening mammography are at risk for a false-positive result and associated adverse consequences. A recent meta-analysis of the sensitivity and specificity of mammography found that the probability of a false-positive mammogram was between 0.9% and 6.5%, with most studies falling between 2% and 4% (85). Although relatively few studies provided data stratified by age, the rate of false-positive results did not differ between women 40 to 49 years of age and women 50 years of age or older in the Canadian National Breast Screening Study (8687), the San Francisco Demonstration Project (88), or the Nijmegen case–control study (89). Other studies have examined the cumulative risk for a false-positive mammogram over time. In an analysis of data from the Harvard Pilgrim Health Care study, the cumulative risks for a false-positive mammogram for women 40 to 49 years of age was 30% after 5 mammograms and 56% after 10 mammograms (90). Other analyses have demonstrated cumulative rates of false-positive mammograms of 21% (91) and 38% (92) after 10 mammograms. Relatively few studies describe diagnostic evaluations among women with abnormal mammograms. Among the 631 false-positive mammograms in the Harvard Pilgrim Health Care study, 162 resulted in additional outpatient visits, 560 resulted in additional diagnostic imaging, and 128 resulted in biopsy. An analysis of the Stockholm trial demonstrated that false-positive mammograms (among 231 women 40 to 49 years of age) resulted in 648 physician visits, 244 fine-needle aspirations, 92 additional mammographies, and 55 excisional biopsies (93).

We included 22 studies that investigated the outcomes of false-positive screening mammograms (94115). These outcomes included general anxiety and depression, anxiety specific to breast cancer, perceived susceptibility to breast cancer, adherence to screening mammography, and frequency of breast self-examination.

Overall, these studies found that false-positive mammograms were associated with a small increase in generalized anxiety and depression during the evaluation period, which resolved quickly after the evaluation was completed. In 1 study, these increases were seen only in comparison with women who had a negative test result and not in comparison with women who had not undergone screening (114). Several studies documented a more sustained increase in anxiety specific to breast cancer; however, such increases tended to be small and were confined to few women (92, 106, 109110) and several studies found no such increase (99, 101, 115). Two studies (98, 105) reported that increased anxiety specific to breast cancer recurred at the next screening. In general, psychological consequences were greater among women who underwent biopsy than women who had further imaging only.

Most studies found that women who had a false-positive mammogram were just as likely to undergo subsequent mammography screening as women who did not have a false-positive mammogram (100, 105107, 112113). Two studies found slightly lower rates of subsequent screening among women who had a false-positive mammogram (98, 108). Having had a false-positive mammogram was associated with an increase in the frequency of breast self-examination (99105) and of breast- and non–breast-related health care visits (96).

Appendix Table 4 details evidence from these studies on the risk for false-positive test results.

Table Jump PlaceholderAppendix Table 4.  False-Positive Test Results*
False Reassurance

Some proportion of women who have a negative mammogram will develop breast cancer before their next screening. Concern about the risk for false reassurance centers on the possibility that a negative mammogram may lead women to delay seeking attention for a subsequent breast abnormality. If delay in presentation is associated with progressive disease, false reassurance might result in advanced-stage cancer. We identified 2 studies that estimate the probability of these events after a negative mammogram. A survey of 516 women in the Dutch screening program found that more than 99% of women would be concerned about breast cancer if they felt a breast lump and would pursue medical evaluation within a week (116). This probability was not affected by having previous negative screenings. In a study of 336 women with newly diagnosed breast cancer in Finland, 29% of women with a negative mammogram delayed treatment, compared with 0% of women with screen-detected cancer (117). However, the study did not provide information about the extent or clinical significance of the delay.

Pain from the Mammography Procedure

We included 22 studies that investigated pain and discomfort associated with mammography (43, 118138). The prevalence of pain varied widely. For example, 1 study found that 77% of women experienced pain, whereas another study reported that 28% of women had considerable pain. This difference could be due to the distinction between “pain” and “considerable pain.” It also could be attributed to differences in the instruments used to measure pain, but it persisted across studies using the same instruments or response scales. In studies that measured whether pain was a deterrent to having future mammography, few women agreed that the pain caused by mammography would prevent them from attending future screening. The degree of pain was associated with the stage of menstrual cycle (126, 135136), anxiety (121, 132), and premammography anticipation of pain (43, 121, 134, 138).

Appendix Table 5 details evidence from these studies on the risk for pain on mammography.

Table Jump PlaceholderAppendix Table 5.  Pain from the Mammography Procedure*
Individualizing Risks and Benefits

Considerable evidence indicates that the risks and benefits of screening mammography vary among women. This variation exists across age groups but has particular clinical relevance for women younger than age 50 years. Lower rates of disease in this age group make individual variation more important. This variation arises in 3 main domains. First, clinical characteristics have been demonstrated to affect mammography performance, including age, family history of breast cancer, and breast density. Second, the absolute benefit of mammography is correlated with the predicted breast cancer risk, both because the relative decrease in breast cancer mortality rate translates into a larger absolute decrease when the baseline risk without screening is higher and because the rate of false-positive results greatly depends on the prevalence of breast cancer in the population. Third, individual values and risk preferences determine the effect that positive and negative mammography outcomes will have on quality of life.

Women with a history of breast cancer in a first-degree relative are more likely to have screen-detected cancer than are women without a family history of breast cancer (139153, 141). For women 40 to 49 years of age, 4.7 cases are detected per 1000 examinations among women with a family history compared with 2.7 cases per 1000 examinations among women without a family history. For women 50 to 59 years of age, the rates are 6.6 and 4.6 cases per 1000 examinations, respectively (140141). In general, the rate of cancer detection among women with a family history of breast cancer matches that among women without a family history who are a decade older. The incidence of false-positive and false-negative mammograms seems to be slightly higher among women with a family history of breast cancer than among women without a family history of breast cancer (139141).

Several studies suggest that the sensitivity of screening mammography is lower among women with dense breasts. In an analysis of almost 330 000 women, sensitivity was 62.2% in women with extremely dense breasts compared with 88.2% in women whose breasts were almost entirely fat (142). Specificity also changes with breast density. Among women 40 to 44 years of age, 9.7% of women with extremely dense breasts had a false-positive mammogram compared with 4.2% of women with breasts that were almost entirely fat (143). False-positive mammograms are also more common if it has been longer since the last screening and if a woman has had a previous breast biopsy (143).

Information about breast cancer risk can be based on the presence or absence of individual risk factors or on the output of prediction models that incorporate data about several risk factors. The most commonly used individual risk factors for assessing breast cancer risk are age and family history of breast cancer. Breast cancer risk increases steadily with age, from a 5-year risk of 0.28% for a 35-year-old woman to a 5-year risk of 2.35% for a 75-year-old woman (144). Family history also has a substantial effect on risk, with the presence of a first-degree relative conferring a 2- to 3-fold increase in risk and the presence of a second-degree relative conferring a 30% to 50% increase in risk (145). The most commonly used risk prediction model is the Gail model, which was used for enrollment in the initial trial of tamoxifen for breast cancer prevention and is now included in guidelines for tamoxifen use (146148). This model includes age, family history, age at menarche, age at first live birth, age at menopause, breast biopsy history, and race. Validation studies have demonstrated that the Gail model accurately predicts the number of cases of breast cancer that will develop in a given population but is much less accurate in determining which individual women will develop breast cancer (148151). In these studies, the Gail model has a c-statistic (area under the receiver-operating characteristic curve) of 0.58 to 0.67, indicating that it provides only modest discriminatory power over chance alone (c-statistic, 0.5).

Although relatively few studies have measured values and preferences about mammography screening, the evidence suggests that women vary substantially in the value they place on a false-positive test result, a negative mammogram, and the reduction in breast cancer mortality rate from screening. In a survey of 479 U.S. women, 63% would tolerate 500 or more false-positive results for every life saved by screening mammography (152). Only 38% would include information about false-positive results in their decision about screening, although 60% reported that information about nonprogressive breast cancer would influence their decisions. Other studies have demonstrated that most women overestimate their short- and long-term risk for breast cancer and the absolute benefit, although not the relative risk reduction, from screening mammography (153154).

Current evidence indicates that women 40 to 49 years of age who undergo routine mammography screening will decrease their risk for death due to breast cancer but will increase their risks for undergoing unnecessary procedures, breast cancer–related anxiety, discomfort at the time of screening, and exposure to low-dose radiation. Because the incidence of breast cancer and the effectiveness of mammography are lower among women in their 40s than among women 50 years of age or older, mammography screening results in less absolute benefit and greater absolute risk for women 40 to 49 years of age than for women 50 years of age or older. The proportion of women 50 years of age or older whose risks for mammography outweigh the benefits is widely accepted to be clinically insignificant. However, the evidence suggests that this proportion is higher and may be clinically significant for women 40 to 49 years of age. Given this difference, a woman 40 to 49 years of age who had a lower-than-average risk for breast cancer and higher-than-average concerns about false-positive results might reasonably delay screening. Measuring risks and benefits accurately enough to identify these women remains a challenge.

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Elmore JG, Miglioretti DL, Reisch LM, Barton MB, Kreuter W, Christiansen CL. et al.  Screening mammograms by community radiologists: variability in false-positive rates. J Natl Cancer Inst. 2002; 94:1373-80. PubMed
 
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Gail MH, Brinton LA, Byar DP, Corle DK, Green SB, Schairer C. et al.  Projecting individualized probabilities of developing breast cancer for white females who are being examined annually. J Natl Cancer Inst. 1989; 81:1879-86. PubMed
 
Chlebowski RT, Col N, Winer EP, Collyar DE, Cummings SR, Vogel VG 3rd. et al.  American Society of Clinical Oncology technology assessment of pharmacologic interventions for breast cancer risk reduction including tamoxifen, raloxifene, and aromatase inhibition. J Clin Oncol. 2002; 20:3328-43. PubMed
 
Costantino JP, Gail MH, Pee D, Anderson S, Redmond CK, Benichou J. et al.  Validation studies for models projecting the risk of invasive and total breast cancer incidence. J Natl Cancer Inst. 1999; 91:1541-8. PubMed
 
Tice JA, Cummings SR, Ziv E, Kerlikowske K.  Mammographic breast density and the gail model for breast cancer risk prediction in a screening population. Breast Cancer Res Treat. 2005; 94:115-22. PubMed
 
Rockhill B, Spiegelman D, Byrne C, Hunter DJ, Colditz GA.  Validation of the Gail et al. model of breast cancer risk prediction and implications for chemoprevention. J Natl Cancer Inst. 2001; 93:358-66. PubMed
 
Tice JA, Miike R, Adduci K, Petrakis NL, King E, Wrensch MR.  Nipple aspirate fluid cytology and the Gail model for breast cancer risk assessment in a screening population. Cancer Epidemiol Biomarkers Prev. 2005; 14:324-8. PubMed
 
Schwartz LM, Woloshin S, Sox HC, Fischhoff B, Welch HG.  US women's attitudes to false-positive mammography results and detection of ductal carcinoma in situ: cross-sectional survey. West J Med. 2000; 173:307-12. PubMed
 
Schwartz LM, Woloshin S, Black WC, Welch HG.  The role of numeracy in understanding the benefit of screening mammography. Ann Intern Med. 1997; 127:966-72. PubMed
 
Black WC, Nease RF Jr, Tosteson AN.  Perceptions of breast cancer risk and screening effectiveness in women younger than 50 years of age. J Natl Cancer Inst. 1995; 87:720-31. PubMed
 

Figures

Grahic Jump Location
Figure.
Risks and benefits of screening mammography.

Numbers correspond to the risks and benefits outlined in the Table.

Grahic Jump Location

Tables

Table Jump PlaceholderTable.  Risks and Benefits of Screening Mammography
Table Jump PlaceholderAppendix Table 1.  Evidence-Based Medicine Review Score: Criteria Used to Assess Study Quality*
Table Jump PlaceholderAppendix Table 3.  Overdiagnosis*
Table Jump PlaceholderAppendix Table 4.  False-Positive Test Results*
Table Jump PlaceholderAppendix Table 5.  Pain from the Mammography Procedure*

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Estimating net benefits and harms of screening mammography in women age 40-49
Posted on April 4, 2007
Benjamin Djulbegovic
H Lee Moffitt Cancer Center & Research Institute, University of South Florida
Conflict of Interest: None Declared

In the updated systematic review on the effects of screening mammography [SM] in women age 40-49, Armstrong et al [1] used relative effect measures to express most important benefits of SM, while at the same time they expressed most important harms of SM in terms of absolute effect measures. Notably, they estimated that SM is associated with relative-risk reduction in breast cancer mortality of 7-23%, while 30-200 women of age 40-49 will die in annual SM as a result of radiation-induced breast cancer [1]. It would be, however, more appropriate to express benefits and harms using the same effect measures.

It is particularly important to contrast net benefits and net risks in patients with and without SM. Of crucial importance for any prospective woman contemplating undergoing SM is to understand what outcome she can expect with and without SM. If individualized recommendations called by Qaasem et al is to become reality [2], estimates of net benefits and net harms of SM in women with different baseline risks of dying from breast cancer without undergoing SM should have been included in the recent ACP guidelines/systematic review. Had the authors presented data in such a way, they may have calculated that in the BEST case scenario for women at "average risk" of developing breast cancer, SM may save 46 lives/100,000 women screened over 10 years, at the cost of 30/100,000 lives lost. In the WORST case scenario, net benefits is actually negative, and more lives will be lost than saved [see below].

We believe that presenting data in this way may better help women understand benefits and harms of SM which need to be contrasted against their own individual risk for development of breast cancer. Only in this way can we truly exercise a women's preferences and values and preserve their autonomy consistent with ethical and rational decision-making [3].

----- Appendix

Calculation of net benefits [4] (outcome: breast cancer deaths):

Net Benefits (B)= BC "“ BC*(1-RRR) "“ H

BC= Mortality from breast cancer without SM; RRR= relative reduction in breast cancer mortality due to SM; H= radiation-induced breast cancer deaths

Net harms (H) = Mortality without breast cancer- breast cancer mortality due to SM= 1-(1-H)= H

BEST CASE SCENARIO:

BC= 3.3/1,000 women (average risk)[5] RRR=23% [1] H=30/100,000 women [1]

B= 0.0033 -0.0033*(1-0.23)-0.00030 = 0.00046 (= 46/100,000 lives saved) H=0.00030 (30/100,000 lives lost) B/H=1.5 (If woman's preferences are not taken into account, this B/H ratio translates into benefits of SM outweighing its harms only when probability of breast cancer exceeds 39.5%[4].)

WORST CASE SCENARIO

RRR=7% [1]

B= 0.0033 -0.0033*(1-0.07)-0.00030 = -0.000069 (negative net benefits; 69 lives lost/1,000,000 screened)

H= 200/100,000 women1

B= 0.0033 -0.0033*(1-0.07)-0.0020= -0.001769 (negative net benefits; 1769 lives lost/1,000,000 screened)

Literature

1. Armstrong K, Moye E, Williams S, Berlin JA, Reynolds EE. Screening Mammography in Women 40 to 49 Years of Age: A Systematic Review for the American College of Physicians. Ann Intern Med 2007;146(7):516-526.

2. Qaseem A, Snow V, Sherif K, et al. Screening Mammography for Women 40 to 49 Years of Age: A Clinical Practice Guideline from the American College of Physicians. Ann Intern Med 2007;146(7):511-515.

3. Djulbegovic B, Lyman G. Screening mammography at 40-49 years: regret or regret? Lancet 2006;368:2035-2037.

4. Djulbegovic B, Hozo I, Lyman G. Linking evidence-based medicine therapeutic summary measures to clinical decision analysis. MedGenMed 2000(January 13):http://www.medscape.com/Medscape/GeneralMedicine/journal/2000/v02.n01/mgm0113.djul/mgm0113.djul -01.html.

5. Moss SM, Cuckle H, Evans A, L. J, Waller M, Bobrow L. Effect of mammographic screening from age 40 years on breast cancer mortality at 10 year's follow-up: a randomised controlled trial. Lancet 2006;368:2053-60.

Conflict of Interest:

None declared

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Summary for Patients

Screening Mammography in Women Age 40 to 49 Years

The summary below is from the full reports titled “Screening Mammography in Women 40 to 49 Years of Age: A Clinical Practice Guideline from the American College of Physicians” and “Screening Mammography in Women 40 to 49 Years of Age: A Systematic Review for the American College of Physicians.” They are in the 3 April 2007 issue of Annals of Internal Medicine (volume 146, pages 511-515 and 516-526). The first report was written by A. Qaseem, V. Snow, K. Sherif, M. Aronson, K.B. Weiss, and D.K. Owens, for the Clinical Efficacy Assessment Subcommittee of the American College of Physicians; the second report was written by K. Armstrong, E. Moye, S. Williams, J.A. Berlin, and E.E. Reynolds.

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