{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,20]],"date-time":"2026-03-20T20:21:03Z","timestamp":1774038063676,"version":"3.50.1"},"reference-count":37,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2018,7,3]],"date-time":"2018-07-03T00:00:00Z","timestamp":1530576000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Portuguese Foundation for Science and Technology","award":["uid\/dtp\/04213\/2016"],"award-info":[{"award-number":["uid\/dtp\/04213\/2016"]}]},{"name":"Portuguese Foundation for Science and Technology","award":["SFRH\/BPD\/100470\/2014"],"award-info":[{"award-number":["SFRH\/BPD\/100470\/2014"]}]},{"name":"Portuguese Foundation for Science and Technology","award":["SFRH\/BD\/101083\/2014"],"award-info":[{"award-number":["SFRH\/BD\/101083\/2014"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Pediatr"],"published-print":{"date-parts":[[2018,12]]},"DOI":"10.1186\/s12887-018-1182-z","type":"journal-article","created":{"date-parts":[[2018,7,3]],"date-time":"2018-07-03T12:07:27Z","timestamp":1530619647000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Total and regional bone mineral and tissue composition in female adolescent athletes: comparison between volleyball players and swimmers"],"prefix":"10.1186","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0980-0269","authenticated-orcid":false,"given":"Jo\u00e3o","family":"Valente-dos-Santos","sequence":"first","affiliation":[]},{"given":"\u00d3scar M.","family":"Tavares","sequence":"additional","affiliation":[]},{"given":"Jo\u00e3o P.","family":"Duarte","sequence":"additional","affiliation":[]},{"given":"Paulo M.","family":"Sousa-e-Silva","sequence":"additional","affiliation":[]},{"given":"Lu\u00eds M.","family":"Rama","sequence":"additional","affiliation":[]},{"given":"Jos\u00e9 M.","family":"Casanova","sequence":"additional","affiliation":[]},{"given":"Carlos A.","family":"Fontes-Ribeiro","sequence":"additional","affiliation":[]},{"given":"Elisa A.","family":"Marques","sequence":"additional","affiliation":[]},{"given":"Daniel","family":"Courteix","sequence":"additional","affiliation":[]},{"given":"Enio R. V.","family":"Ronque","sequence":"additional","affiliation":[]},{"given":"Edilson S.","family":"Cyrino","sequence":"additional","affiliation":[]},{"given":"Jorge","family":"Conde","sequence":"additional","affiliation":[]},{"given":"Manuel J.","family":"Coelho-e-Silva","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2018,7,3]]},"reference":[{"issue":"12","key":"1182_CR1","doi-asserted-by":"publisher","first-page":"1726","DOI":"10.1007\/s00198-006-0172-4","volume":"17","author":"O Johnell","year":"2006","unstructured":"Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int. 2006;17(12):1726\u201333.","journal-title":"Osteoporos Int"},{"issue":"2","key":"1182_CR2","doi-asserted-by":"publisher","first-page":"294","DOI":"10.1016\/j.bone.2009.10.005","volume":"46","author":"R Rizzoli","year":"2010","unstructured":"Rizzoli R, Bianchi ML, Garabedian M, McKay HA, Moreno LA. Maximizing bone mineral mass gain during growth for the prevention of fractures in the adolescents and the elderly. Bone. 2010;46(2):294\u2013305.","journal-title":"Bone"},{"key":"1182_CR3","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1159\/000103005","volume":"51","author":"JP Bonjour","year":"2007","unstructured":"Bonjour JP, Chevalley T, Rizzoli R, Ferrari S. Gene-environment interactions in the skeletal response to nutrition and exercise during growth. Med Sport Sci. 2007;51:64\u201380.","journal-title":"Med Sport Sci"},{"issue":"2","key":"1182_CR4","doi-asserted-by":"publisher","first-page":"467","DOI":"10.1002\/jbmr.2036","volume":"29","author":"M Behringer","year":"2014","unstructured":"Behringer M, Gruetzner S, McCourt M, Mester J. Effects of weight-bearing activities on bone mineral content and density in children and adolescents: a meta-analysis. J Bone Miner Res. 2014;29(2):467\u201378.","journal-title":"J Bone Miner Res"},{"issue":"3","key":"1182_CR5","first-page":"283","volume":"13","author":"IJ Wallace","year":"2013","unstructured":"Wallace IJ, Kwaczala AT, Judex S, Demes B, Carlson KJ. Physical activity engendering loads from diverse directions augments the growing skeleton. J Musculoskelet Neuronal Interact. 2013;13(3):283\u20138.","journal-title":"J Musculoskelet Neuronal Interact"},{"issue":"1","key":"1182_CR6","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1016\/j.bone.2004.10.001","volume":"36","author":"F Ginty","year":"2005","unstructured":"Ginty F, Rennie KL, Mills L, Stear S, Jones S, Prentice A. Positive, site-specific associations between bone mineral status, fitness, and time spent at high-impact activities in 16- to 18-year-old boys. Bone. 2005;36(1):101\u201310.","journal-title":"Bone"},{"issue":"11","key":"1182_CR7","doi-asserted-by":"publisher","first-page":"877","DOI":"10.1136\/bjsports-2011-090188","volume":"45","author":"CA Boreham","year":"2011","unstructured":"Boreham CA, McKay HA. Physical activity in childhood and bone health. Br J Sports Med. 2011;45(11):877\u20139.","journal-title":"Br J Sports Med"},{"issue":"12","key":"1182_CR8","doi-asserted-by":"publisher","first-page":"1879","DOI":"10.1111\/j.1651-2227.2010.01905.x","volume":"99","author":"R Gruodyte","year":"2010","unstructured":"Gruodyte R, Jurimae J, Cicchella A, Stefanelli C, Passariello C, Jurimae T. Adipocytokines and bone mineral density in adolescent female athletes. Acta Paediatr. 2010;99(12):1879\u201384.","journal-title":"Acta Paediatr"},{"issue":"3","key":"1182_CR9","doi-asserted-by":"publisher","first-page":"371","DOI":"10.1016\/j.bone.2007.05.003","volume":"41","author":"JF Nichols","year":"2007","unstructured":"Nichols JF, Rauh MJ, Barrack MT, Barkai HS. Bone mineral density in female high school athletes: interactions of menstrual function and type of mechanical loading. Bone. 2007;41(3):371\u20137.","journal-title":"Bone"},{"issue":"8","key":"1182_CR10","doi-asserted-by":"publisher","first-page":"457","DOI":"10.1038\/nrendo.2012.49","volume":"8","author":"BK Pedersen","year":"2012","unstructured":"Pedersen BK, Febbraio MA. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol. 2012;8(8):457\u201365.","journal-title":"Nat Rev Endocrinol"},{"issue":"6","key":"1182_CR11","doi-asserted-by":"publisher","first-page":"328","DOI":"10.1249\/JSR.0b013e3182779193","volume":"11","author":"KL Scofield","year":"2012","unstructured":"Scofield KL, Hecht S. Bone health in endurance athletes: runners, cyclists, and swimmers. Current Sports Med Rep. 2012;11(6):328\u201334.","journal-title":"Current Sports Med Rep"},{"issue":"9","key":"1182_CR12","doi-asserted-by":"publisher","first-page":"861","DOI":"10.1016\/j.pmrj.2011.05.019","volume":"3","author":"AS Tenforde","year":"2011","unstructured":"Tenforde AS, Fredericson M. Influence of sports participation on bone health in the young athlete: a review of the literature. PMR. 2011;3(9):861\u20137.","journal-title":"PMR"},{"key":"1182_CR13","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1016\/j.bone.2015.05.023","volume":"80","author":"R Sartori","year":"2015","unstructured":"Sartori R, Sandri M. BMPs and the muscle-bone connection. Bone. 2015;80:37\u201342.","journal-title":"Bone"},{"issue":"10","key":"1182_CR14","doi-asserted-by":"publisher","first-page":"4576","DOI":"10.1210\/jcem.86.10.7960","volume":"86","author":"E Seeman","year":"2001","unstructured":"Seeman E. Clinical review 137: Sexual dimorphism in skeletal size, density, and strength. J Clin Endocrinol Metab. 2001;86(10):4576\u201384.","journal-title":"J Clin Endocrinol Metab"},{"issue":"6","key":"1182_CR15","doi-asserted-by":"publisher","first-page":"1033","DOI":"10.1359\/jbmr.081255","volume":"24","author":"S Kirmani","year":"2009","unstructured":"Kirmani S, Christen D, van Lenthe GH, Fischer PR, Bouxsein ML, McCready LK, et al. Bone structure at the distal radius during adolescent growth. J Bone Miner Res. 2009;24(6):1033\u201342.","journal-title":"J Bone Miner Res"},{"issue":"12","key":"1182_CR16","doi-asserted-by":"publisher","first-page":"2267","DOI":"10.1359\/jbmr.2001.16.12.2267","volume":"16","author":"Y Duan","year":"2001","unstructured":"Duan Y, Turner CH, Kim BT, Seeman E. Sexual dimorphism in vertebral fragility is more the result of gender differences in age-related bone gain than bone loss. J Bone Miner Res. 2001;16(12):2267\u201375.","journal-title":"J Bone Miner Res"},{"issue":"4","key":"1182_CR17","doi-asserted-by":"publisher","first-page":"1277","DOI":"10.1007\/s00198-011-1677-z","volume":"23","author":"LA Burt","year":"2012","unstructured":"Burt LA, Naughton GA, Greene DA, Courteix D, Ducher G. Non-elite gymnastics participation is associated with greater bone strength, muscle size, and function in pre- and early pubertal girls. Osteoporos Int. 2012;23(4):1277\u201386.","journal-title":"Osteoporos Int"},{"issue":"1","key":"1182_CR18","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/j.jbspin.2012.01.006","volume":"80","author":"B Ferry","year":"2013","unstructured":"Ferry B, Lespessailles E, Rochcongar P, Duclos M, Courteix D. Bone health during late adolescence: effects of an 8-month training program on bone geometry in female athletes. Joint Bone Spine. 2013;80(1):57\u201363.","journal-title":"Joint Bone Spine"},{"issue":"2","key":"1182_CR19","doi-asserted-by":"publisher","first-page":"276","DOI":"10.1016\/j.jada.2006.11.008","volume":"107","author":"C Lopes","year":"2007","unstructured":"Lopes C, Aro A, Azevedo A, Ramos E, Barros H. Intake and adipose tissue composition of fatty acids and risk of myocardial infarction in a male Portuguese community sample. J Am Diet Assoc. 2007;107(2):276\u201386.","journal-title":"J Am Diet Assoc"},{"issue":"6","key":"1182_CR20","doi-asserted-by":"publisher","first-page":"e0180357","DOI":"10.1371\/journal.pone.0180357","volume":"12","author":"RR Agostinete","year":"2017","unstructured":"Agostinete RR, Duarte JP, Valente-dos-Santos J, Coelho-e-Silva MJ, Tavares OM, Conde JM, et al. Bone tissue, blood lipids and inflammatory profiles in adolescent male athletes from sports contrasting in mechanical load. PLoS One. 2017;12(6):e0180357.","journal-title":"PLoS One"},{"issue":"6","key":"1182_CR21","doi-asserted-by":"publisher","first-page":"1101","DOI":"10.1016\/j.bone.2008.07.245","volume":"43","author":"AD Baxter-Jones","year":"2008","unstructured":"Baxter-Jones AD, Kontulainen SA, Faulkner RA, Bailey DA. A longitudinal study of the relationship of physical activity to bone mineral accrual from adolescence to young adulthood. Bone. 2008;43(6):1101\u20137.","journal-title":"Bone"},{"key":"1182_CR22","volume-title":"Anthropometric standardization reference manual","author":"T Lohman","year":"1988","unstructured":"Lohman T, Roche AF, Martorell R. Anthropometric standardization reference manual. Human Kinetics: Champaign; 1988."},{"key":"1182_CR23","first-page":"1","volume":"11","author":"RJ Kuczmarski","year":"2002","unstructured":"Kuczmarski RJ, Ogden CL, Guo SS, Grummer-Strawn LM, Flegal KM, Mei Z, et al. 2000 CDC growth charts for the United States: methods and development. Vital Health Stat. 2002;11:1\u2013186.","journal-title":"Vital Health Stat"},{"key":"1182_CR24","first-page":"1","volume":"63","author":"KM Flegal","year":"2013","unstructured":"Flegal KM, Cole TJ. Construction of LMS parameters for the Centers for Disease Control and Prevention 2000 growth charts. Natl Health Stat Rep. 2013;63:1\u20133.","journal-title":"Natl Health Stat Rep"},{"key":"1182_CR25","doi-asserted-by":"crossref","DOI":"10.5040\/9781492596837","volume-title":"Growth, maturation, and physical activity","author":"RM Malina","year":"2004","unstructured":"Malina RM, Bouchard C, Bar-Or O. Growth, maturation, and physical activity. Human Kinetics: Champaign; 2004."},{"issue":"1","key":"1182_CR26","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1249\/MSS.0b013e31818cb278","volume":"41","author":"WG Hopkins","year":"2009","unstructured":"Hopkins WG, Marshall SW, Batterham AM, Hanin J. Progressive statistics for studies in sports medicine and exercise science. Med Sci Sports Exerc. 2009;41(1):3\u201313.","journal-title":"Med Sci Sports Exerc"},{"key":"1182_CR27","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1037\/1082-989X.1.4.331","volume":"1","author":"RL Rosnow","year":"1996","unstructured":"Rosnow RL, Rassithal R. Computing contrast, effect sizes and conternulls on other people is published data: General procedures for research consumer. Psychol Methods. 1996;1:331\u201340.","journal-title":"Psychol Methods"},{"issue":"1","key":"1182_CR28","doi-asserted-by":"publisher","first-page":"208","DOI":"10.1016\/j.bone.2009.10.017","volume":"46","author":"AD Baxter-Jones","year":"2010","unstructured":"Baxter-Jones AD, Burrows M, Bachrach LK, Lloyd T, Petit M, Macdonald H, et al. International longitudinal pediatric reference standards for bone mineral content. Bone. 2010;46(1):208\u201316.","journal-title":"Bone"},{"issue":"6","key":"1182_CR29","doi-asserted-by":"publisher","first-page":"589","DOI":"10.1111\/sms.12378","volume":"25","author":"A Gomez-Bruton","year":"2015","unstructured":"Gomez-Bruton A, Gonzalez-Aguero A, Gomez-Cabello A, Matute-Llorente A, Casajus JA, Vicente-Rodriguez G. The effects of swimming training on bone tissue in adolescence. Scand J Med Sci Sports. 2015;25(6):589\u2013602.","journal-title":"Scand J Med Sci Sports"},{"issue":"5","key":"1182_CR30","doi-asserted-by":"publisher","first-page":"622","DOI":"10.1080\/03014460310001592650","volume":"30","author":"C Padez","year":"2003","unstructured":"Padez C, Rocha MA. Age at menarche in Coimbra (Portugal) school girls: a note on the secular changes. Ann Hum Biol. 2003;30(5):622\u201332.","journal-title":"Ann Hum Biol"},{"issue":"13","key":"1182_CR31","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1136\/bjsports-2015-094623","volume":"49","author":"RM Malina","year":"2015","unstructured":"Malina RM, Rogol AD, Cumming SP, Coelho e Silva MJ, Figueiredo AJ. Biological maturation of youth athletes: assessment and implications. Br J Sports Med. 2015;49(13):852\u20139.","journal-title":"Br J Sports Med"},{"issue":"5","key":"1182_CR32","doi-asserted-by":"publisher","first-page":"e97846","DOI":"10.1371\/journal.pone.0097846","volume":"9","author":"DA Santos","year":"2014","unstructured":"Santos DA, Dawson JA, Matias CN, Rocha PM, Minderico CS, Allison DB, et al. Reference values for body composition and anthropometric measurements in athletes. PLoS One. 2014;9(5):e97846.","journal-title":"PLoS One"},{"issue":"6","key":"1182_CR33","doi-asserted-by":"publisher","first-page":"1494","DOI":"10.1177\/0363546515572142","volume":"43","author":"AS Tenforde","year":"2015","unstructured":"Tenforde AS, Fredericson M, Sayres LC, Cutti P, Sainani KL. Identifying sex-specific risk factors for low bone mineral density in adolescent runners. Am J Sports Med. 2015;43(6):1494\u2013504.","journal-title":"Am J Sports Med"},{"key":"1182_CR34","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1007\/978-3-642-02400-9_2","volume-title":"Radionuclide and Hybrid Bone Imaging","author":"U Kini","year":"2012","unstructured":"Kini U, Nandeesh BN. Physiology of Bone Formation, Remodeling, and Metabolism. In: Fogelman I, Gnanasegaran G, van der Wall H, editors. Radionuclide and Hybrid Bone Imaging. Berlin: Springer; 2012. p. 29\u201357."},{"issue":"3","key":"1182_CR35","doi-asserted-by":"publisher","first-page":"205","DOI":"10.1016\/8756-3282(95)00171-9","volume":"17","author":"PC Fehling","year":"1995","unstructured":"Fehling PC, Alekel L, Clasey J, Rector A, Stillman RJ. A comparison of bone mineral densities among female athletes in impact loading and active loading sports. Bone. 1995;17(3):205\u201310.","journal-title":"Bone"},{"issue":"1","key":"1182_CR36","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0169-6009(08)80086-4","volume":"23","author":"A Heinonen","year":"1993","unstructured":"Heinonen A, Oja P, Kannus P, Sievanen H, Manttari A, Vuori I. Bone mineral density of female athletes in different sports. Bone Miner. 1993;23(1):1\u201314.","journal-title":"Bone Miner"},{"issue":"9","key":"1182_CR37","doi-asserted-by":"publisher","first-page":"1480","DOI":"10.1359\/jbmr.1997.12.9.1480","volume":"12","author":"Y Umemura","year":"1997","unstructured":"Umemura Y, Ishiko T, Yamauchi T, Kurono M, Mashiko S. Five jumps per day increase bone mass and breaking force in rats. J Bone Miner Res. 1997;12(9):1480\u20135.","journal-title":"J Bone Miner Res"}],"container-title":["BMC Pediatrics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12887-018-1182-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12887-018-1182-z\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12887-018-1182-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,11,5]],"date-time":"2020-11-05T00:28:18Z","timestamp":1604536098000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcpediatr.biomedcentral.com\/articles\/10.1186\/s12887-018-1182-z"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,7,3]]},"references-count":37,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2018,12]]}},"alternative-id":["1182"],"URL":"https:\/\/doi.org\/10.1186\/s12887-018-1182-z","relation":{},"ISSN":["1471-2431"],"issn-type":[{"value":"1471-2431","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,7,3]]},"assertion":[{"value":"24 November 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 June 2018","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 July 2018","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The study was approved by the Ethics Committee of the Faculty of Sport Sciences and Physical Education of the University of Coimbra (CE\/FCDEF-UC\/00102014) and was conducted in accordance with the Declaration of Helsinki for human studies of the World Medical Association. Parents or legal guardians and each participant signed an informed consent document.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interest.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Publisher\u2019s Note"}}],"article-number":"212"}}