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Endogenous Sex Hormone Levels and Mammographic Density Among Postmenopausal Women

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Endogenous Sex Hormone Levels and Mammographic Density Among Postmenopausal Women 2641 Endogenous Sex Hormone Levels and Mammographic Density among Postmenopausal Women Rulla M. Tamimi,1,2 Susan E. Hankinson,1,2 Graham A. Colditz,1,2,3 and Celia Byrne4 1Channing Laboratory, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School; 2Department of Epidemiology, Harvard School of Public Health; 3Harvard Center for Cancer Prevention, Boston, Massachusetts; and 4Cancer Genetics and Epidemiology Program, Lombardi Comprehensive Cancer Center, Georgetown University, Washington, District of Columbia Abstract Background: Mammographic density is one of the strongest density. The mean percent mammographic density was predictors of breast cancer risk. The mechanism by which 25.6% among women in the lowest quartile of circulating breast density increases breast cancer risk is unclear estradiol compared with 14.4% among women in the highest although it has been hypothesized that breast density quartile [Spearman correlation (r)=À0.22, P < 0.0001]. reflects cumulative exposure to estrogens. Circulating estrogens alone explained 1% to 5% of the Methods: To evaluate this hypothesis, we conducted a cross- variation of mammographic density. Body mass index was sectional study among 520 postmenopausal women in the positively associated with circulating estradiol levels Nurses’ Health Study that examined the relation between (r = 0.45, P < 0.0001) and inversely related to percent circulating sex hormones and mammographic density. mammographic density (r = À0.51, P < 0.0001). After Women were postmenopausal and not taking exogenous adjustment for body mass index, there was no association hormones at the time of blood collection and mammogram. between estradiol and breast density (r = 0.01, P = 0.81). Percent breast density was measured from digitized mam- Likewise, there was no relation between the other sex mograms using a computer-assisted method. Circulating hormones measured or prolactin and mammographic density estrone, estradiol, androstenedione, testosterone, DHEA, after adjustment for body mass index. DHEA sulfate, sex hormone–binding globulin, progesterone, Conclusion: These findings indicate that in postmenopausal and prolactin were measured in plasma. women, mammographic density is independent of circulat- Results: In contrast to the prior hypothesis, circulating ing sex hormone levels. (Cancer Epidemiol Biomarkers Prev estrogens were inversely related to percent mammographic 2005;14(11):2641–7) Introduction Mammographic density is one of the strongest predictors of association between mammographic density and breast cancer breast cancer risk (1). Women with z75% breast density are at is due to elevated levels of circulating estrogens. Based on a 4- to 6-fold greater risk of breast cancer than women with no these data, it has been hypothesized that breast density density (1, 2). The radiographic appearance of the breast on a represents cumulative exposure to estrogens (14). The purpose mammogram varies depending on the composition of the of the current study was to directly examine the relation breast. Fat is radiolucent and appears dark on a film screen between endogenous estrogens, androgens, progesterone, mammogram. In contrast, epithelial cells and connective tissue prolactin, and sex hormone–binding globulin (SHBG) and are radiodense. They appear light on a mammogram and are mammographic density among postmenopausal women not considered to be ‘‘mammographically dense.’’ currently on exogenous hormones. The mechanism by which mammographic density increases breast cancer risk is unclear although it has been hypothesized that breast density represents increased cellular proliferation. Materials and Methods There is evidence that use of exogenous hormones increases mammographic density (3-9), and combined formulations of Study Design and Population. The Nurses’ Health Study estrogen and progestin may have the most pronounced effects was initiated in 1976 when 121,700 U.S. registered nurses ages (6, 8, 9). Clinical trials have shown that treatment with 30 to 55 years returned an initial questionnaire (15). Informa- tamoxifen, a selective estrogen receptor modulator with tion on body mass index (BMI), reproductive history, age at antiestrogenic effects in the breast, reduces breast density menopause, and postmenopausal hormone use as well as (10-13). The associations of exogenous hormones and tamox- diagnosis of cancer and other diseases are updated every 2 ifen with mammographic density suggest that endogenous years through questionnaires. During 1989 and 1990, blood estrogens may influence breast density and that the positive samples were collected from 32,826 women. Detailed infor- mation regarding blood collection methods has been published (16). In general, blood samples were returned within 26 hours of blood draw; immediately centrifuged; aliquoted into Received 7/27/05; revised 8/19/05; accepted 9/1/05. plasma, RBC, and buffy coat fractions; and stored in liquid Grant support: USPHS grants CA087969, CA049449, and CA075016; Specialized Programs of Research Excellence in Breast Cancer grant CA089393 from the National Cancer Institute, nitrogen freezers. The follow-up rate among women who NIH, Department of Health and Human Services and Breast Cancer Research Fund; and provided blood samples was 99% through 1998. American Cancer Society Cissy Hornung Clinical Research Professorship (G.A. Colditz). We conducted a cross-sectional analysis among controls The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. from a breast cancer case-control study nested within the Section 1734 solely to indicate this fact. Nurses’ Health Study cohort. This nested case-control study Requests for reprints: Rulla M. Tamimi, Channing Laboratory, Department of Medicine, examined plasma sex steroid hormones and breast cancer risk Brigham and Women’s Hospital and Harvard Medical School, 181 Longwood Avenue, Boston, MA 02115. Phone: 617-525-0862. E-mail: [email protected]. and included breast cancer cases diagnosed after blood Copyright D 2005 American Association for Cancer Research. collection but before June 1, 1998, and matched controls (17). doi:10.1158/1055-9965.EPI-05-0558 There were 655 potential postmenopausal controls who had no Cancer Epidemiol Biomarkers Prev 2005;14(11). November 2005 Downloaded from cebp.aacrjournals.org on September 28, 2021. © 2005 American Association for Cancer Research. 2642 Endogenous Sex Hormones and Mammographic Density history of cancer and were not taking postmenopausal DHEA sulfate in 5 samples, for progesterone in 176 samples, hormones at the time of blood collection or during the 3 and for testosterone in 2 samples. When plasma hormone months prior. At the time of mammography collection, 631 values were reported as less than the detectable limit, we set participants were alive and eligible to receive letters for the value to half the detectable limit. participation in this study. Five hundred sixty-two (89.1%) We used the extreme Studentized deviate many-outlier women gave permission to obtain mammograms, whereas 4% procedure to determine outlying hormone values by batch refused, 4% reported never having a mammogram, 2% did not (27). This process resulted in the exclusion of one estrone respond, and 1% could not recall if they had a mammogram. value, two estradiol values, one estrone sulfate value, three For all consenting women, we attempted to obtain the androstenedione values, and one testosterone value. There was mammograms taken before and as close to the date of blood insufficient plasma for all subjects to have measurements on collection as possible. We successfully obtained mammograms the all hormones. Final numbers are presented in Table 3A-C. from 540 controls (96.1% of those consenting). The median time between mammography and blood draw was 8 months Mammographic Density Measurements. To assess mam- (interquartile range, 2.5 years before to 1 month after). Women mographic density, the craniocaudal views of both breasts A for whom we obtained mammograms were very similar to were digitized at 261 m/pixel with a Lumysis 85 laser film those whom we were unable to get mammograms with respect scanner, which covers a range of 0 to 4.0 absorbance. The to age, BMI, and circulating hormone levels. We excluded five software for computer-assisted thresholding was developed at women whose mammograms were not film mammograms. the University of Toronto (28). The film screen images were Because menopausal status and postmenopausal hormone use digitized and viewed on the computer screen. For each image, are associated with both hormone levels and mammographic the observer set one threshold level to define the edge of the density, we restricted all analyses to women who were breast and a second threshold delineating the dense area of the postmenopausal and not taking exogenous hormones at the breast within the original threshold region. The Cumulus time of both mammography and blood collection (n = 520). This software calculated the total number of pixels within the entire study was approved by the Committee on the Use of Human region of interest and within the area identified as dense. Subjects in Research at Brigham and Women’s Hospital. Using these values, the software program calculated the percentage of the breast area that was dense. This measure Laboratory Analyses. Estrone, estradiol, non-SHBG–bound of mammographic breast density
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