Affiliations of authors: School of Public Health, University of Washington (EW, DLM, DSMB, NO, WB), Center for Health Studies, Group Health Cooperative (DLM, DSMB, WB), and Cancer Research and Biostatistics (WB), Seattle, WA; Health Promotion Research (BMG) and Department of Medical Biostatistics (PMV), University of Vermont, College of Medicine, Burlington, VT; Department of Radiology, University of New Mexico, Health Sciences Center, Albuquerque (RDR); Applied Research Program, Department of Cancer Control and Population Sciences, National Cancer Institute, Bethesda, MD (RB-B, SHT); Norris Cotton Cancer Center, Dartmouth-Hitchcock Medical Center, Department of Community and Family Medicine, Dartmouth Medical School, Lebanon, NH (PAC); Department of Radiology, University of North Carolina, Chapel Hill, NC (BCY); Department of Biostatistics, The Cooper Institute, Golden, CO (LS); General Internal Medicine Section, Department of Veterans Affairs and Departments of Medicine and Epidemiology and Biostatistics, University of California, San Francisco, CA (KK)
Correspondence to: Emily White, PhD, Fred Hutchinson Cancer Research Center, MY-B402, P.O. Box 19034, Seattle, WA 98109-1024 (ewhite{at}fhcrc.org)
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ABSTRACT |
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INTRODUCTION |
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Results of prior studies have not clarified the relative advantages of 1-year versus 2-year screening intervals. Two randomized trials compared a 1-year screening interval with a 3-year screening interval (5,6); however, no randomized trials have compared a 1-year interval with a 2-year interval. Observational studies on this topic (711) have been limited by small sample sizes and varying definitions for screening interval. Finally, some groups have used statistical models of the natural history of breast cancer to estimate the cost-effectiveness of mammography by screening interval (12). However, the accuracy of these models depends on the accuracy of the empiric data that enter the model (13)such as information on the stage shift resulting from more frequent screening (14)and few such data exist.
We conducted an observational study to investigate whether women diagnosed with breast cancer after having screening mammograms separated by 2 years are more likely to be diagnosed with advanced-stage tumors or other adverse tumor characteristics (e.g., being estrogen receptor [ER] negative) than those diagnosed with breast cancer after having mammograms separated by 1 year. We examined the association between screening interval and tumor characteristics among women stratified by age and breast density to clarify whether the groups that have lower mammographic sensitivity [i.e., women younger than 50 years and those with mammographically dense breasts (1519)] would benefit more from annual screening than groups with higher mammographic sensitivity (i.e., older women and those with predominantly fatty breasts). We defined the screening interval as the time between a womans two most recent screening mammograms, and we followed women with a 2-year screening interval for 2 years, to ascertain cancer occurrence, and those with a 1-year interval for 1 year, as would occur in a randomized trial. Thus we attempted to capture the two ways in which a longer interval might lead to more advanced disease: more late-stage disease detected at screening because of the longer time tumors would have grow since the prior screen, and more late-stage disease detected clinically after the last screen, because of the longer interval until the next mammographic examination during which cancers could become symptomatic or palpable. For this analysis, we used information from the Breast Cancer Surveillance Consortium, which includes information on over 4 000 000 mammograms and subsequent cancers and that reflects the effectiveness of mammography as routinely practiced in the United States. The use of this resource yielded a large number of breast cancer cases (7840) that met our definition of a 1- or 2-year mammography screening interval, allowing stratification by age and breast density.
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SUBJECTS AND METHODS |
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Information was collected by mammography registries that participate in the National Cancer Institutefunded Breast Cancer Surveillance Consortium. Detailed methods of the consortium have previously been described (20). Briefly, seven sites across the United States collect information from 176 mammography facilities. Information is obtained on the womans demographic and breast cancer risk factors and the mammography results for each mammogram. Each mammography registry links to a regional Surveillance, Epidemiology, and End Results1 (SEER) program or to a state tumor registry that provides information on cancer occurrences, including screen-detected and interval-detected cancers. Five of the seven registries (the exceptions are those in California and Colorado) also link to pathology laboratory records. Cancer ascertainment is estimated to be more than 94% complete (21). Data collected by all seven registries in the Breast Cancer Surveillance Consortium were included in this study: Carolina Mammography Registry, Chapel Hill, North Carolina; Colorado Mammography Project, Denver, Colorado; New Hampshire Mammography Network, Lebanon, New Hampshire; New Mexico Mammography Project, Albuquerque, New Mexico; San Francisco Mammography Registry, San Francisco, California; Vermont Breast Cancer Surveillance System, Burlington, Vermont; and Group Health Cooperative, Seattle, Washington. Each registry obtained approval from its Institutional Review Board to collect these data for this analysis.
Subject Selection and Study Design
We included women who were diagnosed with invasive breast cancer or ductal carcinoma in situ (DCIS) between January 1, 1996, and December 31, 2001, at or following a screening mammographic examination at age 4089 years. We excluded women with a personal history of breast cancer, either by self-report or by a prior diagnosis recorded in the cancer registry, and women who were diagnosed only with lobular carcinoma in situ or with phyllodes, sarcoma, or lymphoma of the breast.
The study design is outlined in Fig. 1. We restricted the analyses to women with breast cancer who had two screening mammograms before their diagnosis. As shown in Fig. 1, the screening interval was defined as the time between the two screening mammograms: a 1-year screening interval was defined as from 9 to 18 months (median 13 months) between mammograms, and a 2-year interval was defined as from more than 18 to 30 months (median 24 months) between mammograms. A mammographic examination was considered to be a screening examination if the radiologist recorded that the examination was for routine screening. Unilateral mammograms (which are likely to be diagnostic) and mammograms that occurred less than 9 months after a prior mammographic examination (which are likely to be a short-term follow-up of a prior examination) were not considered to be screening mammograms. The screening interval was determined by using the dates of prior mammography examinations recorded in each mammography registry (90% of women in the analysis) and self-reported information collected at the screening examination (10% of women).
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Data Collection
Information on tumor stage, grade, ER status, and tumor size was obtained from SEER cancer registries, state cancer registries, and pathology databases. All breast cancers were classified according to the American Joint Committee on Cancer (AJCC) staging system (22). Stage II cancers were separated by nodal status.
Information about demographic factors and breast cancer risk factors was obtained at the time of each mammography examination. Information included the womans birth date, race, ethnicity, current symptoms, whether she had had a breast biopsy, family history of breast cancer, menopausal status, current hormone therapy use, and the time since her last mammography examination. Women were considered to have a family history of breast cancer if they reported having at least one first-degree female relative with breast cancer. Women were considered to be postmenopausal if both ovaries had been removed, if their periods had stopped permanently, or if they were older than 55 years.
Mammographic breast density and mammographic examination assessments were recorded by radiologists at the mammography facilities. Most facilities coded breast density according to the four-category Breast Imaging Reporting and Data System (BI-RADS) terminology of the American College of Radiology (23). We defined dense breasts as ratings of "heterogeneously dense" or "extremely dense," and we defined fatty breasts as ratings of "entirely fat" or "scattered fibroglandular tissue." We considered a cancer to be screen-detected if it were diagnosed within 12 months of a positive mammographic examination (i.e., mammograms with BI-RADS assessment codes of 0, "needs additional evaluation;" 3, "probably benign" with immediate follow-up; 4, "suspicious for malignancy;" or 5, "highly suggestive of malignancy").
Statistical Analyses
Four tumor characteristics (stage, size, grade, and ER status) were dichotomized into adverse characteristics (late stage, tumor size >20 mm, grade III or IV, and ER-negative, respectively) and more favorable characteristics. Late-stage breast cancer was defined as having positive lymph nodes or metastases (lymph nodepositive stage II or stage III or IV). For the dichotomized stage variable, we considered women with positive lymph nodes as having late-stage breast cancer, even if the AJCC stage was unknown. We evaluated the likelihood of diagnosis with each of the adverse versus more favorable cancer characteristics among breast cancer cases with a 2- versus 1-year screening interval by use of logistic regression models. We fit separate models by decade of age and separate models by the two categories of breast density. We adjusted for race, ethnicity, family history of breast cancer, and mammography registry, as well as for age at the index mammographic examination in our analyses of all ages combined and of the breast density subgroups. All statistical tests were two-sided.
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RESULTS |
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Table 2 shows the distribution of tumor characteristics by screening interval, and Table 3 shows the distribution of one of these characteristics, AJCC stage, by age at the index mammographic examination and screening interval. The statistical analysis of the data in Tables 2 and 3 is given in Table 4, which provides odds ratios (ORs) for the association of screening interval with adverse tumor characteristics by age group after adjustment for race and ethnicity, family history of breast cancer, and mammography registry. Further adjustment for menopausal status, hormone therapy use, prior breast biopsy, and breast lump or nipple discharge did not change the results (data not shown). Among women with breast cancer who were 4049 years old at their index mammogram, a greater proportion of those with a 2-year screening interval were diagnosed with late-stage disease than those with a 1-year screening interval (28% versus 21%, Table 3). This difference was similar regardless of whether the analysis included all breast cancers (OR = 1.35, 95% confidence interval [CI] = 1.01 to 1.81) or only invasive breast cancers (OR = 1.37, 95% CI = 1.00 to 186) (Table 4). Among women with breast cancer who were 5059 years old at their index mammogram, there was no difference between those who had a 2-year screening interval and those with a 1-year screening interval in the proportion with late stage at diagnosis (OR = 0.97, 95% CI = 0.75 to 1.25). Among women who were 60 years or older, those with a 2-year screening interval were more likely to be diagnosed with invasive disease versus DCIS than those with a 1-year screening interval (women age 6069 years at index mammogram: OR = 1.51, 95% CI = 1.11 to 2.09; women age 7089 years at index mammogram: OR = 1.52, 95% CI = 1.14 to 2.06), but they were not more likely to have late-stage disease (women age 6069 years at index mammogram: OR = 0.99, 95% CI = 0.72 to 1.35; women age 7089 years at index mammogram: OR = 0.88, 95% CI = 0.64 to 1.19). There were no differences in other tumor characteristics (i.e., tumor size, grade, or ER status; Tables 2 and 4) between women of any age group according to screening interval, except for a possible increase in the percentage of ER-negative tumors among 7089-year-old women who were screened at a 2-year interval.
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The association between screening interval and breast tumor characteristics did not differ between women with dense breasts and those with fatty breasts (Table 5).
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DISCUSSION |
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Our findings are generally consistent with those of previous studies. The two randomized trials on screening interval compared a 1-year interval with a 3-year interval. The earlier trial, which was conducted among women age 4049 years (5), found a greater proportion of interval-detected versus screen-detected cancers in the 3-year interval arm (39%) than in the 1-year interval arm (27%); however, mortality and stage distribution were not reported. In a more recent trial from the United Kingdom (6), almost 100 000 women age 5062 years were randomly assigned after a baseline screen to receive either annual screening mammograms for 3 years or a single screening mammographic examination 3 years after baseline. Tumors were statistically significantly larger in the 3-year interval group than the annual mammography group (34% versus 27% larger than 20 mm, P = 0.05), but there was no difference between the two screening interval groups in tumor stage at diagnosis or in the estimated risk of mortality based on tumor size, grade, and lymph node status. Kerlikowske et al. (24) performed a meta-analysis of the association between screening interval and mortality across eight randomized controlled trials that varied in the length of the screening interval among the trials (rather than within the trials). Mortality reductions for screening every 1833 months were similar to reductions for annual screening for both women aged 4049 and those aged 5074. However only two of the trials included in the meta-analysis screened women in their forties annually (25,26), and these trials had different findings.
Most of the other observational studies that have looked at screening interval used a different definition of screening interval than the one we used, and all had much smaller sample sizes (n = 90 to 275 cancers in the 1- or 2-year interval groups) (710). Most of those studies defined screening interval as the time between the prior screen and diagnosis, which erroneously assigns all interval cancers diagnosed during the first year after a screening exam to the 1-year screening interval group, regardless of the actual interval between the two screening mammograms before the diagnosis. Miltenburg et al. (7) studied women who were diagnosed with breast cancer at age 5069 years and reported that women whose last screen was within 1 year before diagnosis and women whose last screen was 12 years before diagnosis had an identical and statistically significant (both P<0.05) 62% lower risk of death than unscreened women. Similarly, Kaas et al. (8) found no differences in the stage of contralateral breast cancer between breast cancer survivors who had had annual versus biennial screening. However, two other studies found that women who were screened annually had breast tumors that were smaller and less advanced than those who were screened every other year (9,10).
Our finding that women in their forties, but not older women, who received annual versus biennial screening had a reduced risk of late-stage disease is consistent with other lines of evidence that women in their forties, but not older women, might achieve a benefit from annual screening. It is well known that mammography is less sensitive for younger women than for older women (16,17,19). Moreover, Peer et al. (16) reported that, among women younger than 50 years of age, mammography has a particularly low sensitivity for tumors that would arise clinically in the second year after the mammogram. In addition, it has been shown that breast tumors in younger women have a faster growth rate (27,28) and a shorter sojourn time (detectable preclinical period) than those in older women (29). If, as estimated by Tabar et al. (29), the tumor sojourn time is 1.7 years for women age 4049 years and 2.63.8 years for women age 5074 years, then annual screening might be expected to provide a benefit over biennial screening for women in their forties but not for women 50 years or older.
Our finding that, among women age 60 years or older, those with a 2-year screening interval had a smaller proportion of DCIS, a greater proportion of stage I disease, and a similar proportion of stage IIIV disease compared with women of that age with a 1-year screening interval (Table 3) deserves mention. Whereas survival is high for stage I disease, an increase of stage I disease and a decrease in stage 0 disease among older women with a 2-year interval could mean that more such women would need to undergo chemotherapy. Alternatively it is possible that women with a 2-year interval had no more stage I disease than women with a 1-year interval but, rather, had less in situ disease, leading to a greater proportion of stage I disease among all tumors. Consistent with this possibility, the U.K. mammography trial (6) reported a 25% increase in the incidence of DCIS among women randomly assigned to the annual versus 3-year screening interval, which may constitute overdiagnosis of tumors that would not affect a womans survival.
We found no evidence that annual versus biennial screening provides more benefit to women with mammographically dense breasts than to women with predominantly fatty breasts. To our knowledge, we are the first to report on this issue. We found no advantage of annual screening for one group with low mammographic sensitivitywomen with dense breastsalthough we found some benefit for another group with low mammographic sensitivitywomen under age 50. This difference may reflect different biologic mechanisms for the low sensitivity in these two groups. The reduced sensitivity among younger women appears to be a result of both a faster tumor growth rate and the masking effect of density (30). However, the reduced sensitivity associated with increased breast density (independent of age) (15,1719) appears to be caused by tumor masking only, because density is not associated with tumor growth rate (31). Thus, it is possible that a shorter screening interval reduces some of the adverse outcomes (e.g., late stage at diagnosis) that are associated with faster tumor growth, but not the adverse outcomes that are associated with the masking effect of breast density.
One important use of data such as ours is in mathematical models that predict the effectiveness or cost-effectiveness of various screening strategies (12,14,3235). Results of several past analyses (31,34,35) have indicated that a shorter screening interval provides a mortality advantage for women in their forties but little improvement in mortality for older women, similar to the results of our study. However, because breast cancer incidence among women aged 4049 years is less than half that among women 50 years of age or older (36), the benefit of annual screening for younger women is small and the cost per year of life saved is high (32).
Observational studies of screening, such as ours, are methodologically challenging. The strengths of this study are the very large number of cases, the use of data from the Breast Cancer Surveillance Consortium, and the methodologic approach of using the time between the two screening mammograms before the breast cancer diagnosis to define the screening interval and using the screening interval (1 versus 2 years) as the follow-up period for cancer ascertainment. Nonetheless, observational studies, such as this one, have inherent limitations compared with randomized trials. One limitation of this study is that all women with a 2-year interval between two screening mammograms were not followed for interval cancers for the full 2 years after the second mammogram, as they would have been in a randomized trial. Instead, some women with a 2-year interval between their two prior mammograms returned for their next screen after about 1 year (at which time they met our definition of being on a 1-year screening interval). This problem would lead to fewer interval cancers occurring in the 1324-month follow-up period, and these cancers would presumably have included more advanced cases. Thus, there could be a greater difference in the percentage of women with late-stage disease between the 2-year and 1-year screening interval groups than what we observed. We investigated the magnitude of this potential bias by comparing the timing of interval cancer diagnosis for our full study sample with that of one registry for a health maintenance organization (HMO) that has a recommended 2-year mammography screening interval for most women. For women with a 2-year screening interval, the mean time from screening to diagnosis for those in the HMO site was 14.5 months, which is similar to the mean time to diagnosis in the full sample of 13.6 months. Thus, we believe that truncating the follow-up interval at the time of the womans next screen did not have a major effect on our results.
One difference between our design and a randomized trial is that in a trial all women who were free of cancer at a baseline mammogram would be followed from that mammogram and contribute endpoints to their assigned screening interval group, even if a woman developed cancer before her second mammogram. In our study, each women had to be free from cancer at a mammogram and between that mammogram and her next mammogram to determine if she was on a 1- or 2-year screening interval. Thus, it may appear that in our study we omit 1 year of cancers for women who would have been on a 1-year interval, and we omit 2 years of cancers for women who would have been on a 2-year interval. But we compensate for these apparent omissions by attempting to follow up women on a 2-year interval for 2 years after their index mammogram and women on a 1-year interval for 1 year after their index mammogram, whereas a randomized trial would end follow-up with each womans last mammogram. In other words, each round in a randomized trial would be a 1- or 2-year interval ending with a mammogram, whereas in our study each "round" is a mammogram followed by a 1-or 2-year interval. We do not think this difference would bias our results.
Another limitation of the observational design of our study is that the screening interval (1-year or 2-year) was selected by each woman or her health care provider. Thus, our results could be biased if characteristics that are associated with choice of screening interval also predict adverse tumor characteristics. However, we controlled for age, race/ethnicity, family history of breast cancer, and mammography registry, and further adjustment for other factors did not modify our results. Our choice of a breast canceronly analysis (i.e., investigation of the proportion of cases with late-stage disease rather than incidence of late stage of disease in the population) mitigates the issue that women with a higher risk of breast cancer may be more likely to have a shorter screening interval. Had we studied the incidence of late-stage breast cancer, women with a shorter screening interval might have appeared to be at higher risk of late-stage disease than women with a longer screening interval because they are at higher risk of breast cancer at all stages, regardless of screening interval.
Missing or inaccurate data is another limitation of our study. For 10% of the women in our study, the length of the screening interval was based on self-reports, which are less accurate than clinical data (37). The mammographers reports of whether each mammographic examination was for screening or diagnosis could also be in error. However, when we omitted women with self-reports of screening interval or women with self-reported symptoms at a screening mammogram, the results did not change substantively. The proportion of missing data was high for breast density, tumor grade, and ER status and varied somewhat by screening interval. However, most missing data were a result of noncollection of certain variables by some radiology facilities (for breast density) or tumor registries (for tumor grade and ER status). Thus, the missing data would be unlikely to be jointly related to screening interval and stage of disease and therefore unlikely to bias our results.
A final limitation of our study is that we used late stage at diagnosis and other adverse tumor characteristics, rather than mortality, as the outcome. Thus we cannot know with certainty whether our finding of an increase in late stage at diagnosis for younger women with a 2-year screening interval versus a 1-year would translate into mortality differences over time. However, our use of late-stage disease at diagnosis as a surrogate end point for mortality is supported by results of a mass mammography screening trial in Sweden (29), which reported similar percent reductions in stage II or more advanced breast cancers (25%) and in mortality (31%) in screened versus unscreened women.
In summary, we found little evidence that indicates that women who undergo mammography screening every 2 years have an increased risk of late-stage breast cancer compared with women who undergo annual screening, except for women in their forties. Our results may be useful for policy makers and for statistical modelers of mammography screening who seek to understand the costs and benefits of screening annually versus every 2 years.
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NOTES |
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This research was supported by NCI-funded Breast Cancer Surveillance Consortium cooperative agreements (U01CA63740, U01CA86076, U01CA86082, U01CA63736, U01CA70013, U01CA69976, U01CA63731, U01CA70040) (http://breastscreening.cancer.gov/).
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Manuscript received April 12, 2004; revised October 5, 2004; accepted October 14, 2004.
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