{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,10]],"date-time":"2026-03-10T22:35:43Z","timestamp":1773182143740,"version":"3.50.1"},"reference-count":44,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2017,10,30]],"date-time":"2017-10-30T00:00:00Z","timestamp":1509321600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/100000072","name":"National Institute of Dental and Craniofacial Research","doi-asserted-by":"publisher","award":["R01\u2010DE09551"],"award-info":[{"award-number":["R01\u2010DE09551"]}],"id":[{"id":"10.13039\/100000072","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000072","name":"National Institute of Dental and Craniofacial Research","doi-asserted-by":"publisher","award":["R01\u2010DE12101"],"award-info":[{"award-number":["R01\u2010DE12101"]}],"id":[{"id":"10.13039\/100000072","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2018,4,1]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n               <jats:sec>\n                  <jats:title>\u2003<\/jats:title>\n                  <jats:p>This study evaluated the longitudinal relationships among visceral adipose tissue (VAT), subcutaneous adipose tissue (SAT), and peripheral bone strength during adolescence. Fat and lean mass, VAT and SAT area, and android\/gynoid (A\/G) ratio were estimated with DXA. Our main outcome was strength-strain index (SSI), an indicator of peripheral bone strength estimated by pQCT at the radius and tibia. Sex-specific analyses evaluated the longitudinal bone-fat relationship from ages 11 to 19 years with linear mixed models using biological age as the time variable and adjusted for limb length and lean mass in 182 girls and 167 boys. Variables were standardized (mean\u2009=\u20090, SD\u2009=\u20091) prior to model fitting and results shown are parameter estimates\u2009\u00b1\u2009SE. Fat mass and SAT were positively associated with SSI (radius: 0.07\u2009\u00b1\u20090.02, p\u2009=\u20090.003 and 0.05\u2009\u00b1\u20090.02, 0.041, respectively; tibia: 0.09\u2009\u00b1\u20090.02, p\u2009&amp;lt;\u20090.001 and 0.08\u2009\u00b1\u20090.02, p\u2009&amp;lt;\u20090.001, respectively) prior to, but not following adjustment for lean mass in girls. In contrast, fat mass and SAT were negatively associated with radial SSI, both before and after adjustment for lean mass in boys (fat mass: \u20130.05\u2009\u00b1\u20090.01, p\u2009=\u20090.001; SAT: \u20130.04\u2009\u00b1\u20090.01, p\u2009=\u20090.004). In full models, negative associations were limited to VAT in girls and included radial (\u20130.06\u2009\u00b1\u20090.02, p\u2009=\u20090.001) and tibial SSI (\u20130.04\u2009\u00b1\u20090.02, p\u2009=\u20090.033). For boys, there were no significant associations present between VAT and SSI at the radius or tibia. In analyses limited to obese participants, an A\/G ratio was not significantly associated with SSI in girls, but was negatively associated with radial SSI regardless of adjustment for lean mass in boys (\u20130.06\u2009\u00b1\u20090.02, p\u2009=\u20090.018). These results that show a negative relationship between peripheral bone strength and VAT in girls, but greater total and central adiposity in boys, suggest these factors play a role in adequate acquisition of bone strength during adolescence. \u00a9 2017 American Society for Bone and Mineral Research.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1002\/jbmr.3325","type":"journal-article","created":{"date-parts":[[2017,10,30]],"date-time":"2017-10-30T11:06:46Z","timestamp":1509361606000},"page":"580-588","source":"Crossref","is-referenced-by-count":19,"title":["Does Visceral or Subcutaneous Fat Influence Peripheral Cortical Bone Strength During Adolescence? A Longitudinal Study"],"prefix":"10.1093","volume":"33","author":[{"given":"Natalie A","family":"Glass","sequence":"first","affiliation":[{"name":"Department of Orthopaedic SurgeryThe University of Iowa Hospitals & ClinicsIowa CityIAUSA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"James C","family":"Torner","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, College of Public HealthThe University of IowaIowa CityIAUSA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elena M","family":"Letuchy","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, College of Public HealthThe University of IowaIowa CityIAUSA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Trudy L","family":"Burns","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, College of Public HealthThe University of IowaIowa CityIAUSA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kathleen F","family":"Janz","sequence":"additional","affiliation":[{"name":"Department of Health and Human PhysiologyThe University of IowaIowa CityIAUSA"},{"name":"Department of Epidemiology, College of Public HealthThe University of IowaIowa CityIAUSA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julie M","family":"Eichenberger Gilmore","sequence":"additional","affiliation":[{"name":"Department of Preventive & Community DentistryThe University of Iowa College of Dentistry & Dental ClinicsIowa CityIAUSA"},{"name":"Department of Epidemiology, College of Public HealthThe University of IowaIowa CityIAUSA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Janet A","family":"Schlechte","sequence":"additional","affiliation":[{"name":"Department of Internal MedicineThe University of Iowa Hospitals & ClinicsIowa CityIAUSA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Steven M","family":"Levy","sequence":"additional","affiliation":[{"name":"Department of Preventive & Community DentistryThe University of Iowa College of Dentistry & Dental ClinicsIowa CityIAUSA"},{"name":"Department of Epidemiology, College of Public HealthThe University of IowaIowa CityIAUSA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2017,10,30]]},"reference":[{"issue":"7","key":"2024021014354055100_jbmr3325-bib-0001","doi-asserted-by":"crossref","first-page":"2325","DOI":"10.1210\/jc.2008-2501","article-title":"Fat mass is negatively associated with cortical bone size in young healthy male siblings","volume":"94","author":"Taes","year":"2009","journal-title":"J Clin Endocrinol Metab"},{"issue":"9","key":"2024021014354055100_jbmr3325-bib-0002","doi-asserted-by":"crossref","first-page":"3387","DOI":"10.1210\/jc.2008-2422","article-title":"Reciprocal relations of subcutaneous and visceral fat to bone structure and strength","volume":"94","author":"Gilsanz","year":"2009","journal-title":"J Clin Endocrinol Metab"},{"issue":"3","key":"2024021014354055100_jbmr3325-bib-0003","doi-asserted-by":"crossref","first-page":"1247","DOI":"10.1210\/jc.2009-1475","article-title":"Visceral fat is a negative predictor of bone density measures in obese adolescent girls","volume":"95","author":"Russell","year":"2010","journal-title":"J Clin Endocrinol Metab"},{"issue":"12","key":"2024021014354055100_jbmr3325-bib-0004","doi-asserted-by":"crossref","first-page":"2760","DOI":"10.1002\/jbmr.184","article-title":"Lower bone mass in prepubertal overweight children with prediabetes","volume":"25","author":"Pollock","year":"2010","journal-title":"J Bone Miner Res"},{"issue":"1","key":"2024021014354055100_jbmr3325-bib-0005","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1590\/S0004-27302012000100003","article-title":"Influence of visceral and subcutaneous fat in bone mineral density of obese adolescents","volume":"56","author":"Campos","year":"2012","journal-title":"Arq Bras Endocrinol Metabol"},{"key":"2024021014354055100_jbmr3325-bib-0006","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1186\/1471-2431-13-37","article-title":"The relationship between visceral fat thickness and bone mineral density in sedentary obese children and adolescents","volume":"13","author":"Junior","year":"2013","journal-title":"BMC Pediatr"},{"issue":"5)","key":"2024021014354055100_jbmr3325-bib-0007","first-page":"e42","article-title":"Adiposity in children and adolescents: correlates and clinical consequences of fat stored in specific body depots","volume":"7","author":"Katzmarzyk","year":"2012","journal-title":"Pediatr Obes"},{"issue":"2","key":"2024021014354055100_jbmr3325-bib-0008","first-page":"82","article-title":"The interrelationships between abdominal adiposity, leptin and bone mineral content in overweight Latino children","volume":"72","author":"Afghani","year":"2009","journal-title":"Horm Res"},{"issue":"4","key":"2024021014354055100_jbmr3325-bib-0009","doi-asserted-by":"crossref","first-page":"263","DOI":"10.1007\/s00198-003-1542-9","article-title":"Attainment of peak bone mass at the lumbar spine, femoral neck and radius in men and women: relative contributions of bone size and volumetric bone mineral density","volume":"15","author":"Henry","year":"2004","journal-title":"Osteoporos Int"},{"issue":"6","key":"2024021014354055100_jbmr3325-bib-0010","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1001\/jamapediatrics.2014.21","article-title":"Prevalence and trends in obesity and severe obesity among children in the United States, 1999-2012","volume":"168","author":"Skinner","year":"2014","journal-title":"JAMA Pediatr"},{"issue":"3","key":"2024021014354055100_jbmr3325-bib-0011","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1111\/j.1752-7325.1998.tb02998.x","article-title":"Patterns of dietary fluoride supplement use during infancy","volume":"58","author":"Levy","year":"1998","journal-title":"J Public Health Dent"},{"issue":"5","key":"2024021014354055100_jbmr3325-bib-0012","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1038\/oby.2011.367","article-title":"Dual-energy X-ray performs as well as clinical computed tomography for the measurement of visceral fat","volume":"20","author":"Micklesfield","year":"2012","journal-title":"Obesity (Silver Spring)"},{"issue":"3","key":"2024021014354055100_jbmr3325-bib-0013","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1111\/ijpo.249","article-title":"Visceral adipose tissue measured by DXA correlates with measurement by CT and is associated with cardiometabolic risk factors in children","volume":"10","author":"Bosch","year":"2015","journal-title":"Pediatr Obes"},{"issue":"7","key":"2024021014354055100_jbmr3325-bib-0014","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1002\/jbmr.2809","article-title":"The relationship between greater prepubertal adiposity, subsequent age of maturation, and bone strength during adolescence","volume":"31","author":"Glass","year":"2016","journal-title":"J Bone Miner Res"},{"issue":"4","key":"2024021014354055100_jbmr3325-bib-0015","first-page":"689","article-title":"An assessment of maturity from anthropometric measurements","volume":"34","author":"Mirwald","year":"2002","journal-title":"Med Sci Sports Exerc"},{"issue":"Suppl 4","key":"2024021014354055100_jbmr3325-bib-0016","doi-asserted-by":"crossref","first-page":"S164","DOI":"10.1542\/peds.2007-2329C","article-title":"Expert committee recommendations regarding the prevention, assessment, and treatment of child and adolescent overweight and obesity: summary report","volume":"120","author":"Barlow","year":"2007","journal-title":"Pediatrics"},{"key":"2024021014354055100_jbmr3325-bib-0017","doi-asserted-by":"crossref","first-page":"174","DOI":"10.1123\/pes.9.2.174","article-title":"Validation of the physical activity questionnaire for older children","volume":"9","author":"Kowalski","year":"1997","journal-title":"Pediatr Exerc Sci"},{"issue":"5","key":"2024021014354055100_jbmr3325-bib-0018","doi-asserted-by":"crossref","first-page":"1362","DOI":"10.2337\/diacare.26.5.1362","article-title":"Insulin resistance, inflammation, and serum fatty acid composition","volume":"26","author":"Fernandez-Real","year":"2003","journal-title":"Diabetes Care"},{"issue":"4","key":"2024021014354055100_jbmr3325-bib-0019","doi-asserted-by":"crossref","first-page":"1010","DOI":"10.2337\/db06-1656","article-title":"Visceral fat adipokine secretion is associated with systemic inflammation in obese humans","volume":"56","author":"Fontana","year":"2007","journal-title":"Diabetes"},{"issue":"3","key":"2024021014354055100_jbmr3325-bib-0020","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1210\/edrv.23.3.0465","article-title":"Sex steroids and the construction and conservation of the adult skeleton","volume":"23","author":"Riggs","year":"2002","journal-title":"Endocr Rev"},{"issue":"7","key":"2024021014354055100_jbmr3325-bib-0021","doi-asserted-by":"crossref","first-page":"495","DOI":"10.5483\/BMBRep.2008.41.7.495","article-title":"Osteoimmunology: cytokines and the skeletal system","volume":"41","author":"Lee","year":"2008","journal-title":"BMB Rep"},{"issue":"6","key":"2024021014354055100_jbmr3325-bib-0022","doi-asserted-by":"crossref","first-page":"913","DOI":"10.2337\/diabetes.47.6.913","article-title":"Leptin secretion from subcutaneous and visceral adipose tissue in women","volume":"47","author":"van Harmelen","year":"1998","journal-title":"Diabetes"},{"issue":"7","key":"2024021014354055100_jbmr3325-bib-0023","doi-asserted-by":"crossref","first-page":"2029","DOI":"10.2337\/diabetes.51.7.2029","article-title":"Increased lipolysis and decreased leptin production by human omental as compared with subcutaneous preadipocytes","volume":"51","author":"van Harmelen","year":"2002","journal-title":"Diabetes"},{"issue":"4","key":"2024021014354055100_jbmr3325-bib-0024","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1002\/jcb.10156","article-title":"Leptin stimulates human osteoblastic cell proliferation, de novo collagen synthesis, and mineralization: impact on differentiation markers, apoptosis, and osteoclastic signaling","volume":"85","author":"Gordeladze","year":"2002","journal-title":"J Cell Biochem"},{"issue":"4","key":"2024021014354055100_jbmr3325-bib-0025","doi-asserted-by":"crossref","first-page":"E567","DOI":"10.1152\/ajpendo.00315.2011","article-title":"Leptin in human physiology and pathophysiology","volume":"301","author":"Mantzoros","year":"2011","journal-title":"Am J Physiol Endocrinol Metab"},{"issue":"6941","key":"2024021014354055100_jbmr3325-bib-0026","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1038\/nature01705","article-title":"Cloning of adiponectin receptors that mediate antidiabetic metabolic effects","volume":"423","author":"Yamauchi","year":"2003","journal-title":"Nature"},{"issue":"7","key":"2024021014354055100_jbmr3325-bib-0027","doi-asserted-by":"crossref","first-page":"1784","DOI":"10.1172\/JCI29126","article-title":"Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome","volume":"116","author":"Kadowaki","year":"2006","journal-title":"J Clin Invest"},{"issue":"10","key":"2024021014354055100_jbmr3325-bib-0028","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1016\/S0026-0495(03)00195-1","article-title":"Hypoadiponectinemia is associated with visceral fat accumulation and insulin resistance in Japanese men with type 2 diabetes mellitus","volume":"52","author":"Yatagai","year":"2003","journal-title":"Metabolism"},{"issue":"5","key":"2024021014354055100_jbmr3325-bib-0029","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1038\/nm0506-511","article-title":"Overcoming insulin resistance with CNTF","volume":"12","author":"Ahima","year":"2006","journal-title":"Nat Med"},{"issue":"4","key":"2024021014354055100_jbmr3325-bib-0030","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1002\/jbmr.2083","article-title":"Insulin resistance and bone strength: findings from the study of midlife in the United States","volume":"29","author":"Srikanthan","year":"2014","journal-title":"J Bone Miner Res"},{"issue":"2","key":"2024021014354055100_jbmr3325-bib-0031","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.cell.2010.06.002","article-title":"Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition","volume":"142","author":"Fulzele","year":"2010","journal-title":"Cell"},{"issue":"2","key":"2024021014354055100_jbmr3325-bib-0032","doi-asserted-by":"crossref","first-page":"296","DOI":"10.1016\/j.cell.2010.06.003","article-title":"Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism","volume":"142","author":"Ferron","year":"2010","journal-title":"Cell"},{"issue":"6","key":"2024021014354055100_jbmr3325-bib-0033","doi-asserted-by":"crossref","first-page":"560","DOI":"10.1177\/0022034513485600","article-title":"Decreased jaw bone density and osteoblastic insulin signaling in a model of obesity","volume":"92","author":"Pramojanee","year":"2013","journal-title":"J Dent Res"},{"issue":"5","key":"2024021014354055100_jbmr3325-bib-0034","doi-asserted-by":"crossref","first-page":"633","DOI":"10.2337\/diab.45.5.633","article-title":"Abdominal fat and insulin resistance in normal and overweight women: direct measurements reveal a strong relationship in subjects at both low and high risk of NIDDM","volume":"45","author":"Carey","year":"1996","journal-title":"Diabetes"},{"issue":"9","key":"2024021014354055100_jbmr3325-bib-0035","doi-asserted-by":"crossref","first-page":"826","DOI":"10.1001\/archpediatrics.2009.148","article-title":"Effect of android to gynoid fat ratio on insulin resistance in obese youth","volume":"163","author":"Aucouturier","year":"2009","journal-title":"Arch Pediatr Adolesc Med"},{"issue":"9291","key":"2024021014354055100_jbmr3325-bib-0036","doi-asserted-by":"crossref","first-page":"1400","DOI":"10.1016\/S0140-6736(01)06525-4","article-title":"Presence of increased stiffness of the common carotid artery and endothelial dysfunction in severely obese children: a prospective study","volume":"358","author":"Tounian","year":"2001","journal-title":"Lancet"},{"issue":"12","key":"2024021014354055100_jbmr3325-bib-0037","doi-asserted-by":"crossref","first-page":"2948","DOI":"10.2337\/diacare.27.12.2948","article-title":"Visceral and central abdominal fat and anthropometry in relation to diabetes in Asian Indians","volume":"27","author":"Anjana","year":"2004","journal-title":"Diabetes Care"},{"issue":"11)","key":"2024021014354055100_jbmr3325-bib-0038","doi-asserted-by":"crossref","first-page":"e27694","DOI":"10.1371\/journal.pone.0027694","article-title":"Android fat depot is more closely associated with metabolic syndrome than abdominal visceral fat in elderly people","volume":"6","author":"Kang","year":"2011","journal-title":"PLoS One"},{"issue":"4","key":"2024021014354055100_jbmr3325-bib-0039","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1161\/01.CIR.99.4.541","article-title":"Association of body fat distribution and cardiovascular risk factors in children and adolescents","volume":"99","author":"Daniels","year":"1999","journal-title":"Circulation"},{"issue":"4","key":"2024021014354055100_jbmr3325-bib-0040","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1053\/meta.2001.21693","article-title":"Contributions of total body fat, abdominal subcutaneous adipose tissue compartments, and visceral adipose tissue to the metabolic complications of obesity","volume":"50","author":"Smith","year":"2001","journal-title":"Metabolism"},{"issue":"8","key":"2024021014354055100_jbmr3325-bib-0041","doi-asserted-by":"crossref","first-page":"1933","DOI":"10.1038\/oby.2007.231","article-title":"Deep subcutaneous adipose tissue: a distinct abdominal adipose depot","volume":"15","author":"Walker","year":"2007","journal-title":"Obesity (Silver Spring)"},{"issue":"12","key":"2024021014354055100_jbmr3325-bib-0042","doi-asserted-by":"crossref","first-page":"2562","DOI":"10.1002\/oby.20417","article-title":"Molecular and morphologic characterization of superficial- and deep-subcutaneous adipose tissue subdivisions in human obesity","volume":"21","author":"Cancello","year":"2013","journal-title":"Obesity (Silver Spring)"},{"issue":"5","key":"2024021014354055100_jbmr3325-bib-0043","doi-asserted-by":"crossref","first-page":"E941","DOI":"10.1152\/ajpendo.2000.278.5.E941","article-title":"Subdivisions of subcutaneous abdominal adipose tissue and insulin resistance","volume":"278","author":"Kelley","year":"2000","journal-title":"Am J Physiol Endocrinol Metab"},{"issue":"3","key":"2024021014354055100_jbmr3325-bib-0044","doi-asserted-by":"crossref","first-page":"821","DOI":"10.2337\/dc13-1353","article-title":"Structural and functional properties of deep abdominal subcutaneous adipose tissue explain its association with insulin resistance and cardiovascular risk in men","volume":"37","author":"Marinou","year":"2014","journal-title":"Diabetes Care"}],"container-title":["Journal of Bone and Mineral Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fjbmr.3325","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/academic.oup.com\/jbmr\/article-pdf\/33\/4\/580\/56652175\/jbmr3325.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jbmr\/article-pdf\/33\/4\/580\/56652175\/jbmr3325.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,13]],"date-time":"2024-03-13T15:00:28Z","timestamp":1710342028000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jbmr\/article\/33\/4\/580-588\/7605553"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,10,30]]},"references-count":44,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2017,10,30]]},"published-print":{"date-parts":[[2018,4,1]]}},"URL":"https:\/\/doi.org\/10.1002\/jbmr.3325","relation":{},"ISSN":["0884-0431","1523-4681"],"issn-type":[{"value":"0884-0431","type":"print"},{"value":"1523-4681","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2018,4,1]]},"published":{"date-parts":[[2017,10,30]]}}}