Adolescent endogenous sex hormones and breast density in early adulthood

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  Jung, Seungyoun ^a   Egleston, Brian L ^b   Chandler, D Walt ^c   Van Horn, Linda ^d   Hylton, Nola M ^e   Klifa, Catherine C ^f   Lasser, Norman L ^g   LeBlanc, Erin S ^h   Paris, Kenneth ⁱ   Shepherd, John A ^e   Snetselaar, Linda G ^j   Stanczyk, Frank Z ^k   Stevens, Victor J ^h   Dorgan, Joanne F ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c Esoterix Inc   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f Dangeard Group   (United States)

^g RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^h CENTER FOR HEALTH RESEARCH   (United States)

ⁱ LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^j UNIVERSITY OF IOWA   (United States)

^k UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANDROSTENEDIONE; ESTROGEN; PRASTERONE SULFATE; PROGESTERONE; SEX HORMONE; SEX HORMONE BINDING GLOBULIN; TESTOSTERONE;

ADOLESCENT DEVELOPMENT; ADULT; ADULTHOOD; AGE DISTRIBUTION; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST DENSITY; CANCER RISK; FEMALE; FOLLOW UP; HORMONE BLOOD LEVEL; HUMAN; MENARCHE; NUCLEAR MAGNETIC RESONANCE IMAGING; PROSPECTIVE STUDY; SEX HORMONE DETERMINATION; ADOLESCENT; BLOOD; BREAST; BREAST TUMOR; CHILD; CLINICAL TRIAL; CONTROLLED STUDY; METABOLISM; MULTICENTER STUDY; PATHOLOGY; RANDOMIZED CONTROLLED TRIAL; RISK FACTOR;

ADOLESCENT; ADULT; BREAST; BREAST NEOPLASMS; CHILD; DEHYDROEPIANDROSTERONE SULFATE; FEMALE; GONADAL STEROID HORMONES; HUMANS; MAGNETIC RESONANCE IMAGING; RISK FACTORS; SEX HORMONE-BINDING GLOBULIN;

EID: 84931274134     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-015-0581-4     Document Type: Article

References (77)

1. Boyd NF, Martin LJ, Yaffe MJ, Minkin S. Mammographic density and breast cancer risk: current understanding and future prospects. Breast Cancer Res. 2011;13:223.
2. McCormack VA, dos Santos SI. Breast density and parenchymal patterns as markers of breast cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev. 2006;15:1159-69.
3. Vachon CM, Kuni CC, Anderson K, Anderson VE, Sellers TA. Association of mammographically defined percent breast density with epidemiologic risk factors for breast cancer (United States). Cancer Causes Control. 2000;11:653-62.
4. McTiernan A, Martin CF, Peck JD, Aragaki AK, Chlebowski RT, Pisano ED, et al. Estrogen-plus-progestin use and mammographic density in postmenopausal women: Women's Health Initiative randomized trial. J Natl Cancer Inst. 2005;97:1366-76.
5. Greendale GA, Reboussin BA, Slone S, Wasilauskas C, Pike MC, Ursin G. Postmenopausal hormone therapy and change in mammographic density. J Natl Cancer Inst. 2003;95:30-7.
6. Chen JH, Chen WP, Chan S, Yeh DC, Su MY, McLaren CE. Correlation of endogenous hormonal levels, fibroglandular tissue volume and percent density measured using 3D MRI during one menstrual cycle. Ann Oncol. 2013;24:2329-35.
7. Meyer F, Brisson J, Morrison AS, Brown JB. Endogenous sex hormones, prolactin, and mammographic features of breast tissue in premenopausal women. J Natl Cancer Inst. 1986;77:617-20.
8. Boyd NF, Stone J, Martin LJ, Jong R, Fishell E, Yaffe M, et al. The association of breast mitogens with mammographic densities. Br J Cancer. 2002;87:876-82.
9. Noh JJ, Maskarinec G, Pagano I, Cheung LW, Stanczyk FZ. Mammographic densities and circulating hormones: a cross-sectional study in premenopausal women. Breast (Edinburgh, Scotland). 2006;15:20-8.
10. Yong M, Atkinson C, Newton KM, Aiello Bowles EJ, Stanczyk FZ, Westerlind KC, et al. Associations between endogenous sex hormone levels and mammographic and bone densities in premenopausal women. Cancer Causes Control. 2009;20:1039-53.
11. Borugian MJ, Spinelli JJ, Gordon PB, Abanto Z, Brooks-Wilson A, Pollak MN, et al. Fasting insulin and endogenous hormones in relation to premenopausal breast density (Canada). Cancer Causes Control. 2014;25:385-94.
12. Walker K, Fletcher O, Johnson N, Coupland B, McCormack VA, Folkerd E, et al. Premenopausal mammographic density in relation to cyclic variations in endogenous sex hormone levels, prolactin, and insulin-like growth factors. Cancer Res. 2009;69:6490-9.
13. Bremnes Y, Ursin G, Bjurstam N, Rinaldi S, Kaaks R, Gram IT. Endogenous sex hormones, prolactin and mammographic density in postmenopausal Norwegian women. Int J Cancer. 2007;121:2506-11.
14. Verheus M, Peeters PH, van Noord PA, van der Schouw YT, Grobbee DE, van Gils CH. No relationship between circulating levels of sex steroids and mammographic breast density: the Prospect-EPIC cohort. Breast Cancer Res. 2007;9:R53.
15. Johansson H, Gandini S, Bonanni B, Mariette F, Guerrieri-Gonzaga A, Serrano D, et al. Relationships between circulating hormone levels, mammographic percent density and breast cancer risk factors in postmenopausal women. Breast Cancer Res Treat. 2008;108:57-67.
16. McCormack VA, Dowsett M, Folkerd E, Johnson N, Palles C, Coupland B, et al. Sex steroids, growth factors and mammographic density: a cross-sectional study of UK postmenopausal Caucasian and Afro-Caribbean women. Breast Cancer Res. 2009;11:R38.
17. Sprague BL, Trentham-Dietz A, Gangnon RE, Buist DS, Burnside ES, Bowles EJ, et al. Circulating sex hormones and mammographic breast density among postmenopausal women. Horm Cancer. 2011;2:62-72.
18. Woolcott CG, Courneya KS, Boyd NF, Yaffe MJ, McTiernan A, Brant R, et al. Association between sex hormones, glucose homeostasis, adipokines, and inflammatory markers and mammographic density among postmenopausal women. Breast Cancer Res Treat. 2013;139:255-65.
19. Aiello EJ, Tworoger SS, Yasui Y, Stanczyk FZ, Potter J, Ulrich CM, et al. Associations among circulating sex hormones, insulin-like growth factor, lipids, and mammographic density in postmenopausal women. Cancer Epidemiol Biomarkers Prev. 2005;14:1411-7.
20. Greendale GA, Palla SL, Ursin G, Laughlin GA, Crandall C, Pike MC, et al. The association of endogenous sex steroids and sex steroid binding proteins with mammographic density: results from the Postmenopausal Estrogen/Progestin Interventions Mammographic Density Study. Am J Epidemiol. 2005;162:826-34.
21. Tamimi RM, Hankinson SE, Colditz GA, Byrne C. Endogenous sex hormone levels and mammographic density among postmenopausal women. Cancer Epidemiol Biomarkers Prev. 2005;14:2641-7.
22. Schoemaker MJ, Folkerd EJ, Jones ME, Rae M, Allen S, Ashworth A, et al. Combined effects of endogenous sex hormone levels and mammographic density on postmenopausal breast cancer risk: results from the Breakthrough Generations Study. Br J Cancer. 2014;110:1898-907.
23. Warren R, Skinner J, Sala E, Denton E, Dowsett M, Folkerd E, et al. Associations among mammographic density, circulating sex hormones, and polymorphisms in sex hormone metabolism genes in postmenopausal women. Cancer Epidemiol Biomarkers Prev. 2006;15:1502-8.
24. Biro FM, Greenspan LC, Galvez MP, Pinney SM, Teitelbaum S, Windham GC, et al. Onset of breast development in a longitudinal cohort. Pediatrics. 2013;132:1019-27.
25. Russo J, Russo IH. Breast development, hormones and cancer. Adv Exp Med Biol. 2008;630:52-6.
26. Colditz GA, Frazier AL. Models of breast cancer show that risk is set by events of early life: prevention efforts must shift focus. Cancer Epidemiol Biomarkers Prev. 1995;4:567-71.
27. Dewi FN, Wood CE, Lees CJ, Willson CJ, Register TC, Tooze JA, et al. Dietary soy effects on mammary gland development during the pubertal transition in nonhuman primates. Cancer Prev Res (Phila). 2013;6:832-42.
28. Dearth RK, Hiney JK, Srivastava VK, Hamilton AM, Dees WL. Prepubertal exposure to elevated manganese results in estradiol regulated mammary gland ductal differentiation and hyperplasia in female rats. Exp Biol Med. 2014;239:871-82.
29. Dorgan JF, Klifa C, Deshmukh S, Egleston BL, Shepherd JA, Kwiterovich Jr PO, et al. Menstrual and reproductive characteristics and breast density in young women. Cancer Causes Control. 2013;24:1973-83.
30. Collaborative Group on Hormonal Factors in Breast Cancer. Menarche, menopause, and breast cancer risk: individual participant meta-analysis, including 118 964 women with breast cancer from 117 epidemiological studies. Lancet Oncol. 2012;13:1141-51.
31. Dorgan JF, Liu L, Klifa C, Hylton N, Shepherd JA, Stanczyk FZ, et al. Adolescent diet and subsequent serum hormones, breast density, and bone mineral density in young women: results of the Dietary Intervention Study in Children. Cancer Epidemiol Biomarkers Prev. 2010;19:1545-56.
32. Dorgan JF, Hunsberger SA, McMahon RP, Kwiterovich Jr PO, Lauer RM, Van Horn L, et al. Diet and sex hormones in girls: findings from a randomized controlled clinical trial. J Natl Cancer Inst. 2003;95:132-41.
33. Writing Group for the DISC Collaborative Research Group. Efficacy and safety of lowering dietary intake of fat and cholesterol in children with elevated low-density lipoprotein cholesterol. The Dietary Intervention Study in Children (DISC). JAMA. 1995;273:1429-35.
34. DISC Collaborative Research Group. Dietary intervention study in children (DISC) with elevated low-density-lipoprotein cholesterol. Design and baseline characteristics. Ann Epidemiol. 1993;3:393-402.
35. Dorgan JF, McMahon RP, Friedman LA, Van Horn L, Snetselaar LG, Kwiterovich Jr PO, et al. Diet and sex hormones in boys: findings from the dietary intervention study in children. J Clin Endocrinol Metab. 2006;91:3992-6.
36. Obarzanek E, Kimm SY, Barton BA, Van Horn LL, Kwiterovich Jr PO, Simons-Morton DG, et al. Long-term safety and efficacy of a cholesterol-lowering diet in children with elevated low-density lipoprotein cholesterol: seven-year results of the Dietary Intervention Study in Children (DISC). Pediatrics. 2001;107:256-64.
37. Dorgan JF, Klifa C, Shepherd JA, Egleston BL, Kwiterovich Jr PO, Himes JH, et al. Height, adiposity and body fat distribution and breast density in young women. Breast Cancer Res. 2012;14:R107.
38. Tanner JM. Growth at adolescence. 2nd ed. Oxford (UK): Blackwell Scientific, 1962.
39. Dorgan JF, Fears TR, McMahon RP, Aronson Friedman L, Patterson BH, Greenhut SF. Measurement of steroid sex hormones in serum: a comparison of radioimmunoassay and mass spectrometry. Steroids. 2002;67:151-8.
40. Dorgan JF, Baer DJ, Albert PS, Judd JT, Brown ED, Corle DK, et al. Serum hormones and the alcohol-breast cancer association in postmenopausal women. J Natl Cancer Inst. 2001;93:710-5.
41. Nankin HR, Pinto R, Fan DF, Troen P. Daytime titers of testosterone, LH, estrone, estradiol, and testosterone-binding protein: acute effects of LH and LH-releasing hormone in men. J Clin Endocrinol Metab. 1975;41:271-81.
42. Klifa C, Carballido-Gamio J, Wilmes L, Laprie A, Lobo C, Demicco E, et al. Quantification of breast tissue index from MR data using fuzzy clustering. Conference Proc IEEE Eng Med Biol Soc. 2004;3:1667-70.
43. Pettersson A, Graff RE, Ursin G, Santos Silva ID, McCormack V, Baglietto L, et al. Mammographic density phenotypes and risk of breast cancer: a meta-analysis. J Natl Cancer Inst. 2014;106:5.
44. Sizonenko PC. Endocrinology in preadolescents and adolescents. I. Hormonal changes during normal puberty. Am J Dis Child. 1978;132:704-12.
45. Root AW. Endocrinology of puberty. I. Normal sexual maturation. J Pediatr. 1973;83:1-19.
46. Littell RC. SAS for mixed models. 2nd ed. Cary, NC: SAS Institute; 2006.
47. Adami H-O, Hunter DJ, Trichopoulos D. Textbook of Cancer Epidemiology, vol. 36, 2nd edn. Oxford, New York: Oxford University Press; 2008.
48. Fenton SE, Reed C, Newbold RR. Perinatal environmental exposures affect mammary development, function, and cancer risk in adulthood. Annu Rev Pharmacol Toxicol. 2012;52:455-79.
49. Hilakivi-Clarke L, de Assis S, Warri A. Exposures to synthetic estrogens at different times during the life, and their effect on breast cancer risk. J Mammary Gland Biol Neoplasia. 2013;18:25-42.
50. Jernstrom H, Loman N, Johannsson OT, Borg A, Olsson H. Impact of teenage oral contraceptive use in a population-based series of early-onset breast cancer cases who have undergone BRCA mutation testing. Eur J Cancer. 2005;41:2312-20.
51. Anderson TJ, Battersby S, King RJ, McPherson K, Going JJ. Oral contraceptive use influences resting breast proliferation. Hum Pathol. 1989;20:1139-44.
52. Ebeling P, Koivisto VA. Physiological importance of dehydroepiandrosterone. Lancet. 1994;343:1479-81.
53. Bay K, Andersson AM, Skakkebaek NE. Estradiol levels in prepubertal boys and girls-analytical challenges. Int J Androl. 2004;27:266-73.
54. Biro FM, Pinney SM, Huang B, Baker ER, Walt Chandler D, Dorn LD. Hormone changes in peripubertal girls. J Clin Endocrinol Metab. 2014;99:3829-35.
55. Aksglaede L, Sorensen K, Petersen JH, Skakkebaek NE, Juul A. Recent decline in age at breast development: the Copenhagen Puberty Study. Pediatrics. 2009;123:e932-9.
56. Ahmed ML, Ong KK, Dunger DB. Childhood obesity and the timing of puberty. Trends Endocrinol Metab. 2009;20:237-42.
57. Guercio G, Rivarola MA, Chaler E, Maceiras M, Belgorosky A. Relationship between the growth hormone/insulin-like growth factor-I axis, insulin sensitivity, and adrenal androgens in normal prepubertal and pubertal girls. J Clin Endocrinol Metab. 2003;88:1389-93.
58. Ibanez L, Valls C, Ong K, Dunger DB, de Zegher F. Metformin therapy during puberty delays menarche, prolongs pubertal growth, and augments adult height: a randomized study in low-birth-weight girls with early-normal onset of puberty. J Clin Endocrinol Metab. 2006;91:2068-73.
59. Kleinberg DL, Ruan W. IGF-I, GH, and sex steroid effects in normal mammary gland development. J Mammary Gland Biol Neoplasia. 2008;13:353-60.
60. Sternlicht MD. Key stages in mammary gland development: the cues that regulate ductal branching morphogenesis. Breast Cancer Res. 2006;8:201.
61. Greendale GA, Reboussin BA, Sie A, Singh HR, Olson LK, Gatewood O, et al. Effects of estrogen and estrogen-progestin on mammographic parenchymal density. Postmenopausal Estrogen/Progestin Interventions (PEPI) Investigators. Ann Intern Med. 1999;130:262-9.
62. Rosner W, Hryb DJ, Kahn SM, Nakhla AM, Romas NA. Interactions of sex hormone-binding globulin with target cells. Mol Cell Endocrinol. 2010;316:79-85.
63. Andersen ZJ, Baker JL, Bihrmann K, Vejborg I, Sorensen TI, Lynge E. Birth weight, childhood body mass index, and height in relation to mammographic density and breast cancer: a register-based cohort study. Breast Cancer Res. 2014;16:R4.
64. Cabrera SM, Bright GM, Frane JW, Blethen SL, Lee PA. Age of thelarche and menarche in contemporary US females: a cross-sectional analysis. J Pediatr Endocrinol Metab. 2014;27:47-51.
65. Tanner JM. Issues and advances in adolescent growth and development. J Adolesc Health Care. 1987;8:470-8.
66. Bodicoat DH, Schoemaker MJ, Jones ME, McFadden E, Griffin J, Ashworth A, et al. Timing of pubertal stages and breast cancer risk: the Breakthrough Generations Study. Breast Cancer Res. 2014;16:R18.
67. Boyd N, Martin L, Chavez S, Gunasekara A, Salleh A, Melnichouk O, et al. Breast-tissue composition and other risk factors for breast cancer in young women: a cross-sectional study. Lancet Oncol. 2009;10:569-80.
68. Tamimi RM, Byrne C, Colditz GA, Hankinson SE. Endogenous hormone levels, mammographic density, and subsequent risk of breast cancer in postmenopausal women. J Natl Cancer Inst. 2007;99:1178-87.
69. Vihko R, Apter D. Endocrine characteristics of adolescent menstrual cycles: impact of early menarche. J Steroid Biochem. 1984;20:231-6.
70. Rosner W, Auchus RJ, Azziz R, Sluss PM, Raff H. Position statement: Utility, limitations, and pitfalls in measuring testosterone: an Endocrine Society position statement. J Clin Endocrinol Metab. 2007;92:405-13.
71. Kerlikowske K, Grady D, Barclay J, Sickles EA, Ernster V. Effect of age, breast density, and family history on the sensitivity of first screening mammography. JAMA. 1996;276:33-8.
72. Wei J, Chan HP, Helvie MA, Roubidoux MA, Sahiner B, Hadjiiski LM, et al. Correlation between mammographic density and volumetric fibroglandular tissue estimated on breast MR images. Med Phys. 2004;31:933-42.
73. Thompson DJ, Leach MO, Kwan-Lim G, Gayther SA, Ramus SJ, Warsi I, et al. Assessing the usefulness of a novel MRI-based breast density estimation algorithm in a cohort of women at high genetic risk of breast cancer: the UK MARIBS study. Breast Cancer Res. 2009;11:R80.
74. Shepherd JA, Kerlikowske K, Ma L, Duewer F, Fan B, Wang J, et al. Volume of mammographic density and risk of breast cancer. Cancer Epidemiol Biomarkers Prev. 2011;20:1473-82.
75. Milanese TR, Hartmann LC, Sellers TA, Frost MH, Vierkant RA, Maloney SD, et al. Age-related lobular involution and risk of breast cancer. J Natl Cancer Inst. 2006;98:1600-7.
76. Key T, Appleby P, Barnes I, Reeves G. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J Natl Cancer Inst. 2002;94:606-16.
77. Key TJ, Appleby PN, Reeves GK, Travis RC, Alberg AJ, Barricarte A, et al. Sex hormones and risk of breast cancer in premenopausal women: a collaborative reanalysis of individual participant data from seven prospective studies. Lancet Oncol. 2013;14:1009-19.