Abstract
Puberty is a period of physical and psychological maturation, with long-term effects on health. During the 20th century, a secular trend towards earlier puberty occurred in association with improvements in nutrition. The worldwide pandemic of childhood obesity has renewed interest in the relationship between body composition in childhood and the timing and tempo of puberty. Limited evidence suggests that earlier puberty is associated with a tendency towards central fat deposition; therefore, pubertal status needs to be carefully considered in the categorization of childhood and adolescent overweight and obesity. In the other direction, rapid early weight gain is associated with advanced puberty in both sexes, and a clear association exists between increasing BMI and earlier pubertal development in girls. Evidence in boys is less clear, with the majority of studies showing obesity to be associated with earlier puberty and voice break, although a subgroup of boys with obesity exhibits late puberty, perhaps as a variation of constitutional delay in growth and puberty. The possible mechanisms linking adiposity with pubertal timing are numerous, but leptin, adipocytokines and gut peptides are central players. Other possible mediators include genetic variation and environmental factors such as endocrine disrupting chemicals. This Review presents current evidence on this topic, highlighting inconsistencies and opportunities for future research.
Key Points
-
Rapid early weight gain during infancy is associated with advanced puberty in both sexes
-
Clear associations exist between increased BMI values and early pubertal development in girls
-
In boys, the effect of obesity on pubertal timing is controversial, although the majority of studies show obesity to be associated with early puberty
-
Limited evidence suggests that early puberty is associated with a tendency to central fat deposition
-
The mechanisms that link adiposity and timing of puberty remain unclear but probably involve leptin, adipocytokines, gut peptides, genetic variations and environmental factors
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Change history
29 March 2012
In the version of this article initially published the name of one of the authors, Matthew A. Sabin, was spelt incorrectly. The error has been corrected for the HTML and PDF versions of the article.
References
Frisch, R. E. & Revelle, R. Height and weight at menarche and a hypothesis of critical body weights and adolescent events. Science 169, 397–399 (1970).
Johnston, F. E. et al. Height, weight and age at menarche and the “critical weight” hypothesis. Science 174, 1148–1149 (1971).
Frisch, R. E. Pubertal adipose tissue: is it necessary for normal sexual maturation? Evidence from the rat and human female. Fed. Proc. 39, 2395–2400 (1980).
Parent, A. S. et al. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr. Rev. 24, 668–693 (2003).
de Muinck Keizer, S. M. & Mul, D. Trends in pubertal development in Europe. Hum. Reprod. Update 7, 287–291 (2001).
Mul, D. et al. Pubertal development in The Netherlands 1965–1997. Pediatr. Res. 50, 479–486 (2001).
Bourguignon, J. P. et al. Neuroendocrine disruption of pubertal timing and interactions between homeostasis of reproduction and energy balance. Mol. Cell. Endocrinol. 324, 110–120 (2010).
Herman-Giddens, M. E. et al. Secondary sexual characteristics and menses in young girls seen in office practice: a study from the Pediatric Research in Office Settings network. Pediatrics 99, 505–512 (1997).
Herman-Giddens, M. E., Wang, L. & Koch, G. Secondary sexual characteristics in boys: estimates from the national health and nutrition examination survey III, 1988–1994. Arch. Pediatr. Adoles. Med. 155, 1022–1028 (2001).
Freedman, D. S. et al. Relation of age at menarche to race, time period, and anthropometric dimensions: the Bogalusa Heart Study. Pediatrics 110, e43 (2002).
Papadimitriou, A. Sex differences in the secular changes in pubertal maturation. Pediatrics 108, e65 (2001).
Boyne, M. S. et al. Developmental origins of cardiovascular risk in Jamaican children: the Vulnerable Windows Cohort study. Br. J. Nutr. 104, 1026–1033 (2010).
Boyne, M. S. et al. Growth, body composition, and the onset of puberty: longitudinal observations in Afro-Caribbean children. J. Clin. Endocrinol. Metab. 95, 3194–3200 (2010).
Prader, A., Largo, R. H., Molinari, L. & Issler, C. Physical growth of Swiss children from birth to 20 years of age. First Zurich longitudinal study of growth and development. Helv. Paediatr. Acta Suppl. 52, 1–125 (1989).
Marshall, W. A. & Tanner, J. M. Variations in the pattern of pubertal changes in boys. Arch. Dis. Child. 45, 13–23 (1970).
Marshall, W. A. & Tanner, J. M. Variations in the pattern of pubertal changes in girls. Arch. Dis. Child. 44, 291–303 (1969).
Martin, D. D., Hauspie, R. C. & Ranke, M. B. Total pubertal growth and markers of puberty onset in adolescents with GHD: comparison between mathematical growth analysis and pubertal staging methods. Horm. Res. 63, 95–101 (2005).
Karlberg, J. & Boepple, P. A. in Sexual Precocity: Etiology, Diagnosis and Management Ch. 9 (eds Grave, G. D. & Cutler, G. B.) 85–95 (Raven Press Ltd, New York, 1993).
Sandhu, J., Ben Shlomo, Y., Cole, T. J., Holly, J. & Davey, S. G. The impact of childhood body mass index on timing of puberty, adult stature and obesity: a follow-up study based on adolescent anthropometry recorded at Christ's Hospital (1936–1964). Int. J. Obes. (Lond.) 30, 14–22 (2006).
Greil, H. & Kahl, H. Assessment of developmental age: cross-sectional analysis of secondary sexual characteristics. Anthropol. Anz. 63, 63–75 (2005).
Roelants, M., Hauspie, R. & Hoppenbrouers, K. References for growth and pubertal development from birth to 21 years in Flanders, Belgium. Ann. Hum. Biol. 36, 680–694 (2009).
Kiess, W. et al. Body fat mass, leptin and puberty. J. Pediatr. Endocrinol. Metab. 13 (Suppl. 1), 717–722 (2000).
Kiess, W. et al. A role for leptin in sexual maturation and puberty? Horm. Res. 51 (Suppl. 3), 55–63 (1999).
Han, J. C., Lawlor, D. A. & Kimm, S. Y. Childhood obesity. Lancet 375, 1737–1748 (2010).
Patton, G. C. & Viner, R. Pubertal transitions in health. Lancet 369, 1130–1139 (2007).
Burt Solorzano, C. M. & McCartney, C. R. Obesity and the pubertal transition in girls and boys. Reproduction 140, 399–410 (2010).
Ong, K. K. et al. Infancy weight gain predicts childhood body fat and age at menarche in girls. J. Clin. Endocrinol. Metab. 94, 1527–1532 (2009).
Ahmed, M. L., Ong, K. K. & Dunger, D. B. Childhood obesity and the timing of puberty. Trends Endocrinol. Metab. 20, 237–242 (2009).
Himes, J. H. 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. 254–255, 13–21 (2006).
Himes, J. P., Park, K. & Styne, D. Menarche and assessment of body mass index in adolescent girls. J. Pediatr. 155, 393–397 (2009).
Veldhuis, J. D. et al. Endocrine control of body fat composition in infancy, childhood, and puberty. Endocr. Rev. 26, 114–146 (2005).
Brook, C., Clayton, P. & Brown, R. Brook's Clinical Pediatric Endocrinology 5th edn (Blackwell Publishing, Oxford, 2005).
Roemmich, J. N., Clark, P. A., Weltman, A. & Rogol, A. D. Alterations in growth and body composition during puberty. I. Comparing multicompartment body composition models. J. Appl. Physiol. 83, 927–935 (1997).
Malina, R. M. & Bouchard, C. Growth, Maturation and Physical Activity 87–100 (Human Kinetics Books, Champaign, 1991).
Christakis, N. A. & Fowler, J. H. The spread of obesity in a large social network over 32 years. N. Engl. J. Med. 357, 370–379 (2007).
Tommiska, J. et al. LIN28B in constitutional delay of growth and puberty. J. Clin. Endocrinol. Metab. 95, 3063–3066 (2010).
Körner, A. et al. Sex-specific effect of the Val1483Ile polymorphism in the fatty acid synthase gene (FAS) on body mass index and lipid profile in Caucasian children. Int. J. Obes. (Lond.) 31, 353–358 (2007).
Ong, K. K. et al. Genetic variation in LIN28B is associated with the timing of puberty. Nat. Genet. 41, 729–733 (2009).
Fraser, A. et al. Association of maternal weight gain in pregnancy with offspring obesity and metabolic and vascular traits in childhood. Circulation 121, 2557–2564 (2010).
Fredriks, A. M. et al. Continuing positive secular growth change in The Netherlands 1955–1997. Pediatr. Res. 47, 316–323 (2000).
Kiess, W., Blüher, S., Kapellen, T. & Körner, A. Metabolic syndrome in children and adolescents: prevalence, public health issue, and time for initiative. J. Pediatr. Gastroenterol. Nutr. 49, 268–271 (2009).
Sharma, M. International school-based interventions for preventing obesity in children. Obes. Rev. 8, 155–167 (2007).
Körner, A. et al. New predictors of the metabolic syndrome in children–role of adipocytokines. Pediatr. Res. 61, 640–645 (2007).
Körner, A., Kiess, W., Stumvoll, M. & Kovacs, P. Polygenic contribution to obesity: genome-wide strategies reveal new targets. Front. Horm. Res. 36, 12–36 (2008).
Wiegand, S. et al. Type 2 diabetes and impaired glucose tolerance in European children and adolescents with obesity—a problem that is no longer restricted to minority groups. Eur. J. Endocrinol. 151, 199–206 (2004).
Sinha, R. et al. Prevalence of impaired glucose tolerance among children and adolescents with marked obesity. N. Engl. J. Med. 346, 802–810 (2002).
Reich, A. et al. Obesity and blood pressure–results from the examination of 2,365 schoolchildren in Germany. Int. J. Obes. Relat. Metab. Disord. 27, 1459–1464 (2003).
Kiess, W. et al. Clinical aspects of obesity in childhood and adolescence. Obes. Rev. 2, 29–36 (2001).
DiVall, S. A. & Radovick, S. Endocrinology of female puberty. Curr. Opin. Endocrinol. Diabetes Obes. 16, 1–4 (2009).
Delemarre-van de Waal, H. A. Regulation of puberty. Best Pract. Res. Clin. Endocrinol. Metab. 16, 1–12 (2002).
Rosenfield, R. L., Cooke, D. W. & Radovick, S. in Pediatric Endocrinology 3rd edn Ch. 14 (ed. Sperling, M. A.) 530–609 (Saunders Elsevier, Philadelphia, 2008).
Ogden, C. & Carroll, M. Prevalence of obesity among children and adolescents: United States, trends 1963–1965 through 2007–2008. National Center for Health Statistics. Division of Health and Nutrition Examination Surveys 17, 1–5 (2010).
Kindblom, J. M. et al. Pubertal timing predicts previous fractures and BMD in young adult men: the GOOD study. J. Bone Miner. Res. 21, 790–795 (2006).
Kindblom, J. M. et al. Pubertal timing is an independent predictor of central adiposity in young adult males: the Gothenburg osteoporosis and obesity determinants study. Diabetes 55, 3047–3052 (2006).
Heger, S. et al. Impact of weight status on the onset and parameters of puberty: analysis of three representative cohorts from central Europe. J. Pediatr. Endocrinol. Metab. 21, 865–877 (2008).
Meigen, C. et al. Secular trends in body mass index in German children and adolescents: a cross-sectional data analysis via CrescNet between 1999 and 2006. Metabolism 57, 934–949 (2008).
Kleber, M., Schwarz, A. & Reinehr, T. Obesity in children and adolescents: relationship to growth, pubarche, menarche, and voice break. J. Pediatr. Endocrinol. Metab. 24, 125–130 (2011).
Sørensen, K., Aksglaede, L., Petersen, J. H. & Juul, A. Recent changes in pubertal timing in healthy Danish boys: associations with body mass index. J. Clin. Endocrinol. Metab. 95, 263–270 (2010).
de Onis, M., Dasgupta, P., Saha, S., Sengupta, D. & Blössner, M. The National Center for Health Statistics reference and the growth of Indian adolescent boys. Amer. J. Clin. Nutr. 74, 248–253 (2001).
Sulem, P. et al. Genome-wide association study identifies sequence variants on 6q21 associated with age at menarche. Nat. Genet. 41, 734–738 (2009).
He, Q. & Karlberg, J. BMI in childhood and its association with height gain, timing of puberty, and final height. Pediatr. Res. 49, 244–251 (2001).
Juul, A., Magnusdottir, S., Scheike, T., Prytz, S. & Skakkebaek, N. E. Age at voice break in Danish boys: effects of pre-pubertal body mass index and secular trend. Int. J. Androl. 30, 537–542 (2007).
Kaplowitz, P. Delayed puberty in obese boys: comparison with constitutional delayed puberty and response to testosterone therapy. J. Pediatr. 133, 745–749 (1998).
Kaplowitz, P. B. Link between body fat and the timing of puberty. Pediatrics 121 (Suppl. 3), S208–S217 (2008).
Nathan, B. M., Sedlmeyer, I. L. & Palmert, M. R. Impact of body mass index on growth in boys with delayed puberty. J. Pediatr. Endocrinol. Metab. 19, 971–977 (2006).
Wang, Y. Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls. Pediatrics 110, 903–910 (2002).
Kaplowitz, P. B., Slora, E. J., Wasserman, R. C., Pedlow, S. E. & Herman-Giddens, M. E. Earlier onset of puberty in girls: relation to increased body mass index and race. Pediatrics 108, 347–353 (2001).
Kirchengast, S. & Bauer, M. Menarcheal onset is associated with body composition parameters but not with socioeconomic status. Coll. Antropol. 31, 419–425 (2007).
Biro, F. M., Huang, B., Morrison, J. A., Horn, P. S. & Daniels, S. R. Body mass index and waist-to-height changes during teen years in girls are influenced by childhood body mass index. J. Adolesc. Health 46, 245–250 (2010).
Biro, F. M., Khoury, P. & Morrison, J. A. Influence of obesity on timing of puberty. Int. J. Androl. 29, 272–277 (2006).
Aksglaede, L., Juul, A., Olsen, L. W. & Sørensen, T. I. Age at puberty and the emerging obesity epidemic. PLoS ONE 4, e8450 (2009).
Aksglaede, L., Sørensen, K., Petersen, J. H., Skakkebaek, N. E. & Juul, A. Recent decline in age at breast development: the Copenhagen Puberty Study. Pediatrics 123, e932–e939 (2009).
Ibáñez, L., Lopez-Bermejo, A., Diaz, M., Marcos, M. V. & de Zegher, F. Early metformin therapy to delay menarche and augment height in girls with precocious pubarche. Fertil. Steril. 95, 727–730 (2011).
Keim, S. A., Branum, A. M., Klebanoff, M. A. & Zemel, B. S. Maternal body mass index and daughters' age at menarche. Epidemiology 20, 677–681 (2009).
Hernández, M. I., Unanue, N., Gaete, X., Cassorla, F. & Codner, E. Age of menarche and its relationship with body mass index and socioeconomic status [Spanish]. Rev. Med. Chil. 135, 1429–1436 (2007).
Salsberry, P. J., Reagan, P. B. & Pajer, K. Growth differences by age of menarche in African American and White girls. Nurs. Res. 58, 382–390 (2009).
Martos-Moreno, G. A., Chowen, J. A. & Argente, J. Metabolic signals in human puberty: effects of over and undernutrition. Mol. Cell. Endocrinol. 324, 70–81 (2010).
Remer, T. et al. Prepubertal adrenarchal androgens and animal protein intake independently and differentially influence pubertal timing. J. Clin. Endocrinol. Metab. 95, 3002–3009 (2010).
McCartney, C. R. et al. Obesity and sex steroid changes across puberty: evidence for marked hyperandrogenemia in pre- and early pubertal obese girls. J. Clin. Endocrinol. Metab. 92, 430–436 (2007).
Dunger, D. B., Ahmed, M. L. & Ong, K. K. Early and late weight gain and the timing of puberty. Mol. Cell. Endocrinol. 254–255, 140–145 (2006).
Gluckman, P. D. & Hanson, M. A. Evolution, development and timing of puberty. Trends Endocrinol. Metab. 17, 7–12 (2006).
Papadimitriou, A., Nicolaidou, P., Fretzayas, A. & Chrousos, G. P. Clinical review: constitutional advancement of growth, a.k.a. early growth acceleration, predicts early puberty and childhood obesity. J. Clin. Endocrinol. Metab. 95, 4535–4541 (2010).
Hoekstra, R. A., Bartels, M. & Boomsma, D. I. Heritability of testosterone levels in 12-year-old twins and its relation to pubertal development. Twin Res. Hum. Genet. 9, 558–565 (2006).
Wehkalampi, K., Widén, E., Laine, T., Palotie, A. & Dunkel, L. Association of the timing of puberty with a chromosome 2 locus. J. Clin. Endocrinol. Metab. 93, 4833–4839 (2008).
Perry, J. R. et al. Meta-analysis of genome-wide association data identifies two loci influencing age at menarche. Nat. Genet. 41, 648–650 (2009).
Castellano, J. M. et al. Early metabolic programming of puberty onset: impact of changes in postnatal feeding and rearing conditions on the timing of puberty and development of the hypothalamic kisspeptin system. Endocrinology 152, 3396–3408 (2011).
Whatmore, A. J., Hall, C. M., Jones, J., Westwood, M. & Clayton, P. E. Ghrelin concentrations in healthy children and adolescents. Clin. Endocrinol. 59, 649–654 (2003).
Pomerants, T., Tillmann, V., Jürimäe, J. & Jürimäe, T. Relationship between ghrelin and anthropometrical, body composition parameters and testosterone levels in boys at different stages of puberty. J. Endocrinol. Invest. 29, 962–967 (2006).
Ebbeling, C. B., Pawlak, D. B. & Ludwig, D. S. Childhood obesity: public-health crisis, common sense cure. Lancet 360, 473–482 (2002).
O˝zen, S. & Darcon, S¸. Effects of environmental endocrine disruptors on pubertal development. J. Clin. Res. Pediatr. Endocrinol. 3, 1–6 (2011).
Parent, A. S. et al. The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr. Rev. 24, 668–693 (2003).
Diamanti-Kandarakis, E. et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr. Rev. 30, 293–342 (2009).
Ibáñez, L., Ferrer, A., Marcos, M. V., Hierro, F. R. & de Zegher, F. Early puberty: rapid progression and reduced final height in girls with low birth weight. Pediatrics 106, e72 (2000).
Adair, L. S. Size at birth predicts age at menarche. Pediatrics 107, e59 (2001).
Tam, C. S., de Zegher, F., Garnett, S. P., Baur, L. A. & Cowell, C. T. Opposing influences of prenatal and postnatal growth on the timing of menarche. J. Clin. Endocrinol. Metab. 91, 4369–4373 (2006).
Dunger, D. B., Ahmed, M. L. & Ong, K. K. Early and late weight gain and the timing of puberty. Mol. Cell. Endocrinol. 254–255, 140–145 (2006).
Ong, K. K. et al. Insulin-like growth factor I concentrations in infancy predict differential gains in body length and adiposity: the Cambridge Baby Growth Study. Am. J. Clin. Nutr. 90, 156–161 (2009).
Acknowledgements
The authors' work is supported by grants from the Deutsche Forschungsgemeinschaft (KFO-152, to A. K., W. K. and R. W. P.) and from the European Community “PIONEER” (to W. K.). W. K. is also being supported by grants from the Federal Ministry of Education and Research (BMBF), Kompetenznetz “Adipositas”, Konsortium 'LARGE' and the IFB Adipositaserkrankungen, University of Leipzig. M. A. S. is supported through a National Health and Medical Research Council Health Professional Training Fellowship (APP1012201), and the Murdoch Childrens Research Institute is supported in part by the Victorian Government's Operational Infrastructure Support Program.
Author information
Authors and Affiliations
Contributions
I. V. Wagner and M. A. Sabin contributed equally to writing the article and also provided a substantial contribution to discussion of content and to reviewing and editing the manuscript before submission, in the capacity of joint first authors. W. Kiess wrote part of the article, researched data for the article, and provided a substantial contribution to discussion of content and to reviewing and editing the manuscript before submission. R. W. Pfäffle, A. Hiemisch, E. Sergeyev and A. Körner researched data for the article, made a substantial contribution to discussion of content and reviewed or editing the manuscript before submission.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Rights and permissions
About this article
Cite this article
Wagner, I., Sabin, M., Pfäffle, R. et al. Effects of obesity on human sexual development. Nat Rev Endocrinol 8, 246–254 (2012). https://doi.org/10.1038/nrendo.2011.241
Published:
Issue Date:
DOI: https://doi.org/10.1038/nrendo.2011.241
This article is cited by
-
Prenatal Exposure to Parental Lifestyle Factors, Diseases, and Use of Medications and Male Pubertal Development: a Review of Epidemiological Studies Published 2017–2022
Current Epidemiology Reports (2023)
-
Prepubertal BMI, pubertal growth patterns, and long-term BMI: Results from a longitudinal analysis in Chinese children and adolescents from 2005 to 2016
European Journal of Clinical Nutrition (2022)
-
The overall diet quality in childhood is prospectively associated with the timing of puberty
European Journal of Nutrition (2021)
-
Maternal pre-pregnancy body mass index, smoking in pregnancy, and alcohol intake in pregnancy in relation to pubertal timing in the children
BMC Pediatrics (2019)
-
Timing of spermarche and menarche among urban students in Guangzhou, China: trends from 2005 to 2012 and association with Obesity
Scientific Reports (2018)