1932

Abstract

The timing of puberty has important public health, clinical, and social implications. The plasticity of sexual development onset could be a mechanism that adapts to prevailing environmental conditions. Early-life nutrition may provide cues for the environment's suitability for reproduction. This review focuses on recent developments in our understanding of the role of diet in the timing of sexual maturation. Population-based observational studies consistently indicate that childhood obesity is related to the earlier onset of puberty in girls. Similarly, intake of animal foods has been associated with earlier sexual development, whereas vegetable protein intake is related to delayed maturation. Evidence for prenatal nutrition, infant feeding practices, and childhood intake of fat, carbohydrate, and micronutrients is inconsistent. Secondary analyses of prenatal and early-life randomized nutritional interventions with extended follow-up through peripubertal years would help clarify the role of nutrition in the timing of sexual maturation.

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2016-03-18
2024-06-12
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Literature Cited

  1. Adair LS. 1.  2001. Size at birth predicts age at menarche. Pediatrics 107:E59 [Google Scholar]
  2. Adgent MA, Daniels JL, Rogan WJ, Adair L, Edwards LJ. 2.  et al. 2012. Early-life soy exposure and age at menarche. Paediatr. Perinat. Epidemiol. 26:163–75 [Google Scholar]
  3. Al-Sahab B, Adair L, Hamadeh MJ, Ardern CI, Tamim H. 3.  2011. Impact of breastfeeding duration on age at menarche. Am. J. Epidemiol. 173:971–77 [Google Scholar]
  4. Andres A, Moore MB, Linam LE, Casey PH, Cleves MA, Badger TM. 4.  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. 145:871–75 [Google Scholar]
  5. Atay Z, Turan S, Guran T, Furman A, Bereket A. 5.  2011. Puberty and influencing factors in schoolgirls living in Istanbul: end of the secular trend?. Pediatrics 128:e40–45 [Google Scholar]
  6. Bartha JL, Marin-Segura P, Gonzalez-Gonzalez NL, Wagner F, Aguilar-Diosdado M, Hervias-Vivancos B. 6.  2007. Ultrasound evaluation of visceral fat and metabolic risk factors during early pregnancy. Obesity 15:2233–39 [Google Scholar]
  7. Berkey CS, Gardner JD, Frazier AL, Colditz GA. 7.  2000. Relation of childhood diet and body size to menarche and adolescent growth in girls. Am. J. Epidemiol. 152:446–52 [Google Scholar]
  8. Blell M, Pollard TM, Pearce MS. 8.  2008. Predictors of age at menarche in the Newcastle Thousand Families Study. J. Biosoc. Sci. 40:563–75 [Google Scholar]
  9. Bordini B, Rosenfield RL. 9.  2011. Normal pubertal development: Part I: The endocrine basis of puberty. Pediatr. Rev. 32:223–29 [Google Scholar]
  10. Boynton-Jarrett R, Rich-Edwards J, Fredman L, Hibert EL, Michels KB. 10.  et al. 2011. Gestational weight gain and daughter's age at menarche. J. Womens Health 20:1193–200 [Google Scholar]
  11. Britton JA, Wolff MS, Lapinski R, Forman J, Hochman S. 11.  et al. 2004. Characteristics of pubertal development in a multi-ethnic population of nine-year-old girls. Ann. Epidemiol. 14:179–87 [Google Scholar]
  12. Buchan DS, Ollis S, Young JD, Thomas NE, Cooper SM. 12.  et al. 2011. The effects of time and intensity of exercise on novel and established markers of CVD in adolescent youth. Am. J. Hum. Biol. 23:517–26 [Google Scholar]
  13. Buyken AE, Karaolis-Danckert N, Remer T. 13.  2009. Association of prepubertal body composition in healthy girls and boys with the timing of early and late pubertal markers. Am. J. Clin. Nutr. 89:221–30 [Google Scholar]
  14. Carwile JL, Willett WC, Spiegelman D, Hertzmark E, Rich-Edwards J. 14.  et al. 2015. Sugar-sweetened beverage consumption and age at menarche in a prospective study of US girls. Hum. Reprod. 30:675–83 [Google Scholar]
  15. Carwile JL, Willett WC, Wang M, Rich-Edwards J, Frazier AL, Michels KB. 15.  2015. Milk consumption after age 9 years does not predict age at menarche. J. Nutr. 145:1900–8 [Google Scholar]
  16. Charalampopoulos D, McLoughlin A, Elks CE, Ong KK. 16.  2014. Age at menarche and risks of all-cause and cardiovascular death: a systematic review and meta-analysis. Am. J. Epidemiol. 180:29–40 [Google Scholar]
  17. Cheng G, Buyken AE, Shi L, Karaolis-Danckert N, Kroke A. 17.  et al. 2012. Beyond overweight: nutrition as an important lifestyle factor influencing timing of puberty. Nutr. Rev. 70:133–52 [Google Scholar]
  18. Cheng G, Remer T, Prinz-Langenohl R, Blaszkewicz M, Degen GH, Buyken AE. 18.  2010. Relation of isoflavones and fiber intake in childhood to the timing of puberty. Am. J. Clin. Nutr. 92:556–64 [Google Scholar]
  19. Chevalley T, Rizzoli R, Hans D, Ferrari S, Bonjour JP. 19.  2005. Interaction between calcium intake and menarcheal age on bone mass gain: an eight-year follow-up study from prepuberty to postmenarche. J. Clin. Endocrinol. Metab. 90:44–51 [Google Scholar]
  20. Cnattingius S, Villamor E, Lagerros YT, Wikstrom AK, Granath F. 20.  2012. High birth weight and obesity—a vicious circle across generations. Int. J. Obes. 36:1320–24 [Google Scholar]
  21. Colditz GA, Bohlke K, Berkey CS. 21.  2014. Breast cancer risk accumulation starts early: Prevention must also. Breast Cancer Res. Treat. 145:567–79 [Google Scholar]
  22. de Ridder CM, Thijssen JH, Van ‘t Veer P, van Duuren R, Bruning PF. 22.  et al. 1991. Dietary habits, sexual maturation, and plasma hormones in pubertal girls: a longitudinal study. Am. J. Clin. Nutr. 54:805–13 [Google Scholar]
  23. Deardorff J, Berry-Millett R, Rehkopf D, Luecke E, Lahiff M, Abrams B. 23.  2013. Maternal pre-pregnancy BMI, gestational weight gain, and age at menarche in daughters. Matern. Child Health J. 17:1391–98 [Google Scholar]
  24. Dorgan JF, Hunsberger SA, McMahon RP, Kwiterovich PO Jr, Lauer RM. 24.  et al. 2003. Diet and sex hormones in girls: findings from a randomized controlled clinical trial. J. Natl. Cancer Inst. 95:132–41 [Google Scholar]
  25. Dorgan JF, McMahon RP, Friedman LA, Van Horn L, Snetselaar LG. 25.  et al. 2006. Diet and sex hormones in boys: findings from the dietary intervention study in children. J. Clin. Endocrinol. Metab. 91:3992–96 [Google Scholar]
  26. dos Santos Silva I, De Stavola BL, Mann V, Kuh D, Hardy R, Wadsworth ME. 26.  2002. Prenatal factors, childhood growth trajectories and age at menarche. Int. J. Epidemiol. 31:405–12 [Google Scholar]
  27. Dossus L, Allen N, Kaaks R, Bakken K, Lund E. 27.  et al. 2010. Reproductive risk factors and endometrial cancer: The European Prospective Investigation into Cancer and Nutrition. Int. J. Cancer 127:442–51 [Google Scholar]
  28. Downing J, Bellis MA. 28.  2009. Early pubertal onset and its relationship with sexual risk taking, substance use and anti-social behaviour: a preliminary cross-sectional study. BMC Public Health 9:446 [Google Scholar]
  29. Dunbar J, Sheeder J, Lezotte D, Dabelea D, Stevens-Simon C. 29.  2008. Age at menarche and first pregnancy among psychosocially at-risk adolescents. Am. J. Public Health 98:1822–24 [Google Scholar]
  30. Euling SY, Selevan SG, Pescovitz OH, Skakkebaek NE. 30.  2008. Role of environmental factors in the timing of puberty. Pediatrics 121:Suppl. 3S167–71 [Google Scholar]
  31. Frisch RE. 31.  1972. Weight at menarche: similarity for well-nourished and undernourished girls at differing ages, and evidence for historical constancy. Pediatrics 50:445–50 [Google Scholar]
  32. Frisch RE. 32.  1976. Fatness of girls from menarche to age 18 years, with a nomogram. Hum. Biol. 48:353–59 [Google Scholar]
  33. Frisch RE, Revelle R. 33.  1970. Height and weight at menarche and a hypothesis of critical body weights and adolescent events. Science 169:397–99 [Google Scholar]
  34. Frisch RE, Wyshak G, Vincent L. 34.  1980. Delayed menarche and amenorrhea in ballet dancers. N. Engl. J. Med. 303:17–19 [Google Scholar]
  35. Georgopoulos N, Markou K, Theodoropoulou A, Paraskevopoulou P, Varaki L. 35.  et al. 1999. Growth and pubertal development in elite female rhythmic gymnasts. J. Clin. Endocrinol. Metab. 84:4525–30 [Google Scholar]
  36. Gluckman PD, Hanson MA. 36.  2006. Evolution, development and timing of puberty. Trends Endocrinol. Metab. 17:7–12 [Google Scholar]
  37. Glynn JR, Kayuni N, Gondwe L, Price AJ, Crampin AC. 37.  2014. Earlier menarche is associated with a higher prevalence of Herpes simplex type-2 (HSV-2) in young women in rural Malawi. eLIFE 3:e01604 [Google Scholar]
  38. Golub MS, Collman GW, Foster PM, Kimmel CA, Rajpert-De Meyts E. 38.  et al. 2008. Public health implications of altered puberty timing. Pediatrics 121:Suppl. 3S218–30 [Google Scholar]
  39. Grundmann M, von Versen-Hoynck F. 39.  2011. Vitamin D - roles in women's reproductive health?. Reprod. Biol. Endocrinol. 9:146 [Google Scholar]
  40. Gunther AL, Karaolis-Danckert N, Kroke A, Remer T, Buyken AE. 40.  2010. Dietary protein intake throughout childhood is associated with the timing of puberty. J. Nutr. 140:565–71 [Google Scholar]
  41. Gurd B, Klentrou P. 41.  2003. Physical and pubertal development in young male gymnasts. J. Appl. Physiol. 1985 95:1011–15 [Google Scholar]
  42. Halsted JA, Ronaghy HA, Abadi P, Haghshenass M, Amirhakemi GH. 42.  et al. 1972. Zinc deficiency in man. The Shiraz experiment. Am. J. Med. 53:277–84 [Google Scholar]
  43. He C, Zhang C, Hunter DJ, Hankinson SE, Buck Louis GM. 43.  et al. 2010. Age at menarche and risk of type 2 diabetes: results from 2 large prospective cohort studies. Am. J. Epidemiol. 171:334–44 [Google Scholar]
  44. He Q, Karlberg J. 44.  2001. BMI in childhood and its association with height gain, timing of puberty, and final height. Pediatr. Res. 49:244–51 [Google Scholar]
  45. Hughes IA. 45.  2013. Releasing the brake on puberty. N. Engl. J. Med. 368:2513–15 [Google Scholar]
  46. Jansen EC, Herran OF, Villamor E. 46.  2015. Trends and correlates of age at menarche in Colombia: results from a nationally representative survey. Econ. Hum. Biol. 19:138–44 [Google Scholar]
  47. Jansen EC, Marin C, Mora-Plazas M, Villamor E. 47.  2016. Childhood red meat intake frequency is associated with earlier age at menarche. J. Nutr. In press [Google Scholar]
  48. Kale A, Deardorff J, Lahiff M, Laurent C, Greenspan LC. 48.  et al. 2015. Breastfeeding versus formula-feeding and girls' pubertal development. Matern. Child Health J. 19:519–27 [Google Scholar]
  49. Karaolis-Danckert N, Buyken AE, Sonntag A, Kroke A. 49.  2009. Birth and early life influences on the timing of puberty onset: results from the DONALD (DOrtmund Nutritional and Anthropometric Longitudinally Designed) Study. Am. J. Clin. Nutr. 90:1559–65 [Google Scholar]
  50. Keim SA, Branum AM, Klebanoff MA, Zemel BS. 50.  2009. Maternal body mass index and daughters' age at menarche. Epidemiology 20:677–81 [Google Scholar]
  51. Kennedy GC. 51.  1969. Interactions between feeding behavior and hormones during growth. Ann. N. Y. Acad. Sci. 157:1049–61 [Google Scholar]
  52. Kerver JM, Gardiner JC, Dorgan JF, Rosen CJ, Velie EM. 52.  2010. Dietary predictors of the insulin-like growth factor system in adolescent females: results from the Dietary Intervention Study in Children (DISC). Am. J. Clin. Nutr. 91:643–50 [Google Scholar]
  53. Kissinger DG, Sanchez A. 53.  1987. The association of dietary factors with age at menarche. Nutr. Res. 7:471–79 [Google Scholar]
  54. Koo MM, Rohan TE, Jain M, McLaughlin JR, Corey PN. 54.  2002. A cohort study of dietary fibre intake and menarche. Public Health Nutr. 5:353–60 [Google Scholar]
  55. Koprowski C, Ross RK, Mack WJ, Henderson BE, Bernstein L. 55.  1999. Diet, body size and menarche in a multiethnic cohort. Br. J. Cancer 79:1907–11 [Google Scholar]
  56. Kuzawa CW, McDade TW, Adair LS, Lee N. 56.  2010. Rapid weight gain after birth predicts life history and reproductive strategy in Filipino males. PNAS 107:16800–5 [Google Scholar]
  57. Kwok MK, Leung GM, Lam TH, Schooling CM. 57.  2012. Breastfeeding, childhood milk consumption, and onset of puberty. Pediatrics 130:e631–39 [Google Scholar]
  58. Lee HA, Kim YJ, Lee H, Gwak HS, Hong YS. 58.  et al. 2015. The preventive effect of breast-feeding for longer than 6 months on early pubertal development among children aged 7–9 years in Korea. Public Health Nutr. 6:1–8 [Google Scholar]
  59. Lee JM, Appugliese D, Kaciroti N, Corwyn RF, Bradley RH, Lumeng JC. 59.  2007. Weight status in young girls and the onset of puberty. Pediatrics 119:e624–30 [Google Scholar]
  60. Lee JM, Kaciroti N, Appugliese D, Corwyn RF, Bradley RH, Lumeng JC. 60.  2010. Body mass index and timing of pubertal initiation in boys. Arch. Pediatr. Adolesc. Med. 164:139–44 [Google Scholar]
  61. Li SJ, Paik HY, Joung H. 61.  2006. Dietary patterns are associated with sexual maturation in Korean children. Br. J. Nutr. 95:817–23 [Google Scholar]
  62. Maclure M, Travis LB, Willett W, MacMahon B. 62.  1991. A prospective cohort study of nutrient intake and age at menarche. Am. J. Clin. Nutr. 54:649–56 [Google Scholar]
  63. Maisonet M, Christensen KY, Rubin C, Holmes A, Flanders WD. 63.  et al. 2010. Role of prenatal characteristics and early growth on pubertal attainment of British girls. Pediatrics 126:e591–600 [Google Scholar]
  64. Malina RM, Spirduso WW, Tate C, Baylor AM. 64.  1978. Age at menarche and selected menstrual characteristics in athletes at different competitive levels and in different sports. Med. Sci. Sports 10:218–22 [Google Scholar]
  65. Martin RM, Patel R, Kramer MS, Guthrie L, Vilchuck K. 65.  et al. 2013. Effects of promoting longer-term and exclusive breastfeeding on adiposity and insulin-like growth factor-I at age 11.5 years: a randomized trial. JAMA 309:1005–13 [Google Scholar]
  66. McGuinn LA, Ghazarian AA, Joseph Su L, Ellison GL. 66.  2015. Urinary bisphenol A and age at menarche among adolescent girls: evidence from NHANES 2003–2010. Environ. Res. 136:381–86 [Google Scholar]
  67. Merzenich H, Boeing H, Wahrendorf J. 67.  1993. Dietary fat and sports activity as determinants for age at menarche. Am. J. Epidemiol. 138:217–24 [Google Scholar]
  68. Mesa JM, Araujo C, Horta BL, Gigante DP. 68.  2010. Growth patterns in early childhood and the onset of menarche before age twelve. Rev. Saude Publica 44:249–60 [Google Scholar]
  69. Meyer F, Moisan J, Marcoux D, Bouchard C. 69.  1990. Dietary and physical determinants of menarche. Epidemiology 1:377–81 [Google Scholar]
  70. Moisan J, Meyer F, Gingras S. 70.  1990. A nested case-control study of the correlates of early menarche. Am. J. Epidemiol. 132:953–61 [Google Scholar]
  71. Morris DH, Jones ME, Schoemaker MJ, Ashworth A, Swerdlow AJ. 71.  2010. Determinants of age at menarche in the UK: analyses from the Breakthrough Generations Study. Br. J. Cancer 103:1760–64 [Google Scholar]
  72. Mueller NT, Jacobs DR Jr, MacLehose RF, Demerath EW, Kelly SP. 72.  et al. 2015. Consumption of caffeinated and artificially sweetened soft drinks is associated with risk of early menarche. Am. J. Clin. Nutr. 102:648–54 [Google Scholar]
  73. Parent AS, Franssen D, Fudvoye J, Gerard A, Bourguignon JP. 73.  2015. Developmental variations in environmental influences including endocrine disruptors on pubertal timing and neuroendocrine control: revision of human observations and mechanistic insight from rodents. Front. Neuroendocrinol. 38:12–36 [Google Scholar]
  74. Persson I, Ahlsson F, Ewald U, Tuvemo T, Qingyuan M. 74.  et al. 1999. Influence of perinatal factors on the onset of puberty in boys and girls: implications for interpretation of link with risk of long term diseases. Am. J. Epidemiol. 150:747–55 [Google Scholar]
  75. Petridou E, Syrigou E, Toupadaki N, Zavitsanos X, Willett W, Trichopoulos D. 75.  1996. Determinants of age at menarche as early life predictors of breast cancer risk. Int. J. Cancer 68:193–98 [Google Scholar]
  76. Pinkney J, Streeter A, Hosking J, Mostazir M, Jeffery A, Wilkin T. 76.  2014. Adiposity, chronic inflammation, and the prepubertal decline of sex hormone binding globulin in children: evidence for associations with the timing of puberty (Earlybird 58). J. Clin. Endocrinol. Metab. 99:3224–32 [Google Scholar]
  77. Prentice A, Dibba B, Sawo Y, Cole TJ. 77.  2012. The effect of prepubertal calcium carbonate supplementation on the age of peak height velocity in Gambian adolescents. Am. J. Clin. Nutr. 96:1042–50 [Google Scholar]
  78. Ramezani Tehrani F, Moslehi N, Asghari G, Gholami R, Mirmiran P, Azizi F. 78.  2013. Intake of dairy products, calcium, magnesium, and phosphorus in childhood and age at menarche in the Tehran Lipid and Glucose Study. PLOS ONE 8:e57696 [Google Scholar]
  79. Rasmussen AR, Wohlfahrt-Veje C, Tefre de Renzy-Martin K, Hagen CP, Tinggaard J. 79.  et al. 2015. Validity of self-assessment of pubertal maturation. Pediatrics 135:86–93 [Google Scholar]
  80. Rogers IS, Northstone K, Dunger DB, Cooper AR, Ness AR, Emmett PM. 80.  2010. Diet throughout childhood and age at menarche in a contemporary cohort of British girls. Public Health Nutr. 13:2052–63 [Google Scholar]
  81. Salgin B, Norris SA, Prentice P, Pettifor JM, Richter LM. 81.  et al. 2015. Even transient rapid infancy weight gain is associated with higher BMI in young adults and earlier menarche. Int. J. Obes. 39:939–44 [Google Scholar]
  82. Segovia-Siapco G, Pribis P, Messina M, Oda K, Sabate J. 82.  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 [Google Scholar]
  83. Smith JT, Acohido BV, Clifton DK, Steiner RA. 83.  2006. KiSS-1 neurones are direct targets for leptin in the ob/ob mouse. J. Neuroendocrinol. 18:298–303 [Google Scholar]
  84. Smithers LG, Kramer MS, Lynch JW. 84.  2015. Effects of breastfeeding on obesity and intelligence: causal insights from different study designs. JAMA Pediatr. 169:707–8 [Google Scholar]
  85. Strom BL, Schinnar R, Ziegler EE, Barnhart KT, Sammel MD. 85.  et al. 2001. Exposure to soy-based formula in infancy and endocrinological and reproductive outcomes in young adulthood. JAMA 286:807–14 [Google Scholar]
  86. Tanner JM. 86.  1962. Growth at Adolescence Springfield, IL: Thomas [Google Scholar]
  87. Thankamony A, Ong KK, Ahmed ML, Ness AR, Holly JM, Dunger DB. 87.  2012. Higher levels of IGF-I and adrenal androgens at age 8 years are associated with earlier age at menarche in girls. J. Clin. Endocrinol. Metab. 97:E786–90 [Google Scholar]
  88. Tinggaard J, Mieritz MG, Sorensen K, Mouritsen A, Hagen CP. 88.  et al. 2012. The physiology and timing of male puberty. Curr. Opin. Endocrinol. Diabetes Obes. 19:197–203 [Google Scholar]
  89. Trussell J. 89.  1980. Statistical flaws in evidence for the Frisch hypothesis that fatness triggers menarche. Hum. Biol. 52:711–20 [Google Scholar]
  90. Villamor E, Marin C, Mora-Plazas M, Baylin A. 90.  2011. Vitamin D deficiency and age at menarche: a prospective study. Am. J. Clin. Nutr. 94:1020–25 [Google Scholar]
  91. Wang Y, Dinse GE, Rogan WJ. 91.  2012. Birth weight, early weight gain and pubertal maturation: a longitudinal study. Pediatr. Obes. 7:101–9 [Google Scholar]
  92. Watkins DJ, Tellez-Rojo MM, Ferguson KK, Lee JM, Solano-Gonzalez M. 92.  et al. 2014. In utero and peripubertal exposure to phthalates and BPA in relation to female sexual maturation. Environ. Res. 134:233–41 [Google Scholar]
  93. Wiley AS. 93.  2011. Milk intake and total dairy consumption: associations with early menarche in NHANES 1999–2004. PLOS ONE 6:e14685 [Google Scholar]
  94. Yermachenko A, Dvornyk V. 94.  2014. Nongenetic determinants of age at menarche: a systematic review. Biomed. Res. Int. 2014:371583 [Google Scholar]
  95. Zadik Z, Sinai T, Zung A, Reifen R. 95.  2004. Vitamin A and iron supplementation is as efficient as hormonal therapy in constitutionally delayed children. Clin. Endocrinol. 60:682–87 [Google Scholar]
  96. Zhang Y, Cao Y, Shi H, Jiang X, Zhao Y. 96.  et al. 2015. Could exposure to phthalates speed up or delay pubertal onset and development? A 1.5-year follow-up of a school-based population. Environ. Int. 83:41–49 [Google Scholar]
  97. Zhu K, Zhang Q, Foo LH, Trube A, Ma G. 97.  et al. 2006. Growth, bone mass, and vitamin D status of Chinese adolescent girls 3 y after withdrawal of milk supplementation. Am. J. Clin. Nutr. 83:714–21 [Google Scholar]
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