Premenopausal serum androgens and breast cancer risk: A nested case-control study

Breast Cancer Research

Volumn 14, Issue 1, 2012, Pages

  Zeleniuch Jacquotte, Anne ^a   Afanasyeva, Yelena ^a   Kaaks, Rudolf ^b   Rinaldi, Sabina ^c   Scarmo, Stephanie ^a   Liu, Mengling ^a   Arslan, Alan A ^a   Toniolo, Paolo ^a,d   Shore, Roy E ^a,e   Koenig, Karen L ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

^d LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^e RADIATION EFFECTS RESEARCH FOUNDATION   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROSTENEDIONE; ESTROGEN RECEPTOR; PRASTERONE; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE; ANDROGEN; PRASTERONE SULFATE;

ADULT; AGE; AGED; ANDROGEN BLOOD LEVEL; ARTICLE; BLOOD DONOR; BREAST CANCER; CANCER CLASSIFICATION; CANCER INVASION; CANCER RISK; CARCINOMA IN SITU; CASE CONTROL STUDY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ASSOCIATION; FAMILY HISTORY; FEMALE; HUMAN; IMMUNOASSAY; MAJOR CLINICAL STUDY; MEASUREMENT; MENSTRUAL CYCLE; POSTMENOPAUSE; PREDICTIVE VALUE; PREMENOPAUSE; RELIABILITY; RISK ASSESSMENT; RISK FACTOR; BLOOD; BREAST TUMOR; INTRADUCTAL CARCINOMA; METABOLISM; MIDDLE AGED; PAGET NIPPLE DISEASE; RISK; STATISTICAL MODEL;

ADULT; AGED; ANDROGENS; ANDROSTENEDIONE; BREAST NEOPLASMS; CARCINOMA, DUCTAL, BREAST; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CASE-CONTROL STUDIES; DEHYDROEPIANDROSTERONE SULFATE; FEMALE; HUMANS; LOGISTIC MODELS; MIDDLE AGED; ODDS RATIO; PREMENOPAUSE; RISK FACTORS; SEX HORMONE-BINDING GLOBULIN; TESTOSTERONE;

EID: 84856882046     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3117     Document Type: Article

References (62)

1. The Endogenous Hormones Breast Cancer Collaborative Group Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J Natl Cancer Inst 2002, 94:606-616. 10.1093/jnci/94.8.606, 11959894, The Endogenous Hormones Breast Cancer Collaborative Group.
2. Kaaks R, Rinaldi S, Key TJ, Berrino F, Peeters PHM, Biessy C, Dossus L, Lukanova A, Bingham S, Khaw KT, Allen NE, Bueno-de-Mesquita HB, van Gils CH, Grobbee D, Boeing H, Lahmann PH, Nagel G, Chang Claude J, Clavel Chapelon F, Fournier A, Thibaut A, Gonzlez CA, Quirs JR, Tormo MJ, Ardanaz E, Amiano P, Krogh V, Palli D, Panico S, Tumino R, et al. Postmenopausal serum androgens, oestrogens and breast cancer risk: the European prospective investigation into cancer and nutrition. Endocr Relat Cancer 2005, 12:1071-1082. 10.1677/erc.1.01038, 16322344.
3. Woolcott C, Shvetsov Y, Stanczyk F, Wilkens L, White K, Caberto C, Henderson B, Le-Marchand L, Kolonel L, Goodman M. Plasma sex hormone concentrations and breast cancer risk in an ethnically diverse population of postmenopausal women: the Multiethnic Cohort Study. Endocr Relat Cancer 2010, 17:125-134. 10.1677/ERC-09-0211, 2880171, 19903744.
4. Missmer S, Eliassen AH, Barbieri R, Hankinson S. Endogenous estrogen, androgen, and progesterone concentrations and breast cancer risk among postmenopausal women. J Natl Cancer Inst 2004, 96:1856-1865. 10.1093/jnci/djh336, 15601642.
5. Zeleniuch-Jacquotte A, Shore RE, Koenig KL, Akhmedkhanov A, Afanasyeva Y, Kato I, Kim MY, Rinaldi S, Kaaks R, Toniolo P. Postmenopausal levels of estrogen, androgen, and SHBG and breast cancer risk: long-term results of a prospective study. Br J Cancer 2004, 90:153-159. 10.1038/sj.bjc.6601517, 2395327, 14710223.
6. Baglietto L, Severi G, English D, Krishnan K, Hopper J, McLean C, Morris H, Tilley W, Giles G. Circulating steroid hormone levels and risk of breast cancer for postmenopausal women. Cancer Epidemiol Biomarkers Prev 2010, 19:492-502. 10.1158/1055-9965.EPI-09-0532, 20086116.
7. Manjer J, Johansson R, Berglund G, Janzon L, Kaaks R, Agren A, Lenner P. Postmenopausal breast cancer risk in relation to sex steroid hormones, prolactin and SHBG (Sweden). Cancer Causes Control 2003, 14:599-607. 10.1023/A:1025671317220, 14575357.
8. Cummings S, Lee J, Lui L-Y, Stone K, Ljung B, Cauleys J. Sex hormones, risk factors, and risk of estrogen receptor-positive breast cancer in older women: a long-term prospective study. Cancer Epidemiol Biomarkers Prev 2005, 14:1047-1051. 10.1158/1055-9965.EPI-04-0375, 15894651.
9. Wysowski DK, Comstock GW, Helsing KJ, Lau HL. Sex hormone levels in serum in relation to the development of breast cancer. Am J Epidemiol 1987, 125:791-799.
10. Thomas H, Key T, Allen D, Moore J, Dowsett M, Fentiman I, Wang D. A prospective study of endogenous serum hormone concentrations and breast cancer risk in premenopausal women on the island of Guernsey. Br J Cancer 1997, 75:1075-1079. 10.1038/bjc.1997.183, 2222732, 9083346.
11. Kabuto M, Akiba S, Stevens R, Neriishi K, Land C. A prospective study of estradiol and breast cancer in Japanese women. Cancer Epidemiol Biomarkers Prev 2000, 9:575-579.
12. Micheli A, Muti P, Secreto G, Krogh V, Meneghini E, Venturelli E, Sieri S, Pala V, Berrino F. Endogenous sex hormones and subsequent breast cancer in premenopausal women. Int J Cancer 2004, 112:312-318. 10.1002/ijc.20403, 15352045.
13. Page J, Colditz G, Rifai N, Barbieri R, Willett W, Hankinson S. Plasma adrenal androgens and risk of breast cancer in premenopausal women. Cancer Epidemiol Biomarkers Prev 2004, 13:1032-1036.
14. Kaaks R, Berrino F, Key T, Rinaldi S, Dossus L, Biessy C, Secreto G, Amiano P, Bingham S, Boeing H, Bueno de Mesquita H, Chang-Claude J, Clavel-Chapelon F, Fournier A, van Gils C, Gonzalez C, Gurrea A, Critselis E, Khaw K, Krogh V, Lahmann P, Nagel G, Olsen A, Onland-Moret N, Overvad K, Palli D, Panico S, Peeters P, QuirÃfÂ3s J, Roddam A, et al. Serum sex steroids in premenopausal women and breast cancer risk within the European Prospective Investigation into Cancer and Nutrition (EPIC). J Natl Cancer Inst 2005, 97:755-765. 10.1093/jnci/dji132, 15900045.
15. Tworoger S, Missmer S, Eliassen AH, Spiegelman D, Folkerd E, Dowsett M, Barbieri R, Hankinson S. The association of plasma DHEA and DHEA sulfate with breast cancer risk in predominantly premenopausal women. Cancer Epidemiol Biomarkers Prev 2006, 15:967-971. 10.1158/1055-9965.EPI-05-0976, 16702378.
16. Eliassen A, Missmer S, Tworoger S, Spiegelman D, Barbieri R, Dowsett M, Hankinson S. Endogenous steroid hormone concentrations and risk of breast cancer among premenopausal women. J Natl Cancer Inst 2006, 98:1406-1415. 10.1093/jnci/djj376, 17018787.
17. Dorgan J, Stanczyk F, Kahle L, Brinton L. Prospective case-control study of premenopausal serum estradiol and testosterone levels and breast cancer risk. Breast Cancer Res 2010, 12:R98. 10.1186/bcr2779, 3046441, 21087481.
18. Gail MH, Brinton LA, Byar DP, Corle DK, Green SB, Schairer C, Mulvihill JJ. Projecting individualized probabilities of developing breast cancer for white females who are being examined annually. J Natl Cancer Inst 1989, 81:1879-1886. 10.1093/jnci/81.24.1879, 2593165.
19. U.S. Preventive Services Task Force Screening for breast cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 2009, 151:716-726. W-236, U.S. Preventive Services Task Force.
20. American Cancer Society Guidelines for the Early Detection of Cancer. , http://www.cancer.org/Healthy/FindCancerEarly/CancerScreeningGuidelines/american-cancer-society-guidelines-for-the-early-detection-of-cancer
21. U.S. Preventive Services Task Force Chemoprevention of breast cancer: recommendations and rationale. Ann Intern Med 2002, 137:56-58. U.S. Preventive Services Task Force.
22. Chlebowski R, Col N, Winer E, Collyar D, Cummings S, Vogel V, Burstein H, Eisen A, Lipkus I, Pfister D. 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, 20:3328-3343. 10.1200/JCO.2002.06.029, 12149307.
23. Armstrong K, Quistberg DA, Micco E, Domchek S, Guerra C, Armstrong K, Quistberg DA, Micco E, Domchek S, Guerra C. Prescription of tamoxifen for breast cancer prevention by primary care physicians. Arch Intern Med 2006, 166:2260-2265. 10.1001/archinte.166.20.2260, 17101945.
24. Waters EA, Cronin KA, Graubard BI, Han PK, Freedman AN, Waters EA, Cronin KA, Graubard BI, Han PK, Freedman AN. Prevalence of tamoxifen use for breast cancer chemoprevention among U.S. women. Cancer Epidemiol Biomarkers Prev 2010, 19:443-446. 10.1158/1055-9965.EPI-09-0930, 3038785, 20142242.
25. Zhou J, Ng S, Adesanya Famuiya O, Anderson K, Bondy CA. Testosterone inhibits estrogen-induced mammary epithelial proliferation and suppresses estrogen receptor expression. FASEB J 2000, 14:1725-1730. 10.1096/fj.99-0863com, 10973921.
26. Dimitrakakis C, Zhou J, Wang J, Belanger A, LaBrie F, Cheng C, Powell D, Bondy C. A physiologic role for testosterone in limiting estrogenic stimulation of the breast. Menopause 2003, 10:292-298. 10.1097/01.GME.0000055522.67459.89, 12851512.
27. Wood C, Lees C, Cline JM. Mammary gland and endometrial effects of testosterone in combination with oral estradiol and progesterone. Menopause 2009, 16:466-476. 10.1097/gme.0b013e318191747a, 2755604, 19265727.
28. Davis S, Moreau M, Kroll R, Bouchard C, Panay N, Gass M, Braunstein G, Hirschberg A, Rodenberg C, Pack S, Koch H, Moufarege A, Studd J. Testosterone for low libido in postmenopausal women not taking estrogen. N Engl J Med 2008, 359:2005-2017. 10.1056/NEJMoa0707302, 18987368.
29. Glaser R, York A, Dimitrakakis C. Beneficial effects of testosterone therapy in women measured by the validated Menopause Rating Scale (MRS). Maturitas 2011, 68:355-361. 10.1016/j.maturitas.2010.12.001, 21177051.
30. Toniolo PG, Pasternack BS, Shore RE, Sonnenschein EG, Koenig KL, Rosenberg C, Strax P, Strax S. Endogenous hormones and breast cancer: a prospective cohort study. Breast Cancer Res Treat 1991, 18:S23-S26. 10.1007/BF02633522, 1873553.
31. Kato I, Toniolo P, Koenig K, Kahn A, Schymura M, Zeleniuch-Jacquotte A. Comparison of active and cancer registry-based follow-up for breast cancer in a prospective cohort study. Am J Epidemiol 1999, 149:372-378.
32. Rinaldi S, Dechaud H, Biessy C, Morin-Raverot V, Toniolo P, Zeleniuch-Jacquotte A, Akhmedkhanov A, Shore RE, Secreto G, Ciampi A, Riboli E, Kaaks R. Reliability and validity of commercially available, direct radioimmunoassays for measurement of blood androgens and estrogens in postmenopausal women. Cancer Epidemiol Biomark Prev 2001, 10:757-765.
33. Rinaldi S, Geay A, Dechaud H, Biessy C, Zeleniuch-Jacquotte A, Akhmedkhanov A, Shore RE, Riboli E, Toniolo P, Kaaks R. Validity of free testosterone and free estradiol determinations in serum samples from postmenopausal women by theoretical calculations. Cancer Epidemiol Biomarkers Prev 2002, 11:1065-1071.
34. Donner A. A review of inference procedures for the intraclass correlation coefficient in the one-way random effects model. Int Stat Rev 1986, 54:67-82.
35. Rothman M, Carlson N, Xu M, Wang C, Swerdloff R, Lee P, Goh VHH, Ridgway EC, Wierman M. Reexamination of testosterone, dihydrotestosterone, estradiol and estrone levels across the menstrual cycle and in postmenopausal women measured by liquid chromatography-tandem mass spectrometry. Steroids 2011, 76:177-182. 10.1016/j.steroids.2010.10.010, 3005029, 21070796.
36. Missmer S, Spiegelman D, Bertone Johnson E, Barbieri R, Pollak M, Hankinson S. Reproducibility of plasma steroid hormones, prolactin, and insulin-like growth factor levels among premenopausal women over a 2- to 3-year period. Cancer Epidemiol Biomarkers Prev 2006, 15:972-978. 10.1158/1055-9965.EPI-05-0848, 16702379.
37. Burger HG, Dudley EC, Cui J, Dennerstein L, Hopper JL. A prospective longitudinal study of serum testosterone, dehydroepiandrosterone sulfate, and sex hormone-binding globulin levels through the menopause transition. J Clin Endocrinol Metab 2000, 85:2832-2838. 10.1210/jc.85.8.2832, 10946891.
38. Santen RJ, Boyd NF, Chlebowski RT, Cummings S, Cuzick J, Dowsett M, Easton D, Forbes JF, Key T, Hankinson SE, Howell A, Ingle J, . Breast Cancer Prevention Collaborative G Critical assessment of new risk factors for breast cancer: considerations for development of an improved risk prediction model. Endocr Relat Cancer 2007, 14:169-187. 10.1677/ERC-06-0045, 17639036, Breast Cancer Prevention Collaborative G.
39. 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, 93:358-366. 10.1093/jnci/93.5.358, 11238697.
40. Rosner B, Colditz GA, Iglehart JD, Hankinson SE. Risk prediction models with incomplete data with application to prediction of estrogen receptor-positive breast cancer: prospective data from the Nurses' Health Study. Breast Cancer Res 2008, 10:R55. 10.1186/bcr2110, 2575548, 18598349.
41. Helzlsouer K, Alberg AJ, Bush TL, Longcope C, Gordon GB, Comstock GW. A prospective study of endogenous hormones and breast cancer. Cancer Detect Prev 1994, 18:79-85.
42. Eliassen AH, Missmer S, Tworoger S, Hankinson S. Endogenous steroid hormone concentrations and risk of breast cancer: does the association vary by a woman's predicted breast cancer risk?. J Clin Oncol 2006, 24:1823-1830. 10.1200/JCO.2005.03.7432, 16567770.
43. Smith R, Cokkinides V, Brooks D, Saslow D, Brawley O. Cancer screening in the United States, 2010: a review of current American Cancer Society guidelines and issues in cancer screening. CA Cancer J Clin 2010, 60:99-119. 10.3322/caac.20063, 20228384.
44. Gail MH, Costantino JP, Bryant J, Croyle R, Freedman L, Helzlsouer K, Vogel V. Weighing the risks and benefits of tamoxifen treatment for preventing breast cancer. J Natl Cancer Inst 1999, 91:1829-1846. 10.1093/jnci/91.21.1829, 10547390.
45. Ozanne E, Wittenberg E, Garber J, Weeks J. Breast cancer prevention: patient decision making and risk communication in the high risk setting. Breast J 2010, 16:38-47. 10.1111/j.1524-4741.2009.00857.x, 19889168.
46. Stanczyk F. Measurement of androgens in women. Semin Reprod Med 2006, 24:78-85. 10.1055/s-2006-939566, 16633981.
47. Blair I. Analysis of estrogens in serum and plasma from postmenopausal women: past present, and future. Steroids 2010, 75:297-306. 10.1016/j.steroids.2010.01.012, 2840185, 20109478.
48. Sieri S, Krogh V, Bolelli G, Abagnato CA, Grioni S, Pala V, Evangelista A, Allemani C, Micheli A, Tagliabue G, Schunemann HJ, Menard S, Berrino F, Muti P, Sieri S, Krogh V, Bolelli G, Abagnato CA, Grioni S, Pala V, Evangelista A, Allemani C, Micheli A, Tagliabue G, Schunemann HJ, Menard S, Berrino F, Muti P. Sex hormone levels, breast cancer risk, and cancer receptor status in postmenopausal women: the ORDET cohort. Cancer Epidemiol Biomarkers Prev 2009, 18:169-176. 10.1158/1055-9965.EPI-08-0808, 19124495.
49. Farhat G, Cummings S, Chlebowski R, Parimi N, Cauley J, Rohan T, Huang A, Vitolins M, Hubbell FA, Manson J, Cochrane B, Lane D, Lee J. Sex hormone levels and risks of estrogen receptor-negative and estrogen receptor-positive breast cancers. J Natl Cancer Inst 2011, 103:562-570. 10.1093/jnci/djr031, 21330633.
50. Key T. Endogenous oestrogens and breast cancer risk in premenopausal and postmenopausal women. Steroids 2011, 76:812-815. 10.1016/j.steroids.2011.02.029, 21477610.
51. The Endogenous Hormones Breast Cancer Collaborative Group Body mass index, serum sex hormones, and breast cancer risk in postmonopausal women. J Natl Cancer Inst 2003, 95:1218-1226. The Endogenous Hormones Breast Cancer Collaborative Group.
52. van den Brandt PA, Spiegelman D, Yaun SS, Adami HO, Beeson L, Folsom AR, Fraser G, Goldbohm RA, Graham S, Kushi L, Marshall JR, Miller AB, Rohan T, Smith-Warner SA, Speizer FE, Willett WC, Wolk A, Hunter DJ. Pooled analysis of prospective cohort studies on height, weight, and breast cancer risk. Am J Epidemiol 2000, 152:514-527. 10.1093/aje/152.6.514, 10997541.
53. Tehard B, Clavel Chapelon F. Several anthropometric measurements and breast cancer risk: results of the E3N cohort study. Int J Obes 2006, 30:156-163.
54. Somboonporn W, Davis S. Testosterone effects on the breast: implications for testosterone therapy for women. Endocr Rev 2004, 25:374-388. 10.1210/er.2003-0016, 15180949.
55. Liao D, Dickson R. Roles of androgens in the development, growth, and carcinogenesis of the mammary gland. J Steroid Biochem Mol Biol 2002, 80:175-189. 10.1016/S0960-0760(01)00185-6, 11897502.
56. Tiefenbacher K, Daxenbichler G. The role of androgens in normal and malignant breast tissue. Breast Care 2008, 3:325-331. 2931104, 20824027.
57. Hofling M, Hirschberg A, Skoog L, Tani E, Hagerstrom T, von Schoultz B. Testosterone inhibits estrogen/progestogen-induced breast cell proliferation in postmenopausal women. Menopause 2007, 14:183-190. 10.1097/01.gme.0000232033.92411.51, 17108847.
58. Campagnoli C, Colombo P, De Aloysio D, Gambacciani M, Grazioli I, Nappi C, Serra G, Genazzani A. Positive effects on cardiovascular and breast metabolic markers of oral estradiol and dydrogesterone in comparison with transdermal estradiol and norethisterone acetate. Maturitas 2002, 41:299-311. 10.1016/S0378-5122(01)00300-0, 12034517.
59. Davis S, Papalia M-A, Norman R, O'Neill S, Redelman M, Williamson M, Stuckey BGA, Wlodarczyk J, Gard'ner K, Humberstone A. Safety and efficacy of a testosterone metered-dose transdermal spray for treating decreased sexual satisfaction in premenopausal women: a randomized trial. Ann Int Med 2008, 148:569-577.
60. Tamimi R, Hankinson S, Chen W, Rosner B, Colditz G. Combined estrogen and testosterone use and risk of breast cancer in postmenopausal women. Arch Int Med 2006, 166:1483-1489.
61. Ness R, Albano J, McTiernan A, Cauley J. Influence of estrogen plus testosterone supplementation on breast cancer. Arch Int Med 2009, 169:41-46.
62. Rosner W, Auchus R, Azziz R, Sluss P, Raff H. Position statement: Utility, limitations, and pitfalls in measuring testosterone: an Endocrine Society position statement. J Clin Endocrinol Metab 2007, 92:405-413.