The DOI matches its Crossref record.
Endogenous Sex Hormones and Breast Cancer in Postmenopausal Women: Reanalysis of Nine Prospective Studies
Abstract
BACKGROUND: Reproductive and hormonal factors are involved in the etiology of breast cancer, but there are only a few prospective studies on endogenous sex hormone levels and breast cancer risk. We reanalyzed the worldwide data from prospective studies to examine the relationship between the levels of endogenous sex hormones and breast cancer risk in postmenopausal women. METHODS: We analyzed the individual data from nine prospective studies on 663 women who developed breast cancer and 1765 women who did not. None of the women was taking exogenous sex hormones when their blood was collected to determine hormone levels. The relative risks (RRs) for breast cancer associated with increasing hormone concentrations were estimated by conditional logistic regression on case-control sets matched within each study. Linear trends and heterogeneity of RRs were assessed by two-sided tests or chi-square tests, as appropriate. RESULTS: The risk for breast cancer increased statistically significantly with increasing concentrations of all sex hormones examined: total estradiol, free estradiol, non-sex hormone-binding globulin (SHBG)-bound estradiol (which comprises free and albumin-bound estradiol), estrone, estrone sulfate, androstenedione, dehydroepiandrosterone, dehydroepiandrosterone sulfate, and testosterone. The RRs for women with increasing quintiles of estradiol concentrations, relative to the lowest quintile, were 1.42 (95% confidence interval [CI] = 1.04 to 1.95), 1.21 (95% CI = 0.89 to 1.66), 1.80 (95% CI = 1.33 to 2.43), and 2.00 (95% CI = 1.47 to 2.71; P(trend)<.001); the RRs for women with increasing quintiles of free estradiol were 1.38 (95% CI = 0.94 to 2.03), 1.84 (95% CI = 1.24 to 2.74), 2.24 (95% CI = 1.53 to 3.27), and 2.58 (95% CI = 1.76 to 3.78; P(trend)<.001). The magnitudes of risk associated with the other estrogens and with the androgens were similar. SHBG was associated with a decrease in breast cancer risk (P(trend) =.041). The increases in risk associated with increased levels of all sex hormones remained after subjects who were diagnosed with breast cancer within 2 years of blood collection were excluded from the analysis. CONCLUSION: Levels of endogenous sex hormones are strongly associated with breast cancer risk in postmenopausal women.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cited by
Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms
Calle, E. E., & Kaaks, R. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1408 · Cited by 3,613
The relation between different dimensions of alcohol consumption and burden of disease: an overview
Rehm, J., Baliunas, D., Borges, G. L. G., Graham, K., Irving, H., Kehoe, T., Parry, C. D., Patra, J., Popova, S., Poznyak, V., et al. (2010) · Addiction · doi:10.1111/j.1360-0443.2010.02899.x · Cited by 1,174
Body mass index, serum sex hormones, and breast cancer risk in postmenopausal women
Endogenous Hormones Breast Cancer Collaborative Group (2003) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djg022 · Cited by 1,093
Exemestane for Breast-Cancer Prevention in Postmenopausal Women
Goss, P. E., Ingle, J. N., Alés-Martínez, J. E., Cheung, A. M., Chlebowski, R. T., Wactawski-Wende, J., McTiernan, A., Robbins, J., Johnson, K. C., Martin, L. W., et al. (2011) · New England Journal of Medicine · doi:10.1056/nejmoa1103507 · Cited by 970
Harvie, M. N., Pegington, M., Mattson, M. P., Frystyk, J., Dillon, B., Evans, G., Cuzick, J., Jebb, S. A., Martin, B., Cutler, R. G., et al. (2011) · International Journal of Obesity · doi:10.1038/ijo.2010.171 · Cited by 804
Plottel, C. S., & Blaser, M. J. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.10.003 · Cited by 743
Obesity and cancer: the role of dysfunctional adipose tissue
van Kruijsdijk, R. C. M., van der Wall, E., & Visseren, F. L. J. (2009) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-09-0372 · Cited by 715
Adult Weight Change and Risk of Postmenopausal Breast Cancer
Eliassen, A. H., Colditz, G. A., Rosner, B., Willett, W. C., & Hankinson, S. E. (2006) · JAMA · doi:10.1001/jama.296.2.193 · Cited by 654
The Nurses׳ Health Study: lifestyle and health among women
Colditz, G. A., & Hankinson, S. E. (2005) · Nature reviews. Cancer · doi:10.1038/nrc1608 · Cited by 590
Genome-wide association study identifies a new breast cancer susceptibility locus at 6q25.1
Zheng, W., Long, J., Gao, Y.-T., Li, C., Zheng, Y., Xiang, Y.-B., Wen, W., Levy, S., Deming, S. L., Haines, J. L., et al. (2009) · Nature Genetics · doi:10.1038/ng.318 · Cited by 541
Health benefits of resveratrol: Evidence from clinical studies
Singh, A. P., Singh, R., Verma, S. S., Rai, V., Kaschula, C. H., Maiti, P., & Gupta, S. C. (2019) · Medicinal Research Reviews · doi:10.1002/med.21565 · Cited by 523
Physical Activity and Breast Cancer: A Systematic Review
Monninkhof, E. M., Elias, S. G., Vlems, F. A., van der Tweel, I., Schuit, A. J., Voskuil, D. W., & van Leeuwen, F. E. (2007) · Epidemiology · doi:10.1097/01.ede.0000251167.75581.98 · Cited by 503
Obesity and cancer risk: the role of the insulin-IGF axis
Renehan, A. G., Frystyk, J., & Flyvbjerg, A. (2006) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2006.08.006 · Cited by 480
Obesity, adipocytokines, and insulin resistance in breast cancer
Rose, D. P., Komninou, D., & Stephenson, G. D. (2004) · Obesity Reviews · doi:10.1111/j.1467-789x.2004.00142.x · Cited by 460
Challenges to the measurement of estradiol: an Endocrine Society Position Statement
Rosner, W., Hankinson, S. E., Sluss, P. M., Vesper, H. W., & Wierman, M. E. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3780 · Cited by 408
(2013) · The Lancet Oncology · doi:10.1016/s1470-2045(13)70301-2 · Cited by 399
Breast cancer in postmenopausal women is associated with an altered gut metagenome
Zhu, J., Liao, M., Yao, Z., Liang, W., Li, Q., Liu, J., Yang, H., Ji, Y., Wei, W., Tan, A., et al. (2018) · Microbiome · doi:10.1186/s40168-018-0515-3 · Cited by 377
Androgen therapy in women: a reappraisal: an Endocrine Society Clinical Practice Guideline
Wierman, M. E., Arlt, W., Basson, R., Davis, S. R., Miller, K. K., Murad, M. H., Rosner, W., & Santoro, N. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-2260 · Cited by 363
Oestrogen exposure and breast cancer risk
Travis, R. C., & Key, T. J. (2003) · Breast Cancer Research · doi:10.1186/bcr628 · Cited by 346
Fuhrman, B. J., Feigelson, H. S., Flores, R., Gail, M. H., Xu, X., Ravel, J., & Goedert, J. J. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-2222 · Cited by 339
Relation of BMI and physical activity to sex hormones in postmenopausal women
McTiernan, A., Wu, L., Chen, C., Chlebowski, R., Mossavar‐Rahmani, Y., Modugno, F., Perri, M. G., Stanczyk, F. Z., Van Horn, L., Wang, C. Y., et al. (2006) · Obesity · doi:10.1038/oby.2006.191 · Cited by 327
Grace, P. B., Taylor, J. I., Low, Y.-L., Luben, R. N., Mulligan, A. A., Botting, N. P., Dowsett, M., Welch, A. A., Khaw, K.-T., Wareham, N. J., et al. (2004) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.698.13.5 · Cited by 264
Tamimi, R. M., Byrne, C., Colditz, G. A., & Hankinson, S. E. (2007) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djm062 · Cited by 258
Shift work and cancer – considerations on rationale, mechanisms, and epidemiology
Costa, G., Haus, E., & Stevens, R. (2010) · Scandinavian Journal of Work, Environment & Health · doi:10.5271/sjweh.2899 · Cited by 241
Neilson, H. K., Friedenreich, C. M., Brockton, N. T., & Millikan, R. C. (2009) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-08-0756 · Cited by 232
Age at Menarche in Relation to Adult Height
Onland-Moret, N. C., Peeters, P. H. M., van Gils, C. H., Clavel-Chapelon, F., Key, T., Tjønneland, A., Trichopoulou, A., Kaaks, R., Manjer, J., Panico, S., et al. (2005) · American Journal of Epidemiology · doi:10.1093/aje/kwi260 · Cited by 227
Influence of Sex Hormones on Cancer Progression
Folkerd, E. J., & Dowsett, M. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2009.27.4290 · Cited by 229
Effects of estrogen on breast cancer development: Role of estrogen receptor independent mechanisms
Yue, W., Wang, J., Li, Y., Fan, P., Liu, G., Zhang, N., Conaway, M., Wang, H., Korach, K. S., Bocchinfuso, W., et al. (2010) · International Journal of Cancer · doi:10.1002/ijc.25207 · Cited by 196
Ennour-Idrissi, K., Maunsell, E., & Diorio, C. (2015) · Breast Cancer Research · doi:10.1186/s13058-015-0647-3 · Cited by 193
Childhood soy intake and breast cancer risk in Asian American women
Korde, L. A., Wu, A. H., Fears, T., Nomura, A. M. Y., West, D. W., Kolonel, L. N., Pike, M. C., Hoover, R. N., & Ziegler, R. G. (2009) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-08-0405 · Cited by 181
Plasma phytoestrogens and subsequent breast cancer risk
Verheus, M., van Gils, C. H., Keinan-Boker, L., Grace, P. B., Bingham, S. A., & Peeters, P. H. M. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2006.06.0244 · Cited by 166
Melatonin and Breast Cancer: A Prospective Study
Travis, R. C., Allen, D. S., Fentiman, I. S., & Key, T. J. (2004) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djh077 · Cited by 149
Goedert, J. J., Hua, X., Bielecka, A., Okayasu, I., Milne, G. L., Jones, G. S., Fujiwara, M., Sinha, R., Wan, Y., Xu, X., et al. (2018) · British Journal of Cancer · doi:10.1038/bjc.2017.435 · Cited by 144
Baglietto, L., English, D. R., Hopper, J. L., MacInnis, R. J., Morris, H. A., Tilley, W. D., Krishnan, K., & Giles, G. G. (2009) · Breast Cancer Research and Treatment · doi:10.1007/s10549-008-0069-3 · Cited by 134
Qureshi, R., Picon-Ruiz, M., Aurrekoetxea-Rodriguez, I., Nunes de Paiva, V., D’Amico, M., Yoon, H., Radhakrishnan, R., Morata-Tarifa, C., Ince, T., Lippman, M. E., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.05.008 · Cited by 127
Thaler, M. A., Seifert-Klauss, V., & Luppa, P. B. (2015) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2015.06.005 · Cited by 125
Kaaks, R., Bellati, C., Venturelli, E., Rinaldi, S., Secreto, G., Biessy, C., Pala, V, Sieri, S., & Berrino, F. (2003) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1601647 · Cited by 120
Racial differences in premenopausal endogenous hormones
Pinheiro, S. P., Holmes, M. D., Pollak, M. N., Barbieri, R. L., & Hankinson, S. E. (2005) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-04-0944 · Cited by 119
Effects of a 2-year randomized soy intervention on sex hormone levels in premenopausal women
Maskarinec, G., Franke, A. A., Williams, A. E., Hebshi, S., Oshiro, C., Murphy, S., & Stanczyk, F. Z. (2004) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.1736.13.11 · Cited by 92
Mabrok, H. B., Klopfleisch, R., Ghanem, K. Z., Clavel, T., Blaut, M., & Loh, G. (2012) · Carcinogenesis · doi:10.1093/carcin/bgr256 · Cited by 89
The metabolism, analysis, and targeting of steroid hormones in breast and prostate cancer
Capper, C. P., Rae, J. M., & Auchus, R. J. (2016) · Hormones and Cancer · doi:10.1007/s12672-016-0259-0 · Cited by 89
Endogenous oestrogens and breast cancer risk in premenopausal and postmenopausal women
Key, T. J. (2011) · Steroids · doi:10.1016/j.steroids.2011.02.029 · Cited by 89
Tworoger, S. S., Missmer, S. A., Eliassen, A. H., Barbieri, R. L., Dowsett, M., & Hankinson, S. E. (2007) · Cancer Causes & Control · doi:10.1007/s10552-007-9017-5 · Cited by 78
Hedelin, M., Löf, M., Olsson, M., Adlercreutz, H., Sandin, S., & Weiderpass, E. (2008) · The Journal of Nutrition · doi:10.1093/jn/138.5.938 · Cited by 75
Tin Tin, S., Reeves, G. K., & Key, T. J. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01392-z · Cited by 71
Thompson, D. J., Healey, C. S., Baynes, C., Kalmyrzaev, B., Ahmed, S., Dowsett, M., Folkerd, E., Luben, R. N., Cox, D., Ballinger, D., et al. (2008) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-08-0734 · Cited by 61
Potentially functional polymorphisms in ESR1 and breast cancer risk: a meta-analysis
Li, N., Dong, J., Hu, Z., Shen, H., & Dai, M. (2010) · Breast Cancer Research and Treatment · doi:10.1007/s10549-009-0532-9 · Cited by 56
DHEAS levels and mortality in disabled older women: the Women's Health and Aging Study I
Cappola, A. R., Xue, Q.-L., Walston, J. D., Leng, S. X., Ferrucci, L., Guralnik, J., & Fried, L. P. (2006) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/61.9.957 · Cited by 49
Silva, I. D. S., Mangtani, P., McCormack, V., Bhakta, D., McMichael, A. J., & Sevak, L. (2004) · Cancer Causes & Control · doi:10.1023/b:caco.0000043431.85706.d8 · Cited by 48
A controlled 2-mo dietary fat reduction and soy food supplementation study in postmenopausal women
Wu, A. H., Stanczyk, F. Z., Martinez, C., Tseng, C.-C., Hendrich, S., Murphy, P., Chaikittisilpa, S., Stram, D. O., & Pike, M. C. (2005) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/81.5.1133 · Cited by 47
Circulating Sex Steroids and Breast Cancer Risk in Premenopausal Women
Hankinson, S. E., & Eliassen, A. H. (2010) · Hormones and Cancer · doi:10.1007/s12672-009-0003-0 · Cited by 44
Menopausal hormone therapy and breast cancer
Santen, R. J. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2013.06.010 · Cited by 41
Naturally Occurring Mutants Inform SHBG Structure and Function
Wu, T.-S., & Hammond, G. L. (2014) · Molecular Endocrinology · doi:10.1210/me.2014-1058 · Cited by 40
Richardson, H., Ho, V., Pasquet, R., Singh, R. J., Goetz, M. P., Tu, D., Goss, P. E., & Ingle, J. N. (2020) · Menopause · doi:10.1097/gme.0000000000001568 · Cited by 37
Oh, H., Coburn, S. B., Matthews, C. E., Falk, R. T., LeBlanc, E. S., Wactawski-Wende, J., Sampson, J., Pfeiffer, R. M., Brinton, L. A., Wentzensen, N., et al. (2017) · Breast Cancer Research · doi:10.1186/s13058-017-0810-0 · Cited by 36
Modeling motor neuron disease: the matter of time
Arbab, M., Baars, S., & Geijsen, N. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.07.008 · Cited by 33
Kalogera, E., Pistos, C., Provatopoulou, X., Athanaselis, S., Spiliopoulou, C., & Gounaris, A. (2013) · Journal of Chromatography B · doi:10.1016/j.jchromb.2013.09.022 · Cited by 31
Urinary sex steroid excretion levels during a soy intervention among young girls: a pilot study
Maskarinec, G., Morimoto, Y., Novotny, R., Nordt, F. J., Stanczyk, F. Z., & Franke, A. A. (2005) · Nutrition and Cancer · doi:10.1207/s15327914nc5201_3 · Cited by 26
Ihenacho, U., Sriprasert, I., Mack, W. J., Hamilton, A. S., Unger, J. B., Press, M. F., & Wu, A. H. (2022) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntac066 · Cited by 20
Coburn, S. B., Dionne-Odom, J., Alcaide, M. L., Moran, C. A., Rahangdale, L., Golub, E. T., Massad, L. S., Seidman, D., Michel, K. G., Minkoff, H., et al. (2022) · Journal of Women's Health · doi:10.1089/jwh.2021.0276 · Cited by 18
Sivik, T., Gunnarsson, C., Fornander, T., Nordenskjöld, B., Skoog, L., Stål, O., & Jansson, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040568 · Cited by 17
Metadata
- Authors
- The Endogenous Hormones and Breast Cancer Collaborative Group
- Venue
- CancerSpectrum Knowledge Environment
- Publisher
- Oxford University Press (OUP)
- Published
- 2002-04-17
- Volume
- 94
- Issue
- 8
- Pages
- 606-616
- ISSN
- 0027-8874 (ISSN-L)
- 1460-2105
- OpenAlex
- W1511930757
- Cited by
- 1,793
- References
- 0
- FWCI
- 29.61
- Type
- journal article
- Language
- en
- Open access
- closed
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.