Abstract
Purpose
Isoflavones have estrogenic properties that may adversely affect pubertal development of boys. We examined if soy isoflavone consumption is associated with age at pubarche (first onset of pubic hair) in a male population with a wide range of soy intake.
Methods
Boys aged 12–18 years (n = 248) who attended schools around Adventist universities in Southern California and Michigan self-reported their age at pubarche. Intake of soy isoflavones was assessed using a validated Web-based food frequency questionnaire; consumption levels were designated as low, moderate, and high. Descriptives, time-to-event analysis, and Cox proportional hazards regression that controlled for confounders were performed.
Results
Energy-adjusted mean intakes were 0.8–54.9 mg/d for total isoflavones, 0.4–22.1 mg/d for daidzein, and 0.4–28.0 mg/d for genistein. Moderate and high total soy isoflavone intake were significantly associated with earlier adjusted median age at pubarche: 12.58 years [RR (95% CI): 1.58 (1.06, 2.36)] for moderate and 12.50 years [RR (95% CI): 1.63 (1.03, 2.60)] for high vs. 13.00 years for low consumers. Similarly, daidzein and genistein consumption was also significantly associated with age at pubarche. No significant associations were found for facial hair for any of the isoflavones.
Conclusions
Age at pubarche in this male population widely exposed to soy is within the reported range for boys’ pubarcheal age; moderate/high consumers tend to have it earlier compared to low consumers. Further studies are needed to ascertain that substantial exposure to soy isoflavones does not adversely affect pubertal development of boys.
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References
Golub MS, Collman GW, Foster PM et al (2008) Public health implications of altered puberty timing. Pediatrics 121(Suppl 3):S218–S230
Day FR, Elks CE, Murray A, Ong KK, Perry JRB (2015) Puberty timing associated with diabetes, cardiovascular disease and also diverse health outcomes in men and women: the UK Biobank Study. Sci Rep 5:1–12
Aksglaede L, Juul A, Olsen LW, Sorensen TI (2009) Age at puberty and the emerging obesity epidemic. PLoS One 4:e8450
Euling SY, Herman-Giddens ME, Lee PA et al (2008) Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics 121(Suppl 3):S172–S191
Herman-Giddens ME (2006) Recent data on pubertal milestones in United States children: the secular trend toward earlier development. Int J Androl 29:241–246 (discussion 286–290)
Sisk CL, Zehr JL (2005) Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol 26:163–174
Graber JA, Seeley JR, Brooks-Gunn J, Lewinsohn PM (2004) Is pubertal timing associated with psychopathology in young adulthood? J Am Acad Child Adolesc Psychiatry 43:718–726
Albanese A, Stanhope R (1995) Investigation of delayed puberty. Clin Endocrinol (Oxf) 43:105–110
Finkelstein JS, Neer RM, Biller BM, Crawford JD, Klibanski A (1992) Osteopenia in men with a history of delayed puberty. New Engl J Med 326:600–604
Euling SY, Selevan SG, Pescovitz OH, Skakkebaek NE (2008) Role of environmental factors in the timing of puberty. Pediatrics 121(Suppl 3):S167–S171
Zawatski W, Lee MM (2013) Male pubertal development: are endocrine-disrupting compounds shifting the norms? J Endocrinol 218:R1–R12
Mouritsen A, Frederiksen H, Sorensen K et al (2013) Urinary phthalates from 168 girls and boys measured twice a year during a 5-year period: associations with adrenal androgen levels and puberty. J Clin Endocr Metab 98:3755–3764
Lam T, Williams PL, Lee MM et al (2014) Prepubertal organochlorine pesticide concentrations and age of pubertal onset among Russian boys. Environ Int 73:135–142
Gunther ALB, Karaolis-Danckert N, Kroke A, Remer T, Buyken AE (2010) Dietary protein intake throughout childhood is associated with the timing of puberty. J Nutr 140:565–571
Messina M (2010) Soybean isoflavone exposure does not have feminizing effects on men: a critical examination of the clinical evidence. Fertil Steril 93:2095–2104
Segovia-Siapco G, Pribis P, Messina M, Oda K, Sabaté J (2014) Is soy intake related to age-at-onset of menarche? A cross-sectional study among adolescents with a wide range of soy food consumption. Nutr J 13:54
Segovia-Siapco G, Oda K, Sabaté J (2016) Evaluation of the relative validity of a web-based food frequency questionnaire used to assess soy isoflavones and nutrient intake in adolescents. BMC Nutr 2:39. doi:10.1186/s40795-016-0080-8
Schakel SF, Sievert YA, Buzzard IM (1988) Sources of data for developing and maintaining a nutrient database. J Am Diet Assoc 88:1268–1271
Jaceldo-Siegl K, Fraser GE, Chan J, Franke A, Sabaté J (2008) Validation of soy protein estimates from a food-frequency questionnaire with repeated 24-h recalls and isoflavonoid excretion in overnight urine in a Western population with a wide range of soy intakes. Am J Clin Nutr 87:1422–1427
Willett W (2013) Nutritional epidemiology, 3rd edn. Oxford University Press, New York
Bai W, Wang C, Ren C (2014) Intakes of total and individual flavonoids by US adults. Int J Food Sci Nutr 65:9–20
Herman-Giddens ME, Wang L, Koch G (2001) Secondary sexual characteristics in boys: estimates from the National Health and Nutrition Examination Survey III, 1988–1994. Arch Pediatr Adolesc Med 155:1022–1028
Karpati AM, Rubin CH, Kieszak SM, Marcus M, Troiano RP (2002) Stature and pubertal stage assessment in American boys: the 1988–1994 Third National Health and Nutrition Examination Survey. J Adolesc Health 30:205–212
Rasmussen AR, Wohlfahrt-Veje C, Tefre de Renzy-Martin K et al (2015) Validity of self-assessment of pubertal maturation. Pediatrics 135:86–93
Ghaly I, Hussein FH, Abdelghaffar S, Anwar G, Seirvogel RM (2008) Optimal age of sexual maturation in Egyptian children. East Mediterr Health J 14:1391–1399
Jaruratanasirikul S, Yuenyongwiwat S, Kreetapirom P, Sriplung H (2014) Age of onset of pubertal maturation of Thai boys. J Pediatr Endocrinol Metab 27:215–220
Juul A, Teilmann G, Scheike T et al (2006) Pubertal development in Danish children: comparison of recent European and US data. Int J Androl 29:247–254
Papadimitriou A, Douros K, Kleanthous K, Papadimitriou DT, Attilakos A, Fretzayas A (2011) Pubertal maturation of contemporary Greek boys: no evidence of a secular trend. J Adolesc Health 49:434–436
Semiz S, Kurt F, Kurt DT, Zencir M, Sevinc O (2008) Pubertal development of Turkish children. J Pediatr Endocrin Metab 21(10):951–961
Ma HM, Chen SK, Chen RM et al (2011) Pubertal development timing in urban Chinese boys. Int J Androl 34:e435–e445
Messina M, Nagata C, Wu AH (2006) Estimated Asian adult soy protein and isoflavone intakes. Nutr Cancer 55(1):1–12
Lindgren G (1996) Pubertal stages 1980 of Stockholm schoolchildren. Acta Paediatr 85:1365–1367
Thorsson AV, Dagbjartsson A, Palsson GI, Arnorsson VH (2000) Puberty in Icelandic boys. Laeknabladid 86:655–659
Marshall WA, Tanner JM (1970) Variations in the pattern of pubertal changes in boys. Arch Dis Child 45:13–23
Tanner JM (1981) Growth and maturation during adolescence. Nutr Rev 39(2):43–55
Cheng G, Remer T, Prinz-Langenohl R, Blaszkewicz M, Degen GH, Buyken AE (2010) Relation of isoflavones and fiber intake in childhood to the timing of puberty. Am J Clin Nutr 92:556–564
Andres A, Moore MB, Linam LE, Casey PH, Cleves MA, Badger TM (2015) Compared with feeding infants breast milk or cow-milk formula, soy formula feeding does not affect subsequent reproductive organ size at 5 years of age. J Nutr 145:871–875
Cederroth CR, Auger J, Zimmermann C, Eustache F, Nef S (2010) Soy, phyto-oestrogens and male reproductive function: a review. Int J Androl 33:304–316
Chavarro JE, Toth TL, Sadio SM, Hauser R (2008) Soy food and isoflavone intake in relation to semen quality parameters among men from an infertility clinic. Hum Reprod 23:2584–2590
D’Adamo CR, Sahin A (2014) Soy foods and supplementation: a review of commonly perceived health benefits and risks. Altern Ther Health Med 20:39–51
Hamilton-Reeves JM, Vazquez G, Duval SJ, Phipps WR, Kurzer MS, Messina MJ (2010) Clinical studies show no effects of soy protein or isoflavones on reproductive hormones in men: results of a meta-analysis. Fertil Steril 94:997–1007
Klein KO (1998) Isoflavones, soy-based infant formulas, and relevance to endocrine function. Nutr Rev 56:193–204
Lim D, Shaw IC (2016) Is there a link between dietary phytoestrogens and reproductive health in men? A meta-analysis of data from the USA and China. Int J Food Sci Tech 51:23–29
Strom BL, Schinnar R, Ziegler EE et al (2001) Exposure to soy-based formula in infancy and endocrinological and reproductive outcomes in young adulthood. J Am Med Assoc 286:807–814
Tanaka M, Fujimoto K, Chihara Y et al (2009) Isoflavone supplements stimulated the production of serum equol and decreased the serum dihydrotestosterone levels in healthy male volunteers. Prostate Cancer Prostatic Dis 12:247–252
Livingstone MBE, Robson PJ, Wallace JMW (2004) Issues in dietary intake assessment of children and adolescents. Br J Nutr 92(Suppl 2):S213–S222
Cutler GJ, Flood A, Hannan P, Neumark-Sztainer D (2009) Major patterns of dietary intake in adolescents and their stability over time. J Nutr 139:323–328
Fraser GE, Lindsted KD, Knutsen SF, Beeson WL, Bennett H, Shavlik DJ (1998) Validity of dietary recall over 20 years among California Seventh-day Adventists. Am J Epidemiol 148:810–818
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Segovia-Siapco, G., Pribis, P., Oda, K. et al. Soy isoflavone consumption and age at pubarche in adolescent males. Eur J Nutr 57, 2287–2294 (2018). https://doi.org/10.1007/s00394-017-1504-1
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DOI: https://doi.org/10.1007/s00394-017-1504-1