Abstract
Childhood obesity is associated with compromised bone health. We studied bone characteristics and their determinants in obese young adults. The study included 68 subjects with early-onset severe obesity and 73 normal-weight controls. Data on physical activity (PA), diet and smoking were collected. Bone characteristics were measured using peripheral QCT. The obese and control subjects were similar in age (mean 19.6 ± 2.6 years) and height but BMIs differed (39.7 and 22.6 kg/m2). A clustering of unhealthy lifestyles was marked: Obese subjects reported less supervised PA in childhood, adolescence and currently (p < 0.03) and were more likely to smoke (p = 0.005), and had a lower healthy eating index (HEI) (p = 0.007) but similar alcohol consumption compared with controls. In obese women, all crude bone characteristics were higher than in controls; in men, the differences were smaller. Associations of lifestyle factors with bone characteristics were tested using partial correlations. Independently of BMI, supervised PA in adolescence and alcohol consumption were related positively to bone characteristics in both groups. HEI associated positively with bone characteristics only in controls, while smoking was a positive determinant of bone characteristics only in obese subjects. The multivariate model showed that the contribution of lifestyle factors to bone characteristics was minimal compared with BMI. Early-onset obesity is accompanied by poor dietary quality, sedentary lifestyle, and more frequent smoking, but the overall contribution of these lifestyle factors to bone strength is limited. Bone strength is more likely to be compromised in men and in unloaded bone sites in subjects with early-onset severe obesity. The impact of obesity-related endocrine changes on bone characteristics need to be evaluated in future studies.
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Dimitri P, Bishop N, Walsh JS, Eastell R (2012) Obesity is a risk factor for fracture in children but is protective against fracture in adults: a paradox. Bone 50:457–466
Berenson AB, Breitkopf CR, Newman JL, Rahman M (2009) Contribution of fat-free mass and fat mass to bone mineral density among reproductive-aged women of white, black, and Hispanic race/ethnicity. J Clin Densitom 12:200–206
Langsetmo L, Hitchcock CL, Kingwell EJ, Davison KS, Berger C, Forsmo S, Zhou W, Kreiger N, Prior JC, Canadian Multicentre Osteoporosis Study Research Group (2012) Physical activity, body mass index and bone mineral density-associations in a prospective population-based cohort of women and men: the Canadian Multicentre Osteoporosis Study (CaMos). Bone 50:401–408
Adams AL, Kessler JI, Deramerian K, Smith N, Black MH, Porter AH, Jacobsen SJ, Koebnick C (2013) Associations between childhood obesity and upper and lower extremity injuries. Inj Prev 19:191–197
Valerio G, Galle F, Mancusi C, Di Onofrio V, Guida P, Tramontano A, Ruotolo E, Liguori G (2012) Prevalence of overweight in children with bone fractures: a case control study. BMC Pediatr. doi:10.1186/1471-2431-12-166
Kessler J, Koebnick C, Smith N, Adams A (2013) Childhood obesity is associated with increased risk of most lower extremity fractures. Clin Orthop Relat Res 471:1199–1207
Petit MA, Beck TJ, Hughes JM, Lin HM, Bentley C, Lloyd T (2008) Proximal femur mechanical adaptation to weight gain in late adolescence: a six-year longitudinal study. J Bone Miner Res 23:180–188
Sayers A, Tobias JH (2010) Fat mass exerts a greater effect on cortical bone mass in girls than boys. J Clin Endocrinol Metab 95:699–706
Vandewalle S, Taes Y, Van Helvoirt M, Debode P, Herregods N, Ernst C, Roef G, Van Caenegem E, Roggen I, Verhelle F, Kaufman JM, De Schepper J (2013) Bone size and bone strength are increased in obese male adolescents. J Clin Endocrinol Metab 98:3019–3028
Schoenau E, Neu CM, Beck B, Manz F, Rauch F (2002) Bone mineral content per muscle cross-sectional area as an index of the functional muscle-bone unit. J Bone Miner Res 17:1095–1101
Janicka A, Wren TA, Sanchez MM, Dorey F, Kim PS, Mittelman SD, Gilsanz V (2007) Fat mass is not beneficial to bone in adolescents and young adults. J Clin Endocrinol Metab 92:143–147
Bouxsein ML (2005) Determinants of skeletal fragility. Best Pract Res Clin Rheumatol 19:897–911
Kontulainen S, Heinonen A, Kannus P, Pasanen M, Sievanen H, Vuori I (2004) Former exercisers of an 18-month intervention display residual aBMD benefits compared with control women 3.5 years post-intervention: a follow-up of a randomized controlled high-impact trial. Osteoporos Int 15:248–251
Sayers A, Mattocks C, Deere K, Ness A, Riddoch C, Tobias JH (2011) Habitual levels of vigorous, but not moderate or light, physical activity is positively related to cortical bone mass in adolescents. J Clin Endocrinol Metab 96:E793–E802
Deere K, Sayers A, Rittweger J, Tobias JH (2012) A cross-sectional study of the relationship between cortical bone and high-impact activity in young adult males and females. J Clin Endocrinol Metab 97:3734–3743
Goulding A (2007) Risk factors for fractures in normally active children and adolescents. Med Sport Sci 51:102–120
Ottevaere C, Huybrechts I, Benser J, De Bourdeaudhuij I, Cuenca-Garcia M, Dallongeville J, Zaccaria M, Gottrand F, Kersting M, Rey-Lopez JP, Manios Y, Molnar D, Moreno LA, Smpokos E, Widhalm K, De Henauw S, HELENA Study Group (2011) Clustering patterns of physical activity, sedentary and dietary behavior among European adolescents: The HELENA study. BMC Public Health. doi:10.1186/1471-2458-11-328
Sorva R, Lankinen S, Tolppanen EM, Perheentupa J (1990) Variation of growth in height and weight of children. II. After infancy. Acta Paediatr Scand 79:498–506
Viljakainen H, Ivaska KK, Paldanius P, Lipsanen-Nyman M, Saukkonen T, Pietilainen KH, Andersson S, Laitinen K, Makitie O (2014) Suppressed bone turnover in obesity: a link to energy metabolism? A case-control study. J Clin Endocrinol Metab 99:2155–2163
Guenther PM, Reedy J, Krebs-Smith SM, Reeve BB (2008) Evaluation of the healthy eating index-2005. J Am Diet Assoc 108:1854–1864
Nordic Council of Ministers (2014) Nordic Nutrition Recommendations 2012 - Integrating nutrition and physical activity. Nord 2014(002):002
Ranta S, Viljakainen H, Makipernaa A, Makitie O (2012) Peripheral quantitative computed tomography (pQCT) reveals alterations in the three-dimensional bone structure in children with haemophilia. Haemophilia 18:955–961
Viljakainen HT, Pekkinen M, Saarnio E, Karp H, Lamberg-Allardt C, Makitie O (2011) Dual effect of adipose tissue on bone health during growth. Bone 48:212–217
Ankarberg-Lindgren C, Norjavaara E (2004) Changes of diurnal rhythm and levels of total and free testosterone secretion from pre to late puberty in boys: testis size of 3 ml is a transition stage to puberty. Eur J Endocrinol 151:747–757
Kelly DM, Jones TH (2015) Testosterone and obesity. Obes Rev. doi:10.1111/obr.12282
Vicente-Rodríguez G, Ortega FB, Rey-López JP, España-Romero V, Blay VA, Blay G, Martín-Matillas M, Moreno LA, AVENA-Zaragoza group (2009) Extracurricular physical activity participation modifies the association between high TV watching and low bone mass. Bone 45:925–930
Leonard MB, Zemel BS, Wrotniak BH, Klieger SB, Shults J, Stallings VA, Stettler N (2014) Tibia and radius bone geometry and volumetric density in obese compared to non-obese adolescents. Bone 73C:69–76
Cohen A, Dempster DW, Recker RR, Lappe JM, Zhou H, Zwahlen A, Muller R, Zhao B, Guo X, Lang T, Saeed I, Liu XS, Guo XE, Cremers S, Rosen CJ, Stein EM, Nickolas TL, McMahon DJ, Young P, Shane E (2013) Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J Clin Endocrinol Metab 98:2562–2572
Gilsanz V, Chalfant J, Mo AO, Lee DC, Dorey FJ, Mittelman SD (2009) Reciprocal relations of subcutaneous and visceral fat to bone structure and strength. J Clin Endocrinol Metab 94:3387–3393
Ng AC, Melton LJ 3rd, Atkinson EJ, Achenbach SJ, Holets MF, Peterson JM, Khosla S, Drake MT (2013) Relationship of adiposity to bone volumetric density and microstructure in men and women across the adult lifespan. Bone 55:119–125
Rosen CJ, Bouxsein ML (2006) Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2:35–43
Prieto-Alhambra D, Premaor MO, Fina Aviles F, Hermosilla E, Martinez-Laguna D, Carbonell-Abella C, Nogues X, Compston JE, Diez-Perez A (2012) The association between fracture and obesity is site-dependent: a population-based study in postmenopausal women. J Bone Miner Res 27:294–300
Sogaard AJ, Holvik K, Omsland TK, Tell GS, Dahl C, Schei B, Falch JA, Eisman JA, Meyer HE (2014) Abdominal obesity increases the risk of hip fracture. A population-based study of 43 000 women and men aged 60-79 years followed for 8 years. Cohort of Norway. J Intern Med 277:306–317
Shultz SP, Anner J, Hills AP (2009) Paediatric obesity, physical activity and the musculoskeletal system. Obes Rev 10:576–582
Bel S, Michels N, De Vriendt T, Patterson E, Cuenca-Garcia M, Diethelm K, Gutin B, Grammatikaki E, Manios Y, Leclercq C, Ortega FB, Moreno LA, Gottrand F, Gonzalez-Gross M, Widhalm K, Kafatos A, Garaulet M, Molnar D, Kaufman JM, Gilbert CC, Hallstrom L, Sjostrom M, Marcos A, De Henauw S, Huybrechts I, HELENA Study Group (2013) Association between self-reported sleep duration and dietary quality in European adolescents. Br J Nutr 110:949–959
Polfus LM, Smith JA, Shimmin LC, Bielak LF, Morrison AC, Kardia SL, Peyser PA, Hixson JE (2013) Genome-wide association study of gene by smoking interactions in coronary artery calcification. PLoS One 8:e74642
Tanaka H, Tanabe N, Kawato T, Nakai K, Kariya T, Matsumoto S, Zhao N, Motohashi M, Maeno M (2013) Nicotine affects bone resorption and suppresses the expression of cathepsin K, MMP-9 and vacuolar-type H(+)-ATPase d2 and actin organization in osteoclasts. PLoS One 8:e59402
Tucker KL, Chen H, Hannan MT, Cupples LA, Wilson PW, Felson D, Kiel DP (2002) Bone mineral density and dietary patterns in older adults: the Framingham Osteoporosis Study. Am J Clin Nutr 76:245–252
Langsetmo L, Hanley DA, Prior JC, Barr SI, Anastassiades T, Towheed T, Goltzman D, Morin S, Poliquin S, Kreiger N, CaMos Research Group (2011) Dietary patterns and incident low-trauma fractures in postmenopausal women and men aged >/= 50 y: a population-based cohort study. Am J Clin Nutr 93:192–199
Bhupathiraju SN, Lichtenstein AH, Dawson-Hughes B, Hannan MT, Tucker KL (2013) Adherence to the 2006 American Heart Association Diet and Lifestyle Recommendations for cardiovascular disease risk reduction is associated with bone health in older Puerto Ricans. Am J Clin Nutr 98:1309–1316
Andersen S, Frederiksen KD, Hansen S, Brixen K, Gram J, Stoving RK (2014) Bone structure and estimated bone strength in obese patients evaluated by high-resolution peripheral quantitative computed tomography. Calcif Tissue Int 95:19–28
Acknowledgments
H. T. Viljakainen, H. Valta, M. Lipsanen-Nyman, and O. Mäkitie were involved in the recruitment and data collection. H. T. Viljakainen, E. Kajantie , and O. Mäkitie analyzed and interpreted the data. H. T. Viljakainen, H. Valta, and O. Mäkitie were responsible for the writing of the manuscript and the others critically revised the manuscript. All the authors have contributed to the study design and approved the final version of the submitted manuscript. The authors have no disclosures. Research nurses Nea Boman and Sirpa Nolvi are acknowledged for their valuable work in patient assessments. The study was supported by grants from the Academy of Finland, the Folkhälsan Research Foundation, the Finnish Pediatric Research Foundation, the Sigrid Juselius Foundation, and the Helsinki University Hospital Research Funds.
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The study was approved by the Research Ethics Committee of the Hospital District of Helsinki and Uusimaa which includes the observance of human and animal rights. Informed consent was obtained from all individual participants included in the study.
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Supplemental material. Between group differences (= control – obese) in the characteristics of A) radius, B) tibia in men and the characteristics of C) radius and D) tibia in women. Differences were tested with multivariate analysis with models including age, supervised PAss, alcohol consumption, smoking and waist circumference. On x-axis numbering for bone characteristics: 1; Distal Tot CSA [mm2], 2; Tot Den [mg/cm3], 3; Trab Den [mg/cm3], 4; Proximal/Diaphyseal Tot CSA [mm2], 5; Cort Den [mg/cm3] and 6; polar SSI [mm3]. Bars represent mean with 95 % CI (PPTX 138 kb)
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Viljakainen, H.T., Valta, H., Lipsanen-Nyman, M. et al. Bone Characteristics and Their Determinants in Adolescents and Young Adults with Early-Onset Severe Obesity. Calcif Tissue Int 97, 364–375 (2015). https://doi.org/10.1007/s00223-015-0031-4
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DOI: https://doi.org/10.1007/s00223-015-0031-4