The relationship between Insulin-like Growth Factor 1, sex steroids and timing of the pubertal growth spurt
Summary Objective Progress through puberty involves a complex hormonal cascade, but the individual contributions of hormones, particularly IGF‐1, are unknown. We reanalysed Chard growth study data to explore the tempo of puberty based on changes in both height and hormone levels, using a novel metho...
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Published in | Clinical endocrinology (Oxford) Vol. 82; no. 6; pp. 862 - 869 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
Published |
England
Blackwell Publishing Ltd
01.06.2015
Wiley Subscription Services, Inc John Wiley and Sons Inc |
Subjects | |
Online Access | Get full text |
ISSN | 0300-0664 1365-2265 1365-2265 |
DOI | 10.1111/cen.12682 |
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Abstract | Summary
Objective
Progress through puberty involves a complex hormonal cascade, but the individual contributions of hormones, particularly IGF‐1, are unknown. We reanalysed Chard growth study data to explore the tempo of puberty based on changes in both height and hormone levels, using a novel method of growth curve analysis.
Design and Subjects
Schoolboys (n = 54) and girls (n = 70) from Chard, Somerset, England, recruited in 1981 at age 8/9 and followed to age 16.
Measurements
Every 6 months, height and Tanner stages (genitalia, breast, pubic hair) were recorded, and in a subsample (24 boys, 27 girls), blood samples were taken. Serum IGF‐1, testosterone (boys) and oestradiol (girls) were measured by radioimmunoassay. Individual growth curves for each outcome were analysed using variants of the super‐imposition by translation and rotation (SITAR) method, which estimates a mean curve and subject‐specific random effects corresponding to size, and age and magnitude of peak velocity.
Results
The SITAR models fitted the data well, explaining 99%, 65%, 86% and 47% of variance for height, IGF‐1, testosterone and oestradiol, respectively, and 69–88% for the Tanner stages. During puberty, the variables all increased steeply in value in individuals, the ages at peak velocity for the different variables being highly correlated, particularly for IGF‐1 vs height (r = 0·74 for girls, 0·92 for boys).
Conclusions
IGF‐1, like height, the sex steroids and Tanner stages, rises steeply in individuals during puberty, with the timings of the rises tightly synchronized within individuals. This suggests that IGF‐1 may play an important role in determining the timing of puberty. |
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AbstractList | Progress through puberty involves a complex hormonal cascade, but the individual contributions of hormones, particularly IGF-1, are unknown. We reanalysed Chard growth study data to explore the tempo of puberty based on changes in both height and hormone levels, using a novel method of growth curve analysis.OBJECTIVEProgress through puberty involves a complex hormonal cascade, but the individual contributions of hormones, particularly IGF-1, are unknown. We reanalysed Chard growth study data to explore the tempo of puberty based on changes in both height and hormone levels, using a novel method of growth curve analysis.Schoolboys (n = 54) and girls (n = 70) from Chard, Somerset, England, recruited in 1981 at age 8/9 and followed to age 16.DESIGN AND SUBJECTSSchoolboys (n = 54) and girls (n = 70) from Chard, Somerset, England, recruited in 1981 at age 8/9 and followed to age 16.Every 6 months, height and Tanner stages (genitalia, breast, pubic hair) were recorded, and in a subsample (24 boys, 27 girls), blood samples were taken. Serum IGF-1, testosterone (boys) and oestradiol (girls) were measured by radioimmunoassay. Individual growth curves for each outcome were analysed using variants of the super-imposition by translation and rotation (SITAR) method, which estimates a mean curve and subject-specific random effects corresponding to size, and age and magnitude of peak velocity.MEASUREMENTSEvery 6 months, height and Tanner stages (genitalia, breast, pubic hair) were recorded, and in a subsample (24 boys, 27 girls), blood samples were taken. Serum IGF-1, testosterone (boys) and oestradiol (girls) were measured by radioimmunoassay. Individual growth curves for each outcome were analysed using variants of the super-imposition by translation and rotation (SITAR) method, which estimates a mean curve and subject-specific random effects corresponding to size, and age and magnitude of peak velocity.The SITAR models fitted the data well, explaining 99%, 65%, 86% and 47% of variance for height, IGF-1, testosterone and oestradiol, respectively, and 69-88% for the Tanner stages. During puberty, the variables all increased steeply in value in individuals, the ages at peak velocity for the different variables being highly correlated, particularly for IGF-1 vs height (r = 0·74 for girls, 0·92 for boys).RESULTSThe SITAR models fitted the data well, explaining 99%, 65%, 86% and 47% of variance for height, IGF-1, testosterone and oestradiol, respectively, and 69-88% for the Tanner stages. During puberty, the variables all increased steeply in value in individuals, the ages at peak velocity for the different variables being highly correlated, particularly for IGF-1 vs height (r = 0·74 for girls, 0·92 for boys).IGF-1, like height, the sex steroids and Tanner stages, rises steeply in individuals during puberty, with the timings of the rises tightly synchronized within individuals. This suggests that IGF-1 may play an important role in determining the timing of puberty.CONCLUSIONSIGF-1, like height, the sex steroids and Tanner stages, rises steeply in individuals during puberty, with the timings of the rises tightly synchronized within individuals. This suggests that IGF-1 may play an important role in determining the timing of puberty. Progress through puberty involves a complex hormonal cascade, but the individual contributions of hormones, particularly IGF-1, are unknown. We reanalysed Chard growth study data to explore the tempo of puberty based on changes in both height and hormone levels, using a novel method of growth curve analysis. Schoolboys (n = 54) and girls (n = 70) from Chard, Somerset, England, recruited in 1981 at age 8/9 and followed to age 16. Every 6 months, height and Tanner stages (genitalia, breast, pubic hair) were recorded, and in a subsample (24 boys, 27 girls), blood samples were taken. Serum IGF-1, testosterone (boys) and oestradiol (girls) were measured by radioimmunoassay. Individual growth curves for each outcome were analysed using variants of the super-imposition by translation and rotation (SITAR) method, which estimates a mean curve and subject-specific random effects corresponding to size, and age and magnitude of peak velocity. The SITAR models fitted the data well, explaining 99%, 65%, 86% and 47% of variance for height, IGF-1, testosterone and oestradiol, respectively, and 69-88% for the Tanner stages. During puberty, the variables all increased steeply in value in individuals, the ages at peak velocity for the different variables being highly correlated, particularly for IGF-1 vs height (r = 0·74 for girls, 0·92 for boys). IGF-1, like height, the sex steroids and Tanner stages, rises steeply in individuals during puberty, with the timings of the rises tightly synchronized within individuals. This suggests that IGF-1 may play an important role in determining the timing of puberty. Summary Objective Progress through puberty involves a complex hormonal cascade, but the individual contributions of hormones, particularly IGF‐1, are unknown. We reanalysed Chard growth study data to explore the tempo of puberty based on changes in both height and hormone levels, using a novel method of growth curve analysis. Design and Subjects Schoolboys (n = 54) and girls (n = 70) from Chard, Somerset, England, recruited in 1981 at age 8/9 and followed to age 16. Measurements Every 6 months, height and Tanner stages (genitalia, breast, pubic hair) were recorded, and in a subsample (24 boys, 27 girls), blood samples were taken. Serum IGF‐1, testosterone (boys) and oestradiol (girls) were measured by radioimmunoassay. Individual growth curves for each outcome were analysed using variants of the super‐imposition by translation and rotation (SITAR) method, which estimates a mean curve and subject‐specific random effects corresponding to size, and age and magnitude of peak velocity. Results The SITAR models fitted the data well, explaining 99%, 65%, 86% and 47% of variance for height, IGF‐1, testosterone and oestradiol, respectively, and 69–88% for the Tanner stages. During puberty, the variables all increased steeply in value in individuals, the ages at peak velocity for the different variables being highly correlated, particularly for IGF‐1 vs height (r = 0·74 for girls, 0·92 for boys). Conclusions IGF‐1, like height, the sex steroids and Tanner stages, rises steeply in individuals during puberty, with the timings of the rises tightly synchronized within individuals. This suggests that IGF‐1 may play an important role in determining the timing of puberty. Summary Objective Progress through puberty involves a complex hormonal cascade, but the individual contributions of hormones, particularly IGF-1, are unknown. We reanalysed Chard growth study data to explore the tempo of puberty based on changes in both height and hormone levels, using a novel method of growth curve analysis. Design and Subjects Schoolboys (n = 54) and girls (n = 70) from Chard, Somerset, England, recruited in 1981 at age 8/9 and followed to age 16. Measurements Every 6 months, height and Tanner stages (genitalia, breast, pubic hair) were recorded, and in a subsample (24 boys, 27 girls), blood samples were taken. Serum IGF-1, testosterone (boys) and oestradiol (girls) were measured by radioimmunoassay. Individual growth curves for each outcome were analysed using variants of the super-imposition by translation and rotation (SITAR) method, which estimates a mean curve and subject-specific random effects corresponding to size, and age and magnitude of peak velocity. Results The SITAR models fitted the data well, explaining 99%, 65%, 86% and 47% of variance for height, IGF-1, testosterone and oestradiol, respectively, and 69-88% for the Tanner stages. During puberty, the variables all increased steeply in value in individuals, the ages at peak velocity for the different variables being highly correlated, particularly for IGF-1 vs height (r = 0·74 for girls, 0·92 for boys). Conclusions IGF-1, like height, the sex steroids and Tanner stages, rises steeply in individuals during puberty, with the timings of the rises tightly synchronized within individuals. This suggests that IGF-1 may play an important role in determining the timing of puberty. |
Author | Ahmed, M.L. Dunger, D.B. Preece, M.A. Hindmarsh, P. Cole, T.J. |
AuthorAffiliation | 1 Population Policy and Practice Programme UCL Institute of Child Health London UK 2 Department of Paediatrics Children's Hospital Oxford UK 5 Department of Paediatrics University of Cambridge School of Clinical Medicine Cambridge UK 4 Developmental Endocrinology Research Group UCL Institute of Child Health London UK 3 Genetics and Genomic Medicine Programme UCL Institute of Child Health London UK |
AuthorAffiliation_xml | – name: 2 Department of Paediatrics Children's Hospital Oxford UK – name: 5 Department of Paediatrics University of Cambridge School of Clinical Medicine Cambridge UK – name: 1 Population Policy and Practice Programme UCL Institute of Child Health London UK – name: 3 Genetics and Genomic Medicine Programme UCL Institute of Child Health London UK – name: 4 Developmental Endocrinology Research Group UCL Institute of Child Health London UK |
Author_xml | – sequence: 1 givenname: T.J. surname: Cole fullname: Cole, T.J. email: tim.cole@ucl.ac.uk organization: Population Policy and Practice Programme, UCL Institute of Child Health, London, UK – sequence: 2 givenname: M.L. surname: Ahmed fullname: Ahmed, M.L. organization: Department of Paediatrics, Children's Hospital, Oxford, UK – sequence: 3 givenname: M.A. surname: Preece fullname: Preece, M.A. organization: Genetics and Genomic Medicine Programme, UCL Institute of Child Health, London, UK – sequence: 4 givenname: P. surname: Hindmarsh fullname: Hindmarsh, P. organization: Developmental Endocrinology Research Group, UCL Institute of Child Health, London, UK – sequence: 5 givenname: D.B. surname: Dunger fullname: Dunger, D.B. organization: Department of Paediatrics, University of Cambridge School of Clinical Medicine, Cambridge, UK |
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(2012) Higher levels of IGF-I and adrenal androgens at age 8 years are associated with earlier age at menarche in girls. The Journal of Clinical Endocrinology and Metabolism, 97, E786-E790. Tanner, J.M., Whitehouse, R.H. & Takaishi, M. (1966) Standards from birth to maturity for height, weight, height velocity, and weight velocity: British children, 1965 Parts I and II. Archives of Disease in Childhood, 41:454-471, 613-635. Hiney, J.K., Ojeda, S.R. & Dees, W.L. (1991) Insulin-like growth factor-I - a possible metabolic signal involved in the regulation of female puberty. Neuroendocrinology, 54, 420-423. Daftary, S.S. & Gore, A.C. (2005) IGF-1 in the brain as a regulator of reproductive neuroendocrine function. Experimental Biology and Medicine, 230, 292-306. Adair, L.S. (2001) Size at birth predicts age at menarche. Pediatrics, 107, E59. Marshall, W.A. & Tanner, J.M. (1970) Variations in pattern of pubertal changes in boys. Archives of Disease in Childhood, 45, 13-23. 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References_xml | – reference: Thankamony, A., Ong, K.K., Ahmed, M.L. et al. (2012) Higher levels of IGF-I and adrenal androgens at age 8 years are associated with earlier age at menarche in girls. The Journal of Clinical Endocrinology and Metabolism, 97, E786-E790. – reference: Johnson, L., van Jaarsveld, C.H.M., Llewellyn, C.H. et al. (2014) Associations between infant feeding and the size, tempo and velocity of infant weight gain: SITAR analysis of the Gemini twin birth cohort. International Journal of Obesity, 38, 980-987. – reference: Stanhope, R., Brook, C.G.D., Pringle, P.J. et al. (1987) Induction of puberty by pulsatile gonadotropin releasing hormone. Lancet, 2, 552-555. – reference: Cole, T.J., Donaldson, M.D. & Ben-Shlomo, Y. (2010) SITAR - a useful instrument for growth curve analysis. International Journal of Epidemiology, 39, 1558-1566. – reference: Ledford, A.W. & Cole, T.J. (1998) Mathematical models of growth in stature throughout childhood. Annals of Human Biology, 25, 101-115. – reference: Hiney, J.K., Srivastava, V.K., Pine, M.D. et al. (2009) Insulin-like Growth Factor-I activates KiSS-1 gene expression in the brain of the prepubertal female rat. Endocrinology, 150, 376-384. – reference: Ong, K.K., Emmett, P., Northstone, K. et al. (2009) Infancy weight gain predicts childhood body fat and age at menarche in girls. The Journal of Clinical Endocrinology and Metabolism, 94, 1527-1532. – reference: Adair, L.S. (2001) Size at birth predicts age at menarche. Pediatrics, 107, E59. – reference: Marshall, W.A. & Tanner, J.M. (1969) Variations in pattern of pubertal changes in girls. Archives of Disease in Childhood, 44, 291-303. – reference: Prentice, A., Dibba, B., Sawo, Y. et al. (2012) The effect of prepubertal calcium carbonate supplementation on the age of peak height velocity in Gambian adolescents. American Journal of Clinical Nutrition, 96, 1042-1050. – reference: Ong, K., Kratzsch, J., Kiess, W. et al. (2002) Circulating IGF-I levels in childhood are related to both current body composition and early postnatal growth rate. The Journal of Clinical Endocrinology and Metabolism, 87, 1041-1044. – reference: Wathen, N.C., Perry, L.A., Rubenstein, E. et al. (1987) A relationship between sex hormone binding globulin and dehydroepiandrosterone sulfate in normally menstruating females. Gynecological Endocrinology, 1, 47-50. – reference: Wolfe, A., Divall, S. & Wu, S. (2014) The regulation of reproductive neuroendocrine function by insulin and insulin-like growth factor-1 (IGF-1). Frontiers in Neuroendocrinology, 35, 558-572. – reference: Pizzi, C., Cole, T.J., Corvalan, C. et al. (2014) On modelling early life weight trajectories. Journal of the Royal Statistical Society: Series A (Statistics in Society), 177, 371-396. – reference: Sorensen, K., Aksglaede, L., Petersen, J.H. et al. (2012) Serum IGF1 and insulin levels in girls with normal and precocious puberty. European Journal of Endocrinology, 166, 903-910. – reference: Suter, K.J., Pohl, C.R. & Wilson, M.E. (2000) Circulating concentrations of nocturnal leptin, growth hormone, and insulin-like growth factor-I increase before the onset of puberty in agonadal male monkeys: potential signals for the initiation of puberty. The Journal of Clinical Endocrinology and Metabolism, 85, 808-814. – reference: Johnson, L., Llewellyn, C.H., van Jaarsveld, C.H.M. et al. (2011) Genetic and environmental influences on infant growth: prospective analysis of the Gemini twin birth cohort. PLoS One, 6, e19918. – reference: Zhao, J., Xiong, D.-H., Guo, Y. et al. (2007) Polymorphism in the insulin-like growth factor 1 gene is associated with age at menarche in caucasian females. Human Reproduction, 22, 1789-1794. – reference: Sandhu, J., Davey Smith, G., Holly, J. et al. (2006) Timing of puberty determines serum insulin-like growth factor-1 in late adulthood. The Journal of Clinical Endocrinology and Metabolism, 91, 3150-3157. – reference: Mauras, N., Rogol, A.D., Haymond, M.W. et al. (1996) Sex steroids, growth hormone, insulin-like growth factor-1: neuroendocrine and metabolic regulation in puberty. Hormone Research, 45, 74-80. – reference: Marshall, W.A. & Tanner, J.M. (1970) Variations in pattern of pubertal changes in boys. Archives of Disease in Childhood, 45, 13-23. – reference: Preece, M.A. & Baines, M.J. (1978) A new family of mathematical models describing the human growth curve. Annals of Human Biology, 5, 1-24. – reference: Cole, T.J., Statnikov, Y., Santhakumaran, S. et al. (2014) Birth weight and longitudinal growth in infants born below 32 weeks' gestation: a UK population study. Archives of Disease in Childhood. Fetal and Neonatal Edition, 99, F34-F40. – reference: Löfqvist, C., Andersson, E., Gelander, L. et al. (2001) Reference values for IGF-I throughout childhood and adolescence: a model that accounts simultaneously for the effect of gender, age, and puberty. Journal of Clinical Endocrinology and Metabolism, 86, 5870-5876. – reference: Daftary, S.S. & Gore, A.C. (2005) IGF-1 in the brain as a regulator of reproductive neuroendocrine function. Experimental Biology and Medicine, 230, 292-306. – reference: Cole, T.J., Pan, H. & Butler, G.E. (2014) A mixed effects model to estimate timing and intensity of pubertal growth from height and secondary sexual characteristics. Annals of Human Biology, 41, 76-83. – reference: Morrell, D.J., Dadi, H., More, J. et al. (1989) A monoclonal antibody to human insulin-like growth factor-I - characterization, use in radioimmunoassay and effect on the biological activities of the growth factor. Journal of Molecular Endocrinology, 2, 201-206. – reference: R Core Team (2014) R: A Language and Environment for Statistical Computing. 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Fetal and Neonatal Edition – volume: 166 start-page: 903 year: 2012 end-page: 910 article-title: Serum IGF1 and insulin levels in girls with normal and precocious puberty publication-title: European Journal of Endocrinology – volume: 44 start-page: 291 year: 1969 end-page: 303 article-title: Variations in pattern of pubertal changes in girls publication-title: Archives of Disease in Childhood – volume: 2 start-page: 552 year: 1987 end-page: 555 article-title: Induction of puberty by pulsatile gonadotropin releasing hormone publication-title: Lancet – volume: 150 start-page: 376 year: 2009 end-page: 384 article-title: Insulin‐like Growth Factor‐I activates KiSS‐1 gene expression in the brain of the prepubertal female rat publication-title: Endocrinology – volume: 163C start-page: 76 year: 2013 end-page: 85 article-title: Endocrine control of growth publication-title: American Journal of Medical Genetics. Part C – volume: 230 start-page: 292 year: 2005 end-page: 306 article-title: IGF‐1 in the brain as a regulator of reproductive neuroendocrine function publication-title: Experimental Biology and Medicine – volume: 177 start-page: 371 year: 2014 end-page: 396 article-title: On modelling early life weight trajectories publication-title: Journal of the Royal Statistical Society: Series A (Statistics in Society) – volume: 107 start-page: E59 year: 2001 article-title: Size at birth predicts age at menarche publication-title: Pediatrics – volume: 87 start-page: 1041 year: 2002 end-page: 1044 article-title: Circulating IGF‐I levels in childhood are related to both current body composition and early postnatal growth rate publication-title: The Journal of Clinical Endocrinology and Metabolism – volume: 85 start-page: 808 year: 2000 end-page: 814 article-title: Circulating concentrations of nocturnal leptin, growth hormone, and insulin‐like growth factor‐I increase before the onset of puberty in agonadal male monkeys: potential signals for the initiation of puberty publication-title: The Journal of Clinical Endocrinology and Metabolism – volume: 94 start-page: 1527 year: 2009 end-page: 1532 article-title: Infancy weight gain predicts childhood body fat and age at menarche in girls publication-title: The Journal of Clinical Endocrinology and Metabolism – volume: 41 start-page: 76 year: 2014 end-page: 83 article-title: A mixed effects model to estimate timing and intensity of pubertal growth from height and secondary sexual characteristics publication-title: Annals of Human Biology – volume: 31 start-page: 51 year: 1989 article-title: A longitudinal study of serum insulin‐like growth factor I growth and pubertal development 1981–1988 publication-title: Hormone Research – volume: 45 start-page: 13 year: 1970 end-page: 23 article-title: Variations in pattern of pubertal changes in boys publication-title: Archives of Disease in Childhood – ident: e_1_2_8_4_1 doi: 10.1016/j.yfrne.2014.05.007 – ident: e_1_2_8_26_1 doi: 10.1080/03014469800005482 – ident: e_1_2_8_31_1 doi: 10.1210/en.2008-0954 – ident: e_1_2_8_15_1 doi: 10.1136/bmj.d1980 – ident: e_1_2_8_27_1 doi: 10.1136/adc.41.220.613 – ident: e_1_2_8_14_1 doi: 10.3109/03014460.2013.856472 – ident: e_1_2_8_28_1 doi: 10.1016/S0140-6736(87)92932-1 – ident: e_1_2_8_16_1 doi: 10.3945/ajcn.112.037481 – volume: 87 start-page: 1041 year: 2002 ident: e_1_2_8_36_1 article-title: Circulating IGF‐I levels in childhood are related to both current body composition and early postnatal growth rate publication-title: The Journal of Clinical Endocrinology and Metabolism doi: 10.1210/jcem.87.3.8342 – ident: e_1_2_8_10_1 doi: 10.1136/adc.45.239.13 – ident: e_1_2_8_7_1 doi: 10.1210/jc.2011-3261 – ident: e_1_2_8_3_1 doi: 10.1002/ajmg.c.31357 – ident: e_1_2_8_25_1 doi: 10.1080/03014467800002601 – ident: e_1_2_8_18_1 doi: 10.1371/journal.pone.0019918 – ident: e_1_2_8_34_1 doi: 10.1542/peds.107.4.e59 – ident: e_1_2_8_2_1 doi: 10.1210/jc.85.2.808 – volume-title: R: A Language and Environment for Statistical Computing year: 2014 ident: e_1_2_8_24_1 – ident: e_1_2_8_21_1 doi: 10.1371/journal.pone.0090291 – ident: e_1_2_8_30_1 doi: 10.1159/000125924 – ident: e_1_2_8_37_1 doi: 10.1177/153537020523000503 – ident: e_1_2_8_8_1 doi: 10.1210/jcem.86.12.8117 – ident: e_1_2_8_11_1 doi: 10.1677/jme.0.0020201 – ident: e_1_2_8_17_1 doi: 10.1136/archdischild-2014-306237.81 – ident: e_1_2_8_20_1 doi: 10.1111/rssa.12020 – ident: e_1_2_8_6_1 doi: 10.1530/EJE-12-0106 – ident: e_1_2_8_33_1 doi: 10.1093/humrep/dem052 – ident: e_1_2_8_35_1 doi: 10.1210/jc.2008-2489 – ident: e_1_2_8_9_1 doi: 10.1136/adc.44.235.291 – volume: 31 start-page: 51 year: 1989 ident: e_1_2_8_5_1 article-title: A longitudinal study of serum insulin‐like growth factor I growth and pubertal development 1981–1988 publication-title: Hormone Research – ident: e_1_2_8_19_1 doi: 10.1038/ijo.2014.61 – ident: e_1_2_8_23_1 – ident: e_1_2_8_32_1 doi: 10.1210/jc.2005-2318 – start-page: 7 volume-title: The Cambridge Encyclopedia of Human Growth and Development year: 1998 ident: e_1_2_8_22_1 – ident: e_1_2_8_12_1 doi: 10.3109/09513598709082695 – ident: e_1_2_8_29_1 doi: 10.1159/000184763 – ident: e_1_2_8_13_1 doi: 10.1093/ije/dyq115 |
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Snippet | Summary
Objective
Progress through puberty involves a complex hormonal cascade, but the individual contributions of hormones, particularly IGF‐1, are unknown.... Progress through puberty involves a complex hormonal cascade, but the individual contributions of hormones, particularly IGF-1, are unknown. We reanalysed... Summary Objective Progress through puberty involves a complex hormonal cascade, but the individual contributions of hormones, particularly IGF-1, are unknown.... |
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StartPage | 862 |
SubjectTerms | Adolescent Adolescent Development - physiology Body Height - physiology Child England Estradiol - blood Female Humans Insulin-Like Growth Factor I - metabolism Longitudinal Studies Male Original Puberty - physiology Sexual Maturation - physiology Testosterone - blood |
Title | The relationship between Insulin-like Growth Factor 1, sex steroids and timing of the pubertal growth spurt |
URI | https://api.istex.fr/ark:/67375/WNG-5SVHFZQ6-X/fulltext.pdf https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fcen.12682 https://www.ncbi.nlm.nih.gov/pubmed/25418044 https://www.proquest.com/docview/1681517777 https://www.proquest.com/docview/1682423544 https://pubmed.ncbi.nlm.nih.gov/PMC4949545 |
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