Body fatness during childhood and adolescence and breast density in young women: a prospective analysis

Kimberly A Bertrand, Heather J Baer, E John Orav, Catherine Klifa, John A Shepherd, Linda Van Horn, Linda Snetselaar, Victor J Stevens, Nola M Hylton, Joanne F Dorgan, Kimberly A Bertrand, Heather J Baer, E John Orav, Catherine Klifa, John A Shepherd, Linda Van Horn, Linda Snetselaar, Victor J Stevens, Nola M Hylton, Joanne F Dorgan

Abstract

Introduction: Overweight and obesity in childhood and adolescence are associated with reduced breast cancer risk, independent of adult body mass index (BMI). These associations may be mediated through breast density.

Methods: We prospectively examined associations of early life body fatness with adult breast density measured by MRI in 182 women in the Dietary Intervention Study in Children (DISC) who were ages 25-29 at follow-up. Height, weight, and other factors were measured at baseline (ages 8-10) and annual clinic visits through adolescence. We used linear mixed-effects models to quantify associations of percent breast density and dense and non-dense breast volume at ages 25-29 with quartiles of age-specific youth body mass index (BMI) Z-scores, adjusting for clinic, treatment group, current adult BMI, and other well-established risk factors for breast cancer and predictors of breast density.

Results: We observed inverse associations between age-specific BMI Z-scores at all youth clinic visits and percent breast density, adjusting for current adult BMI and other covariates (all p values <0.01). Women whose baseline BMI Z-scores (at ages 8-10 years) were in the top quartile had significantly lower adult breast density, after adjusting for current adult BMI and other covariates [least squares mean (LSM): 23.4 %; 95 % confidence interval (CI): 18.0 %, 28.8 %] compared to those in the bottom quartile (LSM: 31.8 %; 95 % CI: 25.2 %, 38.4 %) (p trend <0.01). Significant inverse associations were also observed for absolute dense breast volume (all p values <0.01), whereas there were no clear associations with non-dense breast volume.

Conclusions: These results support the hypothesis that body fatness during childhood and adolescence may play an important role in premenopausal breast density, independent of current BMI, and further suggest direct or indirect influences on absolute dense breast volume.

Clinical trials registration number: NCT00458588 ; April 9, 2007.

Figures

Fig. 1
Fig. 1
Difference in percent dense volume at the DISC06 follow-up visit per unit increase in body mass index (BMI) Z-score, by youth clinic visits
Fig. 2
Fig. 2
a Mean percent breast density by body fatness in adolescence and at follow-up. b Mean absolute dense breast volume by body fatness in adolescence and at follow-up

References

    1. Ahlgren M, Melbye M, Wohlfahrt J, Sorensen TI. Growth patterns and the risk of breast cancer in women. N Engl J Med. 2004;351:1619–26. doi: 10.1056/NEJMoa040576.
    1. Bardia A, Vachon CM, Olson JE, Vierkant RA, Wang AH, Hartmann LC, et al. Relative weight at age 12 and risk of postmenopausal breast cancer. Cancer Epidemiol Biomarkers Prev. 2008;17:374–8. doi: 10.1158/1055-9965.EPI-07-0389.
    1. Baer HJ, Tworoger SS, Hankinson SE, Willett WC. Body fatness at young ages and risk of breast cancer throughout life. Am J Epidemiol. 2010;171:1183–94. doi: 10.1093/aje/kwq045.
    1. 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. doi: 10.1158/1055-9965.EPI-06-0034.
    1. Yaffe MJ. Mammographic density. Measurement of mammographic density. Breast Cancer Res. 2008;10:209. doi: 10.1186/bcr2102.
    1. Samimi G, Colditz GA, Baer HJ, Tamimi RM. Measures of energy balance and mammographic density in the Nurses’ Health Study. Breast Cancer Res Treat. 2008;109:113–22. doi: 10.1007/s10549-007-9631-7.
    1. Sellers TA, Vachon CM, Pankratz VS, Janney CA, Fredericksen Z, Brandt KR, et al. Association of childhood and adolescent anthropometric factors, physical activity, and diet with adult mammographic breast density. Am J Epidemiol. 2007;166:456–64. doi: 10.1093/aje/kwm112.
    1. Harris HR, Tamimi RM, Willett WC, Hankinson SE, Michels KB. Body size across the life course, mammographic density, and risk of breast cancer. Am J Epidemiol. 2011;174:909–18. doi: 10.1093/aje/kwr225.
    1. McCormack VA, dos Santos SI, De Stavola BL, Perry N, Vinnicombe S, Swerdlow AJ, et al. Life-course body size and perimenopausal mammographic parenchymal patterns in the MRC 1946 British birth cohort. Br J Cancer. 2003;89:852–9. doi: 10.1038/sj.bjc.6601207.
    1. Jeffreys M, Warren R, Gunnell D, McCarron P, Smith GD. Life course breast cancer risk factors and adult breast density (United Kingdom) Cancer Causes Control. 2004;15:947–55. doi: 10.1007/s10552-004-2473-2.
    1. Lope V, Perez-Gomez B, Moreno MP, Vidal C, Salas-Trejo D, Ascunce N, et al. Childhood factors associated with mammographic density in adult women. Breast Cancer Res Treat. 2011;130:965–74. doi: 10.1007/s10549-011-1664-2.
    1. Novotny R, Daida Y, Morimoto Y, Shepherd J, Maskarinec G. Puberty, body fat, and breast density in girls of several ethnic groups. Am J Hum Biol. 2011;23:359–65. doi: 10.1002/ajhb.21145.
    1. Lokate M, Peeters PH, Peelen LM, Haars G, Veldhuis WB, van Gils CH. Mammographic density and breast cancer risk: the role of the fat surrounding the fibroglandular tissue. Breast Cancer Res. 2011;13:R103. doi: 10.1186/bcr3044.
    1. Pettersson A, Hankinson SE, Willett WC, Lagiou P, Trichopoulos D, Tamimi RM. Nondense mammographic area and risk of breast cancer. Breast Cancer Res. 2011;13:R100. doi: 10.1186/bcr3041.
    1. 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: doi:10.1093/jnci/dju078
    1. Dietary intervention study in children (DISC) with elevated low-density-lipoprotein cholesterol. Design and baseline characteristics. DISC Collaborative Research Group. Ann Epidemiol. 1993;3:393–402.
    1. 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). The Writing Group for the DISC Collaborative Research Group. JAMA. 1995;273:1429–35.
    1. Obarzanek E, Hunsberger SA, Van Horn L, Hartmuller VV, Barton BA, Stevens VJ, et al. Safety of a fat-reduced diet: the dietary intervention study in children (DISC) Pediatrics. 1997;100:51–9. doi: 10.1542/peds.100.1.51.
    1. Obarzanek E, Kimm SY, Barton BA, Van Horn LL, Kwiterovich PO, Jr, 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. doi: 10.1542/peds.107.2.256.
    1. Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Wei R, et al. CDC growth charts: United States. Adv Data. 2000;314:1–27.
    1. 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 follow-up study. Cancer Epidemiol Biomarkers Prev. 2010;19:1545–56. doi: 10.1158/1055-9965.EPI-09-1259.
    1. Pettee Gabriel K, Klifa C, Perez A, Kriska AM, High RR, Snetselaar L, et al. Adolescent and young adult exposure to physical activity and breast density. Med Sci Sports Exerc. 2013;45:1515–23. doi: 10.1249/MSS.0b013e318289a7f8.
    1. ACR practice guideline for the performance of contrast-enhanced magnetic resonance imaging (MRI) of the breast [Amended 2014 (Resolution 39)]
    1. Klifa C, Carballido-Gamio J, Wilmes L, Laprie A, Lobo C, DeMicco E, et al. Quantitation of breast tissue index from MR data using fuzzy clustering. Conf Proc IEEE Eng Med Biol Soc. 2004;3:1667–70.
    1. Dorgan JF, Klifa C, Shepherd JA, Egleston BL, Kwiterovich PO, Jr, Himes JH, et al. Height, adiposity and body fat distribution and breast density in young women. Breast Cancer Res. 2012;14:R107. doi: 10.1186/bcr3228.
    1. Dorgan JF, Klifa C, Deshmukh S, Egleston BL, Shepherd JA, Kwiterovich PO, Jr, et al. Menstrual and reproductive characteristics and breast density in young women. Cancer Causes Control. 2013;24:1973–83. doi: 10.1007/s10552-013-0273-2.
    1. Duan N. Smearing estimate: a nonparametric retransformation approach. JASA. 1983;79:605–10. doi: 10.1080/01621459.1983.10478017.
    1. Marquaridt DW. Generalized inverses, ridge regression, biased linear estimation, and nonlinear estimation. Technometrics. 1970;12:591–612. doi: 10.1080/00401706.1970.10488699.
    1. Belsley DA, Kuh E, Welsch RE. Regression diagnostics: identifying influential data and sources of collinearity. New York: Wiley; 1980.
    1. Neter J, Wasserman W, Kutner MH. Applied linear regression models. Homewood, IL: Irwin; 1989.
    1. Kennedy P. A guide to econometrics. Oxford: Blackwell; 1992.
    1. Hair JFJ, Anderson RE, Tatham RL, Black WC. Multivariate data analysis. 3. New York: Macmillan; 1995.
    1. Caire-Juvera G, Arendell LA, Maskarinec G, Thomson CA, Chen Z. Associations between mammographic density and body composition in Hispanic and non-Hispanic white women by menopause status. Menopause. 2008;15:319–25. doi: 10.1097/gme.0b013e3181405b8a.
    1. Rice MS, Bertrand KA, Lajous M, Tamimi RM, Torres-Mejia G, Biessy C, et al. Body size throughout the life course and mammographic density in Mexican women. Breast Cancer Res Treat. 2013;138:601–10. doi: 10.1007/s10549-013-2463-8.
    1. 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.
    1. Russo J, Gusterson BA, Rogers AE, Russo IH, Wellings SR, van Zwieten MJ. Comparative study of human and rat mammary tumorigenesis. Lab Invest. 1990;62:244–78.
    1. Russo J, Tay LK, Russo IH. Differentiation of the mammary gland and susceptibility to carcinogenesis. Breast Cancer Res Treat. 1982;2:5–73. doi: 10.1007/BF01805718.
    1. Andersen ZJ, Baker JL, Bihrmann K, Vejborg I, Sorensen T, 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. doi: 10.1186/bcr3596.
    1. 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. doi: 10.1158/1055-9965.EPI-10-1150.
    1. Baer HJ, Colditz GA, Willett WC, Dorgan JF. Adiposity and sex hormones in girls. Cancer Epidemiol Biomarkers Prev. 2007;16:1880–8. doi: 10.1158/1055-9965.EPI-07-0313.
    1. Rich-Edwards JW, Goldman MB, Willett WC, Hunter DJ, Stampfer MJ, Colditz GA, et al. Adolescent body mass index and infertility caused by ovulatory disorder. Am J Obstet Gynecol. 1994;171:171–7. doi: 10.1016/0002-9378(94)90465-0.
    1. Cabanes A, Wang M, Olivo S, DeAssis S, Gustafsson JA, Khan G, et al. Prepubertal estradiol and genistein exposures up-regulate BRCA1 mRNA and reduce mammary tumorigenesis. Carcinogenesis. 2004;25:741–8. doi: 10.1093/carcin/bgh065.
    1. Nagasawa H, Yanai R, Shodono M, Nakamura T, Tanabe Y. Effect of neonatally administered estrogen or prolactin on normal and neoplastic mammary growth and serum estradiol-17 beta level in rats. Cancer Res. 1974;34:2643–6.
    1. Apter D, Vihko R. Endocrine determinants of fertility: serum androgen concentrations during follow-up of adolescents into the third decade of life. J Clin Endocrinol Metab. 1990;71:970–4. doi: 10.1210/jcem-71-4-970.
    1. Caprio S, Hyman LD, Limb C, McCarthy S, Lange R, Sherwin RS, et al. Central adiposity and its metabolic correlates in obese adolescent girls. Am J Physiol. 1995;269:E118–126.
    1. Ong K, Kratzsch J, Kiess W, Dunger D. Circulating IGF-I levels in childhood are related to both current body composition and early postnatal growth rate. J Clin Endocrinol Metab. 2002;87:1041–4. doi: 10.1210/jcem.87.3.8342.
    1. Velie EM, Zhang Z, Kerver JM, Gardiner JC, Rosen CJ, Dorgan JF. Abstract B78: Adiposity and the IGF-axis in girls during pubertal development. Canc Prev Res. 2012;5:B78. doi: 10.1158/1940-6207.PREV-12-B78.
    1. Poole EM, Tworoger SS, Hankinson SE, Schernhammer ES, Pollak MN, Baer HJ. Body size in early life and adult levels of insulin-like growth factor 1 and insulin-like growth factor binding protein 3. Am J Epidemiol. 2011;174:642–51. doi: 10.1093/aje/kwr123.
    1. Rice MS, Tworoger SS, Rosner BA, Pollak MN, Hankinson SE, Tamimi RM. Insulin-like growth factor-1, insulin-like growth factor-binding protein-3, growth hormone, and mammographic density in the Nurses’ Health Studies. Breast Cancer Res Treat. 2012;136:805–12. doi: 10.1007/s10549-012-2303-2.
    1. Byrne C, Colditz GA, Willett WC, Speizer FE, Pollak M, Hankinson SE. Plasma insulin-like growth factor (IGF) I, IGF-binding protein 3, and mammographic density. Cancer Res. 2000;60:3744–8.
    1. 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. doi: 10.1158/1055-9965.EPI-04-0920.
    1. Diorio C, Berube S, Byrne C, Masse B, Hebert-Croteau N, Yaffe M, et al. Influence of insulin-like growth factors on the strength of the relation of vitamin D and calcium intakes to mammographic breast density. Cancer Res. 2006;66:588–97. doi: 10.1158/0008-5472.CAN-05-1959.
    1. dos Santos SI, Johnson N, De Stavola B, Torres-Mejia G, Fletcher O, Allen DS, et al. The insulin-like growth factor system and mammographic features in premenopausal and postmenopausal women. Cancer Epidemiol Biomarkers Prev. 2006;15:449–55. doi: 10.1158/1055-9965.EPI-05-0555.
    1. Bremnes Y, Ursin G, Bjurstam N, Rinaldi S, Kaaks R, Gram IT. Insulin-like growth factor and mammographic density in postmenopausal Norwegian women. Cancer Epidemiol Biomarkers Prev. 2007;16:57–62. doi: 10.1158/1055-9965.EPI-06-0788.
    1. Maskarinec G, Takata Y, Chen Z, Gram IT, Nagata C, Pagano I, et al. IGF-I and mammographic density in four geographic locations: a pooled analysis. Int J Cancer. 2007;121:1786–92. doi: 10.1002/ijc.22834.
    1. Berkey CS, Gardner JD, Frazier AL, Colditz GA. Relation of childhood diet and body size to menarche and adolescent growth in girls. Am J Epidemiol. 2000;152:446–52. doi: 10.1093/aje/152.5.446.
    1. Berkey CS, Frazier AL, Gardner JD, Colditz GA. Adolescence and breast carcinoma risk. Cancer. 1999;85:2400–9. doi: 10.1002/(SICI)1097-0142(19990601)85:11<2400::AID-CNCR15>;2-O.
    1. Olson LK, Tan Y, Zhao Y, Aupperlee MD, Haslam SZ. Pubertal exposure to high fat diet causes mouse strain-dependent alterations in mammary gland development and estrogen responsiveness. Int J Obes. 2010;34:1415–26. doi: 10.1038/ijo.2010.51.

Source: PubMed

3
Se inscrever