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We aimed to determine this timing based on pubertal growth markers. Secondary aims were to estimate the differences in growth between cohorts and identify the role of overweight in onset timing.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Design<\/jats:title>\n<jats:p>This multicohort study includes data from three Finnish cohorts\u2014the Type 1 Diabetes Prediction and Prevention (DIPP, <jats:italic>N<\/jats:italic> = 2,825) Study, the Special Turku Coronary Risk Factor Intervention Project (STRIP, <jats:italic>N<\/jats:italic> = 711), and the Boy cohort (<jats:italic>N<\/jats:italic> = 66). Children were monitored for growth and Tanner staging (except in DIPP).<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Methods<\/jats:title>\n<jats:p>The growth data were analyzed using a Super-Imposition by Translation And Rotation growth curve model, and pubertal onset analyses were run using a time-to-pubertal onset model.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Results<\/jats:title>\n<jats:p>The time-to-pubertal onset model used age at peak height velocity (aPHV), peak height velocity (PHV), and overweight status as covariates, with interaction between aPHV and overweight status for girls, and succeeded in determining the onset timing. Cross-validation showed a good agreement (71.0% for girls, 77.0% for boys) between the observed and predicted onset timings. Children in STRIP were taller overall (girls: 1.7 [95% CI: 0.9, 2.5] cm, boys: 1.0 [0.3, 2.2] cm) and had higher PHV values (girls: 0.13 [0.02, 0.25] cm\/year, boys: 0.35 [0.21, 0.49] cm\/year) than those in DIPP. Boys in the Boy cohort were taller (2.3 [0.3, 4.2] cm) compared with DIPP. Overweight girls showed pubertal onset at 1.0 [0.7, 1.4] year earlier compared with other girls. In boys, there was no such difference.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec005\">\n<jats:title>Conclusions<\/jats:title>\n<jats:p>The novel modeling approach provides an opportunity to evaluate the Tanner breast\/genital stage\u2013based pubertal onset timing in cohort studies including longitudinal data on growth but lacking pubertal follow-up.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pone.0260137","type":"journal-article","created":{"date-parts":[[2021,11,18]],"date-time":"2021-11-18T18:42:04Z","timestamp":1637260924000},"page":"e0260137","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":10,"title":["Determining the timing of pubertal onset via a multicohort analysis of 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diabetes using height velocity and trajectories","volume":"104","author":"J Zhu","year":"2018","journal-title":"J Clin Endocrinol Metab"},{"key":"pone.0260137.ref020","doi-asserted-by":"crossref","first-page":"e171769","DOI":"10.1001\/jamapediatrics.2017.1769","article-title":"Association between linear growth and bone accrual in a diverse cohort of children and adolescents","volume":"171","author":"SE McCormack","year":"2017","journal-title":"JAMA Pediatr"},{"key":"pone.0260137.ref021","article-title":"Pubertal Growth, IGF-1, and Windows of Susceptibility: Puberty and Future Breast Cancer Risk","author":"FM Biro","year":"2020","journal-title":"J Adolesc Health"},{"key":"pone.0260137.ref022","unstructured":"Peltonen M, Harald K, M\u00e4nnist\u00f6 S, Saarikoski L, Peltom\u00e4ki P, Lund L, et al. Kansallinen FINRISKI 2007-terveystutkimus: tutkimuksen toteutus ja tulokset. 2008."},{"key":"pone.0260137.ref023","doi-asserted-by":"crossref","first-page":"1266","DOI":"10.3390\/ijerph14101266","article-title":"Association between obesity and puberty timing: a systematic review and meta-analysis","volume":"14","author":"W Li","year":"2017","journal-title":"Int J Environ Res Public Health"},{"key":"pone.0260137.ref024","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1093\/ije\/dyaa056","article-title":"Childhood overweight and obesity and timing of puberty in boys and girls: cohort and sibling-matched analyses","volume":"49","author":"N Brix","year":"2020","journal-title":"Int J Epidemiol"},{"key":"pone.0260137.ref025","doi-asserted-by":"crossref","first-page":"e1667","DOI":"10.1210\/clinem\/dgz222","article-title":"Obesity is associated with earlier pubertal onset in boys","volume":"105","author":"AS Busch","year":"2020","journal-title":"J Clin Endocrinol Metab"},{"key":"pone.0260137.ref026","doi-asserted-by":"crossref","first-page":"903","DOI":"10.1542\/peds.110.5.903","article-title":"Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls","volume":"110","author":"Y Wang","year":"2002","journal-title":"Pediatrics"},{"key":"pone.0260137.ref027","first-page":"139","article-title":"Body mass index and timing of pubertal initiation in boys","volume":"164","author":"JM Lee","year":"2010","journal-title":"Arch Pediatr Adolesc Med"},{"key":"pone.0260137.ref028","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1007\/s001250051616","article-title":"Feasibility of genetic and immunological prediction of type I diabetes in a population-based birth cohort","volume":"44","author":"A Kupila","year":"2001","journal-title":"Diabetologia"},{"key":"pone.0260137.ref029","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/S0140-6736(95)90580-4","article-title":"Prospective randomised trial in 1062 infants of diet low in saturated fat and cholesterol","volume":"345","author":"H Lapinleimu","year":"1995","journal-title":"Lancet"},{"key":"pone.0260137.ref030","doi-asserted-by":"crossref","first-page":"1386","DOI":"10.1161\/01.CIR.94.6.1386","article-title":"Prospective randomized trial of low-saturated-fat, low-cholesterol diet during the first 3 years of life: the STRIP baby project","volume":"94","author":"H Niinikoski","year":"1996","journal-title":"Circulation"},{"key":"pone.0260137.ref031","doi-asserted-by":"crossref","first-page":"2570","DOI":"10.1210\/jc.2015-3329","article-title":"Testicular growth during puberty in boys with and without a history of congenital cryptorchidism","volume":"101","author":"S Sadov","year":"2016","journal-title":"J Clin Endocrinol Metab"},{"key":"pone.0260137.ref032","doi-asserted-by":"crossref","DOI":"10.1201\/b18041","volume-title":"Modelling Survival Data in Medical Research","author":"D Collett","year":"2015","edition":"3"},{"key":"pone.0260137.ref033","unstructured":"R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria). URL https:\/\/www.R-project.org\/."},{"key":"pone.0260137.ref034","unstructured":"Cole T. sitar: Super Imposition by Translation And Rotation Growth Curve Analysis. Version 1.1.1, 2019. URL https:\/\/CRAN.R-project.org\/package=sitar."},{"key":"pone.0260137.ref035","unstructured":"Therneau TM. A Package for Survival Analysis in R. Version 2.44\u20131.1, 2019. 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