Pubertal development in Danish children: comparison of recent European and US data
Abstract
Two recent epidemiological studies (PROS and NHANES III) from the USA noted earlier sexual maturation in girls, leading to increased attention internationally to the age at onset of puberty. We studied the timing of puberty in a large cohort of healthy Danish children in order to evaluate differences between USA and Denmark, as well as to look for possible secular trends in pubertal development. Healthy Caucasian children from public schools in Denmark participated in the study which was carried out in 1991-1993. A total number of 826 boys and 1,100 girls (aged 6.0-19.9 years) were included, and pubertal stages were assessed by clinical examination according to methods of Tanner. In boys testicular volume was determined using an orchidometer. We found that age at breast development 2 (B2) was 10.88 years, and mean menarcheal age was 13.42 years. Girls with body mass index (BMI) above the median had significantly earlier puberty (age at B2 10.42 years) compared with girls with BMI below the median (age at B2 11.24 years, p < 0.0001). Similarly, menarcheal age was significantly lower in girls with BMI above the median compared with girls with BMI below the median (13.12 vs. 13.70 years, p = 0.0012). In Danish boys we found that age at genital stage 2 (G2) was 11.83 years. Both sexes were significantly taller compared with data from 1964, but timing of pubertal maturation seemed unaltered. Finally, puberty occurred much later in Denmark compared with recent data from USA. We could not detect any downwards secular trend in the timing of puberty in Denmark between 1964 and 1991-1993 as seen in the US. Obesity certainly plays a role in the timing of puberty, but the marked differences between Denmark and USA cannot be attributed exclusively to differences in BMI. A possible role of other factors like genetic polymorphisms, nutrition, physical activity or endocrine disrupting chemicals must therefore also be considered. Therefore, we believe it is crucial to monitor the pubertal development closely in Denmark in the coming decades.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Two European studies in which careful physical examination was used to ascertain breast development showed no substantial advance in age of puberty onset.
“By contrast, two European studies in which careful physical examination was used to ascertain breast development showed no substantial advance in age of puberty onset.24,25”
From Pubertal development and regulation (2016) · cites this paper as [25]
Cites
Variations in pattern of pubertal changes in girls
Marshall, W. A., & Tanner, J. M. (1969) · Archives of Disease in Childhood · doi:10.1136/adc.44.235.291 · Cited by 5,963 · see citing works
Variations in the pattern of pubertal changes in boys
Marshall, W. A., & Tanner, J. M. (1970) · Archives of Disease in Childhood · doi:10.1136/adc.45.239.13 · Cited by 5,147 · see citing works
Evidence for decreasing quality of semen during past 50 years.
Carlsen, E., Giwercman, A., Keiding, N., & Skakkebæk, N. E. (1992) · BMJ · doi:10.1136/bmj.305.6854.609 · Cited by 2,768 · see citing works
Self-citationOgden, C. L., Kuczmarski, R. J., Flegal, K. M., Mei, Z., Guo, S. S., Wei, R. X., Grummer‐Strawn, L. M., Curtin, L. R., Roche, A. F., & Johnson, C. L. (2002) · PEDIATRICS · doi:10.1542/peds.109.1.45 · Cited by 2,017 · see citing works
Parent, A.-S., Teilmann, G., Juul, A., Skakkebaek, N. E., Toppari, J., & Bourguignon, J.-P. (2003) · Endocrine Reviews · doi:10.1210/er.2002-0019 · Cited by 1,762 · see citing works
Self-citationHerman-Giddens, M. E., Slora, E. J., Wasserman, R. C., Bourdony, C. J., Bhapkar, M. V., Koch, G. G., & Hasemeier, C. M. (1997) · PEDIATRICS · doi:10.1542/peds.99.4.505 · Cited by 1,709 · see citing works
Juul, A., Bang, P., Hertel, N. T., Main, K., Dalgaard, P., Jørgensen, K., Müller, J., Hall, K. E., & Skakkebaek, N. E. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.78.3.744 · Cited by 773 · see citing works
Self-citationAge at menarche and racial comparisons in US girls
Chumlea, W. C., Schubert, C. M., Roche, A. F., Kulin, H. E., Lee, P. A., Himes, J. H., & Sun, S. S. (2003) · PEDIATRICS · doi:10.1542/peds.111.1.110 · Cited by 685 · see citing works
National Estimates of the Timing of Sexual Maturation and Racial Differences Among US Children
Sun, S. S., Schubert, C. M., Chumlea, W. C., Roche, A. F., Kulin, H. E., Lee, P. A., Himes, J. H., & Ryan, A. S. (2002) · PEDIATRICS · doi:10.1542/peds.110.5.911 · Cited by 544 · see citing works
Difference in prevalence of congenital cryptorchidism in infants between two Nordic countries
Boisen, K. A., Kaleva, M. M., Main, K. M., Virtanen, H. E., Haavisto, A.-M., Schmidt, I., Chellakooty, M., Damgaard, I., Kai, C. M., Reunanen, M. S., et al. (2004) · The Lancet · doi:10.1016/s0140-6736(04)15998-9 · Cited by 510 · see citing works
Self-citationAnderson, S. E., Dallal, G. E., & Must, A. (2003) · PEDIATRICS · doi:10.1542/peds.111.4.844 · Cited by 485 · see citing works
Kaplowitz, P. B., & Oberfield, S. E. (1999) · PEDIATRICS · doi:10.1542/peds.104.4.936 · Cited by 475 · see citing works
BMI in Childhood and Its Association with Height Gain, Timing of Puberty, and Final Height
He, Q., & KARLBERG, J. P. E. (2001) · Pediatric Research · doi:10.1203/00006450-200102000-00019 · Cited by 450 · see citing works
Testicular volume during adolescence. Cross-sectional and longitudinal studies.
ZACHMANN, M., Prader, A., Kind, H. P., Häfliger, H., & Budliger, H. (1974) · PubMed · Cited by 444 · see citing works
Wu, T., Mendola, P., & Buck, G. M. (2002) · Pediatrics · doi:10.1542/peds.110.4.752 · Cited by 394 · see citing works
Freedman, D. S., Khan, L. K., Serdula, M. K., Dietz, W. H., Srinivasan, S. R., & Berenson, G. S. (2002) · PEDIATRICS · doi:10.1542/peds.110.4.e43 · Cited by 341 · see citing works
Pubertal development in The Netherlands 1965–1997
Mul, D., Fredriks, A. M., van Buuren, S., Oostdijk, W., Verloove-Vanhorick, S. P., & Wit, J. M. (2001) · Pediatric Research · doi:10.1203/00006450-200110000-00010 · Cited by 313 · see citing works
Normal ages of pubertal events among American males and females
Lee, P. A. (1980) · Journal of Adolescent Health Care · doi:10.1016/s0197-0070(80)80005-2 · Cited by 228 · see citing works
Pubertal development in Swiss girls.
Largo, R. H., & Prader, A. (1983) · PubMed · Cited by 194 · see citing works
INDIVIDUAL DIFFERENCES IN PHYSICAL CHANGES ASSOCIATED WITH ADOLESCENCE IN GIRLS
Reynolds, E. L. (1948) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.1948.02030020341006 · Cited by 194 · see citing works
Pubertal development in Swiss boys.
Rh, L., & Prader, A. (1983) · PubMed · Cited by 192 · see citing works
Foster, T., Voors, A. W., Webber, L., Frerichs, R. R., & Berenson, G. (1977) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/30.4.582 · Cited by 169 · see citing works
INDICES OF PHYSIOLOGICAL MATURITY: DERIVATION AND INTERRELATIONSHIPS1
Nicolson, A. B., & Hanley, C. (1953) · Child Development · doi:10.1111/j.1467-8624.1953.tb04713.x · Cited by 161 · see citing works
Adaptive Two Stage Designs and the Conditional Error Function
Posch, M., & Bauer, P. (1999) · Biometrical Journal · doi:10.1002/(sici)1521-4036(199910)41:6 · Cited by 153 · see citing works
Wattigney, W. A., Srinivasan, S. R., Chen, W., Greenlund, K. J., & Berenson, G. S. (1999) · PubMed · Cited by 150 · see citing works
Are Pubertal Changes in Girls Before Age 8 Benign?
Midyett, L. K., Moore, W. V., & Jacobson, J. D. (2003) · PEDIATRICS · doi:10.1542/peds.111.1.47 · Cited by 137 · see citing works
Self-Assessment of Pubertal Stage in Overweight Children
Bonat, S. H., Pathomvanich, A., Keil, M. F., Field, A. E., & Yanovski, J. A. (2002) · PEDIATRICS · doi:10.1542/peds.110.4.743 · Cited by 135 · see citing works
Chalumeau, M., Hadjiathanasiou†, C. G., Ng, S. M., Cassio, A., Mul, D., Cisternino, M., Partsch, C., Theodoridis, C., Didi, M., CACCIARI, E., et al. (2003) · The Journal of Pediatrics · doi:10.1067/s0022-3476(03)00328-7 · Cited by 126 · see citing works
Current Age of Onset of Puberty
Rosenfield, R. L., Bachrach, L. K., Chernausek, S. D., Gertner, J. M., Gottschalk, M. E., Hardin, D. S., Pescovitz, O. H., & Saenger, P. H. (2000) · PEDIATRICS · doi:10.1542/peds.106.3.622 · Cited by 125 · see citing works
Puberty begins with a characteristic subcutaneous body fat mass in each sex
Vizmanos-Lamotte, B., & Martí-Henneberg, C. (2000) · European Journal of Clinical Nutrition · doi:10.1038/sj.ejcn.1600920 · Cited by 122 · see citing works
Pubertal stages 1980 of Stockholm schoolchildren
Lindgren, G. (1996) · Acta Paediatrica · doi:10.1111/j.1651-2227.1996.tb13927.x · Cited by 82 · see citing works
Growth in Early Life and Its Relation to Pubertal Growth
Luo, Z. C., Cheung, Y. B., He, Q., Albertsson-Wikland, K. G., & KARLBERG, J. P. E. (2003) · Epidemiology · doi:10.1097/00001648-200301000-00016 · Cited by 72 · see citing works
Andersen, E. (1968) · PubMed · Cited by 56 · see citing works
[Increase in overweight and obesity amongst Copenhagen schoolchildren, 1947-2003].
Pearson, S., Olsen, L. W., Hansen, B., & Sørensen, T. I. A. (2005) · PubMed · Cited by 54 · see citing works
A halt in the secular trend towards earlier menarche in Denmark
Helm, P., & Grønlund, L. (1998) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1034/j.1600-0412.1998.770213.x · Cited by 45 · see citing works
ANDERSEN, H. J. (1968) · Acta Paediatrica · doi:10.1111/j.1651-2227.1968.tb05653.x · Cited by 45 · see citing works
Danubio, M. E., Simone, M. D., Vecchi, F., et al. (2004) · American Journal of Human Biology · doi:10.1002/ajhb.20028 · Cited by 44 · see citing works
Sexual maturation in East German Girls*
Engelhardt, L., Willers, B., & Pelz, L. (1995) · Acta Paediatrica · doi:10.1111/j.1651-2227.1995.tb13569.x · Cited by 37 · see citing works
Hertel, N. T., Stoltenberg, M., Juul, A., et al. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.76.4.8473407 · Cited by 37 · see citing works
Self-citation[Heights and weights in Danish school children in 1971-1972].
Andersen, E. O., Andersen, H., Hutchings, B., et al. (1974) · PubMed · Cited by 34 · see citing works
Simone, M. D., Danubio, M. E., Amicone, E., et al. (2004) · Annals of Human Biology · doi:10.1080/03014460410001705013 · Cited by 32 · see citing works
Decrease in Menarcheal Age From 1966 to 1983 in Denmark
Helm, P., & Helm, S. (1984) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016348409155552 · Cited by 29 · see citing works
A continuous decline in menarcheal age in Denmark
Olesen, A. W. (2000) · Annals of Human Biology · doi:10.1080/03014460050044856 · Cited by 29 · see citing works
Main, K. M., Jarden, M., Angelo, L. D., Dinesen, B., Hertel, N. T., Juul, A., Müller, J., & Skakkebæk, N. E. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.3.8077374 · Cited by 28 · see citing works
Self-citationHertel, N. T. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.76.4.924 · Cited by 23 · see citing works
Self-citationHertel, N. T., Scheike, T., Juul, A., et al. (1995) · PubMed · Cited by 14 · see citing works
Self-citationPapadimitriou, A. (2004) · PEDIATRICS · doi:10.1542/peds.113.1.177 · Cited by 10 · see citing works
[Measurement of testicular volume with Prader's orchiometer in 1,389 boys 5--15 1/2 years old].
‐Sørensen, K. B., Nielsen, J., Busch, P., Hamborg-Petersen, B., Hansen, E., Lb, L., Nielsen, K., Jp, P., Rossen, K., Sk, S., et al. (1979) · PubMed · Cited by 6 · see citing works
Herman-Giddens, M. E., Wang, L., & Koch, G. (2001) · Archives of Pediatrics & Adolescent Medicine · doi:10.1001/archpedi.155.9.1022 · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Boehm, U., Bouloux, P.-M., Dattani, M. T., de Roux, N., Dodé, C., Dunkel, L., Dwyer, A. A., Giacobini, P., Hardelin, J.-P., Juul, A., et al. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.112 · Cited by 874 · see citing works
Self-citationExamination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings
Euling, S. Y., Herman-Giddens, M. E., Lee, P. A., Selevan, S. G., Juul, A., SØrensen, T. I. A., Dunkel, L., Himes, J. H., Teilmann, G., & Swan, S. H. (2008) · PEDIATRICS · doi:10.1542/peds.2007-1813d · Cited by 662 · see citing works
Self-citationRecent decline in age at breast development: The Copenhagen Puberty Study
Aksglaede, L., Sørensen, K., Petersen, J. H., Skakkebæk, N. E., & Juul, A. (2009) · Pediatrics · doi:10.1542/peds.2008-2491 · Cited by 626 · see citing works
Self-citationPubertal development and regulation
Abreu, A. P., & Kaiser, U. B. (2016) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(15)00418-0 · Cited by 611 · see citing works
Childhood obesity and the timing of puberty
Ahmed, M. L., Ong, K. K., & Dunger, D. B. (2009) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2009.02.004 · Cited by 409 · see citing works
Recent changes in pubertal timing in healthy danish boys: associations with body mass index
Sørensen, K., Aksglaede, L., Petersen, J. H., & Juul, A. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-1478 · Cited by 393 · see citing works
Sørensen, K., Mouritsen, A., Aksglaede, L., Hagen, C. P., Mogensen, S. S., & Juul, A. (2012) · Hormone Research in Paediatrics · doi:10.1159/000336325 · Cited by 386 · see citing works
Self-citationValidity of self-assessment of pubertal maturation
Rasmussen, A. R., Wohlfahrt-Veje, C., Tefre de Renzy-Martin, K., Hagen, C. P., Tinggaard, J., Mouritsen, A., Mieritz, M. G., & Main, K. M. (2015) · Pediatrics · doi:10.1542/peds.2014-0793 · Cited by 264 · see citing works
Self-citationCourant, F., Aksglaede, L., Antignac, J.-P., Monteau, F., Sorensen, K., Andersson, A.-M., Skakkebaek, N. E., Juul, A., & Bizec, B. L. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-1140 · Cited by 172 · see citing works
Self-citationSafety and efficacy of pediatric growth hormone therapy: results from the full KIGS cohort
Maghnie, M., Ranke, M. B., Geffner, M. E., Vlachopapadopoulou, E., Ibáñez, L., Carlsson, M., Cutfield, W., Rooman, R., Gomez, R., Wajnrajch, M. P., et al. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac517 · Cited by 120 · see citing works
Age of menarche and time to pregnancy
Guldbrandsen, K., Hakonsen, L. B., Ernst, A., Toft, G., Lyngso, J., Olsen, J., & Ramlau-Hansen, C. H. (2014) · Human Reproduction · doi:10.1093/humrep/deu153 · Cited by 58 · see citing works
Mood seasonality: A cross-sectional study of subjects aged between 10 and 25 years
Tonetti, L., Barbato, G., Fabbri, M., Adan, A., & Natale, V. (2007) · Journal of Affective Disorders · doi:10.1016/j.jad.2006.06.008 · Cited by 52 · see citing works
Teilmann, G., Petersen, J. H., Gormsen, M., Damgaard, K., Skakkebæk, N. E., & Jensen, T. K. (2009) · Hormone Research in Paediatrics · doi:10.1159/000236085 · Cited by 44 · see citing works
Self-citationGunapalasingham, G., Frithioff-Bøjsøe, C., Lund, M. A. V., Hedley, P. L., Fonvig, C. E., Dahl, M., Pedersen, O., Christiansen, M., Hansen, T., Lausten-Thomsen, U., et al. (2019) · Scandinavian Journal of Clinical and Laboratory Investigation · doi:10.1080/00365513.2019.1581945 · Cited by 23 · see citing works
Physical Changes During Pubertal Transition
Robeva, R., & Kumanov, P. (2016) · Puberty · doi:10.1007/978-3-319-32122-6_4 · Cited by 5 · see citing works
- Authors
- JUUL, A., TEILMANN, G., SCHEIKE, T., HERTEL, N. T., HOLM, K., LAURSEN, E. M., MAIN, K. M., & SKAKKEBÆK, N. E.
- Affiliations
- University of Copenhagen (DK)
- Corresponding author
- JUUL, A.
- Venue
- International Journal of Andrology
- Publisher
- Wiley
- Published
- 2006-02
- Volume
- 29
- Issue
- 1
- Pages
- 247-255
- ISSN
- 0105-6263 (ISSN-L)
- 1365-2605
- OpenAlex
- W2005838348
- Cited by
- 300
- References
- 49
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 8 · 2023: 14 · 2022: 18 · 2021: 15 · 2020: 14 · 2019: 22 · 2018: 11 · 2017: 15 · 2016: 19 · 2015: 12 · 2014: 14 · 2013: 9 · 2012: 23
- FWCI
- 13.68
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- International Journal of Andrology (publishedVersion)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Human Health and Disease
- Health Sciences › Health Professions › General Health Professions › Adolescent Sexual and Reproductive Health
- Keywords
- pubertal timing, puberty onset, secular trends, breast development, menarche, body mass index, childhood obesity, Danish children, Tanner stages, testicular volume
- MeSH terms
- Adolescent, Adult, Body Height, Body Weight, Child, Denmark, Europe, Female, Humans, Male, Menarche, Puberty, Reference Standards, Retrospective Studies, Sexual Maturation, United States, Urban Population, Cohort Studies, Body Mass Index, White People
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review