Cited by 1,762Hypothalamic control of reproductive hormonesAdolescent Sexual and Reproductive HealthHuman Health and Disease

The Timing of Normal Puberty and the Age Limits of Sexual Precocity: Variations around the World, Secular Trends, and Changes after Migration

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Parent, Anne-Simone, Teilmann, Grete, Juul, Anders, Skakkebaek, Niels E., Toppari, Jorma, Bourguignon, Jean-Pierre·2003·Endocrine Reviews

Abstract

During the past decade, possible advancement in timing of puberty has been reported in the United States. In addition, early pubertal development and an increased incidence of sexual precocity have been noticed in children, primarily girls, migrating for foreign adoption in several Western European countries. These observations are raising the issues of current differences and secular trends in timing of puberty in relation to ethnic, geographical, and socioeconomic background. None of these factors provide an unequivocal explanation for the earlier onset of puberty seen in the United States. In the formerly deprived migrating children, refeeding and catch-up growth may prime maturation. However, precocious puberty is seen also in some nondeprived migrating children. Attention has been paid to the changing milieu after migration, and recently, the possible role of endocrine- disrupting chemicals from the environment has been considered. These observations urge further study of the onset of puberty as a possible sensitive and early marker of the interactions between environmental conditions and genetic susceptibility that can influence physiological and pathological processes.

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Registry

Crossref · 10.1210/er.2002-0019

Cites

272 of 272 references verified0 citation errors · 0 not checkable

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  • Age of menarche varies between populations, ranging from 11.0 to 14.1 years, with a mean of 12.6 years, and has decreased significantly over the last century.

    “Age of menarche varies between populations, ranging from 11.0 to 14.1 years, with the mean of 12.6 years, and this has decreased significantly over the last century.28”

    From Nutrition in adolescents: physiology, metabolism, and nutritional needs (2017) · cites this paper as [28]

    “Age references in well-off conditions” (p. 5) documents differences between populations, but gives 12.0–13.5 years for Western Europe; it does not give the claimed 11.0–14.1-year range or a cross-population mean of 12.6 years. “Secular trends” (pp. 6–7) reports a marked historical decline, but says more recent trends vary by country and have stalled in some. (LLM, conf=0.90)

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  • Boys' height velocity begins 1-2 years after girls, and as a result boys' growth in height occurs for a longer period than girls, and final adult height is usually achieved by 17 years of age.

    “Boys' height velocity begins 1-2 years after girls, and, as a result, boys' growth in height occurs for a longer period than girls, and final adult height is usually achieved by 17 years of age.28,30”

    From Nutrition in adolescents: physiology, metabolism, and nutritional needs (2017) · cites this paper as [28]

    In “Age references in well-off conditions” (p. 5), the paper says girls classically precede boys by an average of 0.8 years in pubertal onset, while noting that some recent studies found no difference. That partly supports later maturation in boys, but it does not establish that boys’ height velocity begins 1–2 years later, that they grow for longer, or that adult height is usually reached by age 17. The discussion of final height (p. 11) explicitly sets aside pubertal growth and final-height patterns. (LLM, conf=0.79)

    Experimental — accuracy not yet measured
  • In girls with late initiation of puberty, there can be a decrease in the interval between thelarche and menarche.

    “In girls with late initiation of puberty, there can be a decrease in the interval between thelarche and menarche.6”

    From Pubertal development and regulation (2016) · cites this paper as [6]

  • In countries across the globe, the age of puberty has continued to decline.

    “In countries across the globe, the age of puberty has continued to decline”

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Cites

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5 of the 277 references couldn’t be matched to a known paper.

Research works printed but not linked: 9

  1. [65]65. Eveleth PB, Tanner JM 1990 Worldwide variation in human growth, 2nd ed. Cambridge, UK: Cambridge University Press
  2. [95]95. Bodzsar EB, Susanne C 1998 Secular growth change in Europe. Budapest: Eo ¨tvo ¨ University Press
  3. [141]141. Ojeda SR, Ma YJ, Dziedzic B, Prevot V 2000 Astrocyte-neuron signaling and the onset of female puberty. In: Bourguignon JP, Plant TM, eds. The onset of puberty in perspective. Amsterdam: Elsevier Science; 41-57
  4. [203]203. Bourguignon JP, Lebrethon MC, Ge ´rard A, Purnelle G, Vandersmissen E, Parent AS, Yamanaka C 2000 Amino acid neurotransmission and early ontogeny of pulsatile GnRH secretion from the rat hypothalamus. In: Bourguignon JP, Plant TM, eds. The onset of puberty in perspective . Amsterdam: Elsevier Science; 119129
  5. [207]207. Farooqi IS, O'Rahilly S 2000 Human congenital leptin deficiency: the role of leptin in the onset of puberty. In: Bourguignon JP, Plant - TM, eds. The onset of puberty in perspective . Amsterdam: Elsevier Science; 363-369
  6. [208]208. Kalra SP, Pu S, Horvath TL, Kalra PS 2000 Leptin and NPY regulation of GnRH secretion and energy homeostasis. In: Bourguignon JP, Plant TM, eds. The onset of puberty in perspective . Amsterdam: Elsevier Science; 317-327
  7. [209]209. LebrethonMC,VandersmissenE,Ge ´rardA,ParentAS,JunienJL, Bourguignon JP 2000 Leptin and neuropeptide Y stimulation of pulsatile GnRH secretion in vitro through distinct mechanisms. In: BourguignonJP,Plant TM, eds. The onset of puberty in perspective . Amsterdam: Elsevier Science; 329-337
  8. [215]215. d'Alle `ves V, Gruaz-Gumowski NM, Aubert ML 2000 The GHIGF-I axis in sexual maturation: the rat paradigm. In: Bourguignon JP, Plant TM, eds. The onset of puberty in perspective. Amsterdam: Elsevier Science; 59-69
  9. [216]216. Wilson ME, Suter KJ 2000 The GH-IGF-I axis in sexual maturation: the monkey paradigm. In: Bourguignon JP, Plant TM, eds. The onset of puberty in perspective . Amsterdam: Elsevier Science; 71-83

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Authors
Parent, A.-S., Teilmann, G., Juul, A., Skakkebaek, N. E., Toppari, J., & Bourguignon, J.-P.
Affiliations
  • University of Liège (BE)
  • Copenhagen University Hospital (DK)
  • Department of Growth and Reproduction (G.T., A.J., N.E.S.), Copenhagen University Hospital, Rigshospitalet, DK-2100 Copenhagen Ø, Denmark
  • University of Turku (FI)
Corresponding author
Bourguignon, Jean-Pierre
Venue
Endocrine Reviews
Published
2003-10-01
Volume
24
Issue
5
Pages
668-693
ISSN
  • 0163-769X (ISSN-L)
  • 1945-7189
OpenAlex
W2153589742
Cited by
1,762
References
277
Citations by year
2026: 49 · 2025: 73 · 2024: 66 · 2023: 92 · 2022: 94 · 2021: 100 · 2020: 162 · 2019: 102 · 2018: 81 · 2017: 82 · 2016: 81 · 2015: 85 · 2014: 81 · 2013: 101 · 2012: 87
FWCI
7.22
Type
journal article
Language
en
Open access
Locations
  • Endocrine Reviews (publishedVersion)
  • PubMed (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (publishedVersion)
  • ORBi (University of Liège) (submittedVersion, other-oa)
Funders
  • European Commission
  • Fonds De La Recherche Scientifique - FNRS
Topics
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
  • Health Sciences › Health Professions › General Health Professions › Adolescent Sexual and Reproductive Health
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Human Health and Disease
Keywords
timing of puberty, precocious puberty, secular trends, migration, international adoption, catch-up growth, refeeding, ethnic differences, socioeconomic factors, endocrine disruptors, environmental factors, genetic susceptibility, pubertal development
MeSH terms
Age Factors, Child, Climate, Developing Countries, Emigration and Immigration, Female, Humans, Male, Nutritional Physiological Phenomena, Puberty, Puberty, Precocious, Stress, Physiological, Photoperiod

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