[en] The aim of this chapter is to revise some common views on changes in pubertal timing. This revision is based on recent epidemiological findings on the clinical indicators of pubertal timing and data on environmental factor effects and underlying mechanisms. A current advancement in timing of female puberty is usually emphasized. It appears, however, that timing is also changing in males. Moreover, the changes are towards earliness for initial pubertal stages and towards lateness for final stages in both sexes. Such observations indicate the complexity of environmental influences on pubertal timing. The mechanisms of changes in pubertal timing may involve both the central neuroendocrine control and peripheral effects at tissues targeted by gonadal steroids. While sufficient energy availability is a clue to the mechanism of pubertal development, changes in the control of both energy balance and reproduction may vary under the influence of common determinants such as endocrine-disrupting chemicals (EDCs). These effects can take place right before puberty as well as much earlier, during fetal and neonatal life. Finally, environmental factors can interact with genetic factors in determining changes in pubertal timing. Therefore, the variance in pubertal timing is no longer to be considered under absolutely separate control by environmental and genetic determinants. Some recommendations are provided for evaluation of EDC impact in the management of pubertal disorders and for possible reduction of EDC exposure along the precautionary principle.
Disciplines :
Endocrinology, metabolism & nutrition Pediatrics
Author, co-author :
Parent, Anne-Simone ; Université de Liège > Département des sciences cliniques > Pédiatrie
Franssen, Delphine ; Université de Liège > Département des sciences cliniques > Pédiatrie
Herman-Giddens ME, Slora EJ, Wasserman RC, Bourdony CJ, Bhapkar MV, Koch GG, Hasemeier CM: Secondary sexual characteristics and menses in young girls seen in office practice: a study from the Pediatric Research in Office Settings Network. Pediatrics 1997; 99: 505-512.
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-e939.
Herman-Giddens ME, Steffes J, Harris D, Slora E, Hussey M, Dowshen SA, Wasserman R, Serwint JR, Smitherman L, Reiter EO: Secondary sexual characteristics in boys: data from the Pediatric Research in Office Settings Network. Pediatrics 2012; 130:e1058-e1068.
Krstevska-Konstantinova M, Charlier C, Craen M, Du Caju M, Heinrichs C, de Beaufort C, Plomteux G, Bourguignon JP: Sexual precocity after immigration from developing countries to Belgium: evidence of previous exposure to organochlorine pesticides. Hum Reprod 2001; 16: 1020-1026.
Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP: The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev 2003; 24: 668-693.
Parent AS, Franssen D, Fudvoye J, Gerard A, Bourguignon JP: 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 2015; 38: 12-36.
Jeurissen A: Age of the establishment of the menarche and its evolution in Belgium during the last 40 years (in French). Acta Paediatr Belg 1969; 23: 319-330.
Vercauteren M, Susanne C: The secular trend of height and menarche in Belgium: are there any signs of a future stop? Eur J Pediatr 1985; 144: 306-309.
Roelants M, Hauspie R, Hoppenbrouwers K: References for growth and pubertal development from birth to 21 years in Flanders, Belgium. Ann Hum Biol 2009; 36: 680-694.
Talma H, Schonbeck Y, van Dommelen P, Bakker B, van Buuren S, Hirasing RA: Trends in menarcheal age between 1955 and 2009 in the Netherlands. PLoS One 2013; 8:e60056.
Aksglaede L, Olsen LW, Sorensen TI, Juul A: Forty years trends in timing of pubertal growth spurt in 157,000 Danish school children. PLoS One 2008; 3: e2728.
Sorensen K, Aksglaede L, Petersen JH, Juul A: Recent changes in pubertal timing in healthy Danish boys: associations with body mass index. J Clin Endocrinol Metab 2010; 95: 263-270.
Juul A, Magnusdottir S, Scheike T, Prytz S, Skakkebaek NE: Age at voice break in Danish boys: effects of pre-pubertal body mass index and secular trend. Int J Androl 2007; 30: 537-542.
Mul D, Fredriks AM, van Buuren S, Oostdijk W, Verloove-Vanhorick SP, Wit JM: Pubertal development in the Netherlands 1965-1997. Pediatr Res 2001; 50: 479-486.
Clavel-Chapelon F; E3N-EPIC Group, European Prospective Investigation into Cancer: Evolution of age at menarche and at onset of regular cycling in a large cohort of French women. Hum Reprod 2002; 17: 228-232.
Bourguignon JP, Juul A: Normal female puberty in a developmental perspective. Endocr Dev 2012; 22: 11-23.
Stattin H, Kerr M, Skoog T: Early pubertal timing and girls' problem behavior: integrating two hypotheses. J Youth Adolesc 2011; 40: 1271-1287.
Petersen AC: Adolescent development. Annu Rev Psychol 1988; 39: 583-607.
Patton GC, McMorris BJ, Toumbourou JW, Hemphill SA, Donath S, Catalano RF: Puberty and the onset of substance use and abuse. Pediatrics 2004; 114: e300-e306.
Boynton-Jarrett R, Wright RJ, Putnam FW, Lividoti Hibert E, Michels KB, Forman MR, Rich-Edwards J: Childhood abuse and age at menarche. J Adolesc Health 2013; 52: 241-247.
Biro FM, Huang B, Crawford PB, Lucky AW, Striegel-Moore R, Barton BA, Daniels S: Pubertal correlates in black and white girls. J Pediatr 2006; 148: 234-240.
Kulin HE, Grumbach MM, Kaplan SL: Changing sensitivity of the pubertal gonadal hypothalamic feedback mechanism in man. Science 1969; 166: 1012-1013.
Rasier G, Parent AS, Gerard A, Lebrethon MC, Bourguignon JP: Early maturation of gonadotropinreleasing hormone secretion and sexual precocity after exposure of infant female rats to estradiol or dichlorodiphenyltrichloroethane. Biol Reprod 2007; 77: 734-742.
Rasier G, Parent AS, Gerard A, Denooz R, Lebrethon MC, Charlier C, Bourguignon JP: Mechanisms of interaction of endocrine-disrupting chemicals with glutamate-evoked secretion of gonadotropin-releasing hormone. Toxicol Sci 2008; 102: 33-41.
Ibanez L, Lopez-Bermejo A, Diaz M, Marcos MV: Endocrinology and gynecology of girls and women with low birth weight. Fetal Diagn Ther 2011; 30: 243-249.
Biro FM, Khoury P, Morrison JA: Influence of obesity on timing of puberty. Int J Androl 2006; 29: 272-277; discussion 286-290.
Dunger DB, Ahmed ML, Ong KK: Early and late weight gain and the timing of puberty. Mol Cell Endocrinol 2006; 254-255: 140-145.
Ong KK, Potau N, Petry CJ, Jones R, Ness AR, Honour JW, de Zegher F, Ibanez L, Dunger DB; Avon Longitudinal Study of Parents and Children Study Team: Opposing influences of prenatal and postnatal weight gain on adrenarche in normal boys and girls. J Clin Endocrinol Metab 2004; 89: 2647-2651.
Cheng G, Buyken AE, Shi L, Karaolis-Danckert N, Kroke A, Wudy SA, Degen GH, Remer T: Beyond overweight: nutrition as an important lifestyle factor influencing timing of puberty. Nutr Rev 2012; 70: 133-152.
Himes JH: Examining the evidence for recent secular changes in the timing of puberty in US children in light of increases in the prevalence of obesity. Mol Cell Endocrinol 2006; 254-255: 13-21.
Roa J, Tena-Sempere M: Energy balance and puberty onset: emerging role of central mTOR signaling. Trends Endocrinol Metab 2010; 21: 519-528.
Ong KK, Ahmed ML, Dunger DB: Lessons from large population studies on timing and tempo of puberty (secular trends and relation to body size): the European trend. Mol Cell Endocrinol 2006; 254-255: 8-12.
Ibanez L, Jimenez R, de Zegher F: Early pubertymenarche after precocious pubarche: relation to prenatal growth. Pediatrics 2006; 117: 117-121.
van Noord PA, Kaaks R: The effect of wartime conditions and the 1944-45 'Dutch famine' on recalled menarcheal age in participants of the DOM breast cancer screening project. Ann Hum Biol 1991; 18: 57-70.
Tahirovic HF: Menarchal age and the stress of war: an example from Bosnia. Eur J Pediatr 1998; 157: 978-980.
Moffitt TE, Caspi A, Belsky J, Silva PA: Childhood experience and the onset of menarche: a test of a sociobiological model. Child Dev 1992; 63: 47-58.
Wierson M, Long PJ, Forehand RL: Toward a new understanding of early menarche: the role of environmental stress in pubertal timing. Adolescence 1993; 28: 913-924.
Lomniczi A, Loche A, Castellano JM, Ronnekleiv OK, Bosch M, Kaidar G, Knoll JG, Wright H, Pfeifer GP, Ojeda SR: Epigenetic control of female puberty. Nat Neurosci 2013; 16: 281-289.
Lebrethon MC, Aganina A, Fournier M, Gerard A, Parent AS, Bourguignon JP: Effects of in vivo and in vitro administration of ghrelin, leptin and neuropeptide mediators on pulsatile gonadotrophin-releasing hormone secretion from male rat hypothalamus before and after puberty. J Neuroendocrinol 2007; 19: 181-188.
Bourguignon JP, Franssen D, Gerard A, Janssen S, Pinson A, Naveau E, Parent AS: Early neuroendocrine disruption in hypothalamus and hippocampus: developmental effects including female sexual maturation and implications for endocrine disrupting chemical screening. J Neuroendocrinol 2013; 25: 1079-1087.
Bourguignon JP, Rasier G, Lebrethon MC, Gerard A, Naveau E, Parent AS: Neuroendocrine disruption of pubertal timing and interactions between homeostasis of reproduction and energy balance. Mol Cell Endocrinol 2010; 324: 110-120.
Franssen D, Ioannou YS, Alvarez-Real A, Gerard A, Mueller JK, Heger S, Bourguignon JP, Parent AS: Pubertal timing after neonatal diethylstilbestrol exposure in female rats: neuroendocrine vs peripheral effects and additive role of prenatal food restriction. Reprod Toxicol 2014; 44: 63-72.
Swan SH, Main KM, Liu F, Stewart SL, Kruse RL, Calafat AM, Mao CS, Redmon JB, Ternand CL, Sullivan S, Teague JL; Study for Future Families Research Team: Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect 2005; 113: 1056-1061.
Barrett ES, Redmon JB, Wang C, Sparks A, Swan SH: Exposure to prenatal life events stress is associated with masculinized play behavior in girls. Neurotoxicology 2014; 41: 20-27.
Bourguignon JP: Linear growth as a function of age at onset of puberty and sex steroid dosage: therapeutic implications. Endocr Rev 1988; 9: 467-488.
Smith EP, Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, Williams TC, Lubahn DB, Korach KS: Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med 1994; 331: 1056-1061.
Carani C, Qin K, Simoni M, Faustini-Fustini M, Serpente S, Boyd J, Korach KS, Simpson ER: Effect of testosterone and estradiol in a man with aromatase deficiency. N Engl J Med 1997; 337: 91-95.
Hero M, Wickman S, Dunkel L: Treatment with the aromatase inhibitor letrozole during adolescence increases near-final height in boys with constitutional delay of puberty. Clin Endocrinol 2006; 64: 510-513.
