From the Department of Epidemiology and
Biostatistics (Drs Kerlikowske, Grady, and Ernster, and Mr Sandrock) and the
Division of General Internal Medicine, Department of Medicine (Ms Rubin),
University of California, San Francisco, and the General Internal Medicine
Section, Department of Veterans Affairs Medical Center, San Francisco, Calif
(Drs Kerlikowske and Grady).
Reprint requests to San Francisco
Veterans Affairs Medical Center, General Internal Medicine Section, 111A1, 4150
Clement St, San Francisco, CA 94121 (Dr Kerlikowske).
Outline
Graphics
Abstract^
Objective: To determine the efficacy of screening mammography by age, number of mammographic views per screen, screening interval, and duration of follow-up.
Design: Literature review and meta-analysis.
Data Identification and Analysis.Literature search of English-language studies reported from January 1966 to October 31, 1993, using MEDLINE, manual literature review, and consultation with experts. A total of 13 studies were selected, and their results were combined using meta-analytic techniques based on the assumption of fixed effects.
Main Results.The overall summary relative risk (RR) estimate for breast cancer mortality for women aged 50 to 74 years undergoing screening mammography compared with those who did not was 0.74 (95% confidence interval (CI), 0.66 to 0.83). The magnitude of the benefit in this age group was similar regardless of number of mammographic views per screen, screening interval, or duration of follow-up. In contrast, none of the summary RR estimates for women aged 40 to 49 years was significantly less than 1.0, irrespective of screening intervention or duration of follow-up. The overall summary RR estimate in women aged 40 to 49 years was 0.93 (95% CI, 0.76 to 1.13); the summary RR estimate for those studies that used two-view mammography was 0.87 (95% CI, 0.68 to 1.12) compared with 1.02 (95% CI, 0.73 to 1.44) for those studies that used one-view mammography, and for those studies with 7 to 9 years of follow-up, the summary RR estimate was 1.02 (95% CI, 0.82 to 1.27) compared with 0.83 (95% CI, 0.65 to 1.06) for those studies with 10 to 12 years of follow-up.
Conclusion: Screening mammography significantly reduces breast cancer mortality in women aged 50 to 74 years after 7 to 9 years of follow-up, regardless of screening interval or number of mammographic views per screen. There is no reduction in breast cancer mortality in women aged 40 to 49 years after 7 to 9 years of follow-up. Screening mammography may be effective in reducing breast cancer mortality in women aged 40 to 49 years after 10 to 12 years of follow-up, but the same benefit could probably be achieved by beginning screening at menopause or 50 years of age.
(JAMA. 1995;273:149-154)
The goal of screening mammography is to reduce mortality from breast cancer. In clinical trials, screening mammography has been shown to reduce mortality from breast cancer 20% to 39% among women aged 50 years and older [1,2,3,4,5,6]. Among women aged 40 to 49 years, the evidence to support the efficacy of screening mammography is less convincing. Eight randomized controlled trials have reported no statistically significant reduction in breast cancer mortality in women aged 40 to 49 years after 7 to 10 years of follow-up [2,3,4,5,6,7,8,9]. However, after 10 years of follow-up, a nonsignificant trend toward reduced mortality ranging from 13% to 23% is observed in several studies [6,8,9].
These findings have led to disagreement concerning the benefit of screening mammography in women aged 40 to 49 years. The major reason for disagreement is that individual studies have included too few women aged 40 to 49 years to detect a statistically significant difference in breast cancer mortality in this age group [10]. There is also controversy about the ideal interval for screening, the ideal number of mammographic views per screen, the role of clinical breast examination, and the potential impact of newer mammographic equipment adopted in the 1980s.
We used meta-analytic techniques [11] to combine relative risks (RRs) and odds ratios (ORs) from multiple studies of screening mammography to provide increased power to determine the efficacy of screening mammography in reducing breast cancer mortality. We also combined RRs and ORs to evaluate the effect of the number of mammographic views performed per screen, screening interval, and duration of follow-up and to assess the benefit of clinical breast examination performed in conjunction with mammographic screening.
METHODS^
A comprehensive literature search of English-language
studies from January 1966 to October 31, 1993, was performed using the MEDLINE
database and the following terms: breast neoplasm, mortality, mass screening,
and female. A total of 264 articles were found. Review articles, letters, and
comments were eliminated, thus narrowing the references to 200. From these 200
references, all randomized controlled trials and cohort and case-control
studies of the efficacy of screening mammography were selected; 75 references
were identified.
These 75 references were then reviewed to determine if they met the following inclusion criteria: (1) experimental study with the main outcome of breast cancer death, prospective cohort study with internal controls with the main outcome of breast cancer death, or case-control study with population-based controls with the main outcome of breast cancer death; (2) follow-up of at least 5 years and a minimum of 10 breast cancer deaths; (3) RR or OR reported with a confidence interval (CI) or data presented in the article that permitted calculation of an RR or OR and CI; and (4) RR or OR reported that was adjusted for age or based on controls that were age matched to cases. We excluded hospital-based case-control studies and cohort studies without controls [12,13,14,15,16].
After the application of these criteria, 32 articles remained. An additional eight references were identified by manual literature searches of reference lists in relevant papers and consultations with colleagues and experts. Two of the authors abstracted data from each article. If there was disagreement regarding results, a third author reviewed the article in question and resolved the disagreement. The abstractors were not blinded to the journal, year of publication, or authors. For studies that resulted in several publications, data from the most recent publication with 7 to 9 years of follow-up and data from the most recent publication with 10 to 12 years of follow-up were used. We selected those interval follow-up categories to be inclusive of all available published RRs and ORs. A total of 25 references were excluded because of multiple publications from the same study. Thus, 15 references from 13 studies remained for the meta-analysis [2,3,4,5,6,7,8,9,17,18,19,20,21,22,23]. An updated, unpublished analysis of the Edinburgh trial that was presented at the International Union Against Cancer Executive Committee Meeting on Breast Cancer Screening in Premenopausal Women in Developed Countries was also included in the meta-analysis [24].
To estimate the risk of death from breast cancer in women who underwent screening mammography, we pooled RRs and ORs from individual studies to calculate summary estimates of RR using statistical methods described by Greenland [25] based on the assumption of fixed effects. The RRs and ORs from all studies were combined for overall summary RR estimates for women aged 40 to 74 years, 50 to 74 years, and 40 to 49 years. Separate summary RR estimates were also calculated for experimental vs nonexperimental studies. The Florence case-control study did not present data on screening efficacy based on age at first screening examination [20]. For this reason, data from that study were included in the overall summary RR estimate for breast cancer mortality but not in the analyses of efficacy for women aged 40 to 49 years or 50 to 74 years.
Summary RR estimates were calculated based on number of mammographic views per screen (one view vs two views), screening interval (12 months vs >12 months), duration of follow-up (7 to 9 years vs 10 to 12 years), duration of screening (3 to 5 years vs 8 to 10 years), whether clinical breast examination was performed in addition to mammography, and date the study began (before 1980 vs 1980 or later). If studies reported RRs or ORs after 7 to 9 years of follow-up and after 10 to 12 years of follow-up, RRs or ORs reported for each follow-up period were pooled with the appropriate time period. For the analysis based on the number of mammographic views, the Edinburgh study--which performed two-view mammography at baseline and one-view mammography on subsequent screens--was included with the two-view mammography studies since the summary RR estimates were similar regardless of whether the study was combined with the one-view mammography studies or two-view mammography studies. When determining the summary RR estimate for number of mammographic views per screen, screening interval, whether clinical breast examination was performed in addition to mammography, and study start date, we used RRs and ORs reported from the most recent publication.
A test for heterogeneity was performed for all summary RR estimates. Since the power of statistical tests of heterogeneity is low, a relatively high critical value for P of.2 was selected to avoid underestimating the presence of heterogeneity.
RESULTS^
Women Aged 40 to 74 Years at
Screening^
We found a total of 13 studies (nine randomized
controlled trials and four case-control studies) that met our inclusion
criteria Table 1. The reported RRs and ORs for
women aged 40 to 74 years from the 12 studies included in the meta-analysis
ranged from 0.51 to 0.97 Table 2, with an overall
summary RR estimate for breast cancer death among women who underwent screening
mammography compared with women who did not of 0.75 (95% CI, 0.68 to 0.83).
Case-control studies had a significantly lower summary RR estimate than
randomized controlled trials (0.62 vs 0.79) Table
3. For this reason we excluded case-control studies from other summary
estimates when analyzing studies by number of views, screening interval,
duration of screening and follow-up, clinical breast examination, and study
start date.
Table 1. Randomized Controlled Trials and Case-Control Studies Included
in Meta-analysis
Table 2. Relative Risks (RRs), Odds Ratios, and 95% Confidence Intervals
(CIs) of Screening Mammography Studies Used in Meta-analysis
Table 3. Summary Relative Risk (RR) Estimates and 95% Confidence
Intervals (CIs) From Meta-analysis by Age and Screening Variables
The summary RR estimates were similar for randomized controlled trials that performed two-view mammography vs one-view mammography (0.80 vs 0.76) Table 3; performed screening mammography every 12 months vs every 18 to 33 months (0.77 vs 0.79); included 7 to 9 years of follow-up vs 10 to 12 years of follow-up (0.78 vs 0.77); screened for 3 to 5 years vs 8 to 10 years (0.79 vs 0.78); and performed clinical breast examination in conjunction with screening mammography vs screening mammography alone (0.79 vs 0.78). Studies that started before 1980 had a lower summary RR estimate than studies that began in 1980 or after (0.77 vs 0.87).
Women Aged 50 to 74 Years at
Screening^
We found 10 studies (eight randomized controlled trials
and two case-control studies) that met inclusion criteria
Table 2. All of the reported RRs were less than
1.0, and five studies reported RRs that were significantly less than 1.0
Table 2. The overall summary RR estimate for the
10 studies was 0.74 (95% CI, 0.66 to 0.83). Case-control studies had a
significantly lower summary RR estimate than randomized controlled trials (0.45
vs 0.77) Table 3 and were thus excluded from
other summary estimates.
Summary RR estimates were similar for randomized controlled trials that performed screening mammography every 12 months vs every 18 to 33 months (0.77 vs 0.77); included 7 to 9 years of follow-up vs 10 to 12 years of follow-up (0.73 vs 0.76); screened for 3 to 5 years vs 8 to 10 years (0.76 vs 0.78); and performed clinical breast examination in conjunction with screening mammography vs screening mammography alone (0.80 vs 0.76). Although not significantly different, the summary RR estimate for studies that performed one-view mammography was lower than for studies that performed two-view mammography (0.70 vs 0.83). Studies that started before 1980 had a somewhat lower summary RR estimate than studies that began in 1980 or after (0.76 vs 0.83).
Women Aged 40 to 49 Years at
Screening^
We found nine studies (eight randomized controlled
trials and one case-control study) that met inclusion criteria
Table 2. Five of the nine studies reported RRs or
ORs less than 1.0, but none was significantly less than 1.0
Table 2. The overall summary RR estimate for the
nine studies was 0.93 (95% CI, 0.76 to 1.13) and for randomized controlled
trials was 0.92 (95% CI, 0.75 to 1.13) Table
3.
The summary RR estimates were similar for randomized controlled trials that performed screening mammography every 18 to 33 months compared with every 12 months (0.88 vs 0.99) and performed clinical breast examination in conjunction with screening mammography compared with screening mammography alone (0.93 vs 0.91). Although not significantly different, studies in which women underwent two-view mammography had a lower summary RR estimate than studies that performed one-view mammography (0.87 vs 1.02). None of these summary RR estimates was significantly less than 1.0.
Studies that had 10 to 12 years of follow-up had a lower summary RR estimate than those that had only 7 to 9 years of follow-up (0.83 vs 1.02, respectively), and studies that screened for 8 to 10 years had a lower summary RR estimate than those that screened for 3 to 5 years (0.86 vs 0.98). However, none of these summary RR estimates was significantly less than 1.0. Women aged 40 to 49 years who underwent two-view mammography and had 7 to 9 years of follow-up had no reduction in breast cancer mortality compared with unscreened women (RR=1.04; 95% CI, 0.81 to 1.34). There were only three clinical trials in which women aged 40 to 49 years underwent two-view mammography and had 10 to 12 years of follow-up; in those, the RR for reduction in breast cancer mortality was 0.96 (95% CI, 0.71 to 1.3) after 7 to 9 years of follow-up and 0.73 (95% CI, 0.54 to 1.0) after 10 to 12 years of follow-up. Studies that started before 1980 had a lower summary RR estimate than studies that began in 1980 or later (0.83 vs 1.16).
COMMENT^
The results of our meta-analysis suggest that screening
mammography reduces breast cancer mortality by 26% (95% CI, 17% to 34%) in
women aged 50 to 74 years but does not significantly reduce breast cancer
mortality in women aged 40 to 49 years. A recent meta-analysis by Elwood et al
[26] of published data from six randomized
controlled trials of screening mammography with 7 years of follow-up found a
34% reduction in breast cancer mortality in women aged 50 to 74 years but no
reduction in breast cancer mortality in women aged 40 to 49 years. In addition
to the published data from the six randomized controlled trials, we included
unpublished updated data from the Edinburgh trial [24] and published results from the Gothenburg trial
[8,9], the Canadian trials
[7,18], and case-control studies
[17,19,20,21]. Despite these differences, the
summary RR estimates we report are similar to those reported by Elwood et al
(RR=0.66 and 95% CI, 0.55 to 0.79, for women aged 50 to 74 years; RR=0.99 and
95% CI, 0.74 to 1.32, for women aged 40 to 49 years) [26].
Women Aged 50 to 74 Years^
We found a statistically significant reduction in
breast cancer mortality in women aged 50 to 74 years, regardless of the number
of mammographic views per screen, screening interval, duration of screening or
follow-up, or addition of clinical breast examination. Proponents of two-view
mammography emphasize that the sensitivity for detecting breast cancer is 8%
higher (range, 0% to 18.4%) in women who have two-view mammography
[27]. However, the sensitivity of one-view
mammography (86% to 95%) [2,26,28] vs two-view
mammography (88%) [18] in women older than 50
years is similar, and our results suggest that there are no differences in the
reduction in breast cancer mortality between screening with one view or two
views Table 3. Thus, in women aged 50 years and
older, one-view mammography appears to have sufficient sensitivity to reduce
breast cancer mortality. Some have also argued that it is more cost-effective
to perform two-view mammography since the proportion of screening mammography
recalled for evaluation of abnormalities is higher with one-view mammography
[29,30]. However, randomized controlled trials
using one-view mammography have similar recall rates (5%)
[2,31] as those obtained in studies that use
two-view mammography (3.4% to 6%) [7,18,32].
Among women aged 50 years and older, screening every 18 to 33 months resulted in the same 23% reduction in breast cancer mortality as screening every 12 months. Since the sojourn time (time spent in the preclinical, mammographically detectable state) of breast cancer is thought to be about 3.5 years in women aged 50 to 69 years [2,33], these findings are not surprising. Screening more frequently than every 2 years in this age group does not appear to add extra benefit in reducing breast cancer mortality [34] but will increase the cost of screening.
Clinical breast examination in addition to mammography did not decrease breast cancer mortality beyond the reduction achieved by mammography alone for women aged 50 to 74 years or for women aged 40 to 49 years. Since clinical breast examination detects palpable lesions only and its sensitivity is low (46% to 68%) [9,18], it is not surprising that clinical breast examination adds little benefit to that achieved by screening mammography. However, the quality of clinical breast examinations was suboptimal in some studies, possibly underestimating the potential benefit of clinical breast examination. Data from randomized controlled trials did not allow us to evaluate the benefit of clinical breast examination alone. In the Canadian trial, women aged 50 to 59 years were randomized to receive either mammography and clinical breast examination or clinical breast examination alone. This study showed that mammography and clinical breast examination did not decrease breast cancer mortality beyond the reduction achieved by clinical breast examination alone [18]. However, it is not clear if mammography failed to decrease breast cancer mortality or if optimal clinical breast examinations were just as effective as mammography.
Women Aged 40 to 49 Years^
For women aged 40 to 49 years followed for 7 to 9
years, there was a nonsignificant increase (2%) (95% CI, -18% to +27%) in
breast cancer mortality, and for those followed for 10 to 12 years, there was a
nonsignificant reduction (17%) (95% CI, -35% to +6%) in breast cancer
mortality. Overall, screening mammography reduced breast cancer mortality by 7%
(95% CI, -24% to +13%) in this age group after 7 to 12 years of follow-up.
Despite the diverse design of the various screening mammography studies, the
combined results are homogenous (chi squared (chi2) test for
heterogeneity; P=.5), indicating little variability among the studies. Pooled
data from the Swedish trials [8] and results from
the Health Insurance Plan trial [35] have also
suggested a benefit from screening mammography in younger women that does not
occur until after 9 to 10 years of follow-up.
This finding is difficult to explain. Some have argued that prolonged follow-up of the small number of women aged 40 to 49 years enrolled in randomized controlled studies is required to accumulate adequate numbers of breast cancer deaths to provide statistical power to show a reduction in breast cancer mortality among those screened [10]. However, if the explanation is simply lack of statistical power, the percentage reduction in breast cancer mortality due to screening reported at 7 to 9 years of follow-up should be similar to that reported at 10 to 12 years of follow-up, only with wider CIs. This does not appear to be the case, since the summary RR estimate from studies with only 7 to 9 years of follow-up [5,7,8,17] shows a 2% increase in breast cancer mortality among women undergoing screening mammography, while the summary RR estimate from studies with 10 to 12 years of follow-up shows a 17% decrease Table 3. These findings would indicate that the issue is not simply lack of statistical power, since the reduction in breast cancer mortality at 7 to 9 years is significantly different than that at 10 to 12 years and the CIs for the two estimates are similarly wide.
We believe these findings are consistent with two possible explanations: (1) since the 95% CI overlaps 1.0, the reduction in breast cancer mortality noted after 10 to 12 years of follow-up may be due to chance, or (2) mammography screening has an increasingly beneficial effect over time. The latter could occur if screening mammography is effective in reducing breast cancer mortality in postmenopausal but not premenopausal women. The median age of menopause in women in the United States is 50.7 years, and approximately 80% of women will become menopausal between the ages of 45 and 54 years [36,37]. In the Health Insurance Plan study, 85% of all breast cancer in women who started screening between 40 and 49 years of age was diagnosed between 45 and 54 years of age, when most women would be menopausal [38]. The majority of women in the Edinburgh and Malmo trials were also probably menopausal when their breast cancer was diagnosed, since the youngest age of women at the start of screening was 45 years. The fact that screening mammography decreases breast cancer mortality in women aged 50 to 74 years within 7 to 9 years is probably because almost all of these women are postmenopausal with breasts with a higher fat content, increasing the sensitivity of mammography to detect small tumors with a good prognosis. Also, screen-detected breast cancers among postmenopausal women less commonly present as advanced stage disease (tumor diameter larger than 20 mm or lymph node involvement) compared with screen-detected breast cancers among premenopausal women [39]. It appears that no benefit is observed in younger women until 10 to 12 years of follow-up, by which time women who were aged 40 to 49 years when they entered the trial are now aged 50 to 61 years and postmenopausal when undergoing screening mammography. These findings suggest that it might be possible to wait to begin screening when women become 50 years old or menopausal and achieve the same benefit in mortality reduction as beginning screening at 40 years of age.
When the data for women aged 40 to 49 years are summarized by number of mammographic views, there is a suggestion that two-view mammography may reduce breast cancer mortality (13% reduction) while one-view mammography is not beneficial (4% increase in breast cancer mortality). For the three randomized controlled trials that used two-view mammography [3,4,6,24], the reduction in breast cancer mortality was 4% after 7 to 9 years of follow-up and 27% after 10 to 12 years. Since younger women's breasts have a lower fat content and consequently are less radiolucent than those of older women, the additional mammographic view may enhance the sensitivity of mammography and, consequently, the chance of finding early breast cancer in these women [40,41]. In younger women, two-view mammography has been reported to have a sensitivity of 81% [7] vs 60% to 70% [2,26,28,42] for one-view mammography. Thus, if women younger than 50 years choose to undergo screening mammography, two views should probably be performed.
Experts in mammography who promote screening for women aged 40 to 49 years believe these women should be screened yearly because younger women tend to have faster-growing tumors [2,33,34]. The time for development of a mammographically detectable tumor is thought to be 1.25 years in women aged 35 to 49 years [2,33], suggesting that annual screening mammography is necessary to detect small occult tumors as early as possible. Our summary estimate results do not suggest that screening women aged 40 to 49 years every 12 months is more effective than screening every 18 to 33 months (1% vs 12% reduction). However, only two studies screened women aged 40 to 49 years annually [6,7], and there was variability in the findings of these two studies (chi squared (chi2) test for heterogeneity; P=.09).
Proponents of screening mammography in women aged 40 to 49 years argue that standards of community practice for mammography have steadily improved since the execution of screening mammography trials and that if newer mammographic equipment operated by trained radiology technicians were used in women aged 40 to 49 years in a randomized controlled trial, screening mammography would prove to be efficacious. Our data do not support this rationale since studies performed before 1980 had lower summary RR estimates than studies performed after 1980 for both younger and older women. Most of this difference is probably due to longer follow-up in the studies that began before 1980; but even among studies with uniform follow-up (7 to 9 years), summary RR estimates were lower for studies that began before 1980 compared with those that began later (among 40- to 49-year-olds, 5% reduction vs 16% increase in breast cancer mortality; among 50- to 74-year-olds, 30% vs 17% reduction). Another possible explanation is that in studies conducted after 1980 women in control groups were more likely to undergo screening mammography, which could attenuate any differences in the impact of screening between screened and unscreened groups [9].
Ideally, we would have examined the effect of all possible combinations of factors to determine if any one combination provides a clearly beneficial screening strategy in women aged 40 to 49 years. For example, we could not evaluate the effect of screening annually with two-view mammography in women aged 40 to 49 years who had at least 10 years of follow-up. Because of the relatively small number of studies and their differing designs, it was not possible to look at the effect of more than one or two factors simultaneously.
CONCLUSION^
Based on the results of our meta-analysis, we recommend
that women aged 50 to 74 years undergo regular screening mammography. Although
we did not perform a formal cost analysis, our findings suggest that optimum
cost-effectiveness may be achieved by screening these women every 2 years
without diminishing the potential benefit of screening. We were unable to
document a reduction in breast cancer mortality in women younger than 50 years
who undergo screening mammography for 7 to 9 years. There may be some benefit
in younger women 10 to 12 years after mammography screening begins, but the
same benefit could probably be achieved by beginning screening at menopause or
50 years of age.
This study was supported in part by grant P50 CA58207 from the National Institutes of Health Breast Cancer Special Projects of Research Excellence. Dr Kerlikowske is supported in part by an American Cancer Society Career Development Award for Primary Care Physicians. Dr Grady is supported in part by a Merck/Society for Epidemiologic Research Clinical Epidemiology Fellowship.
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