The Functional Muscle-Bone Unit in Obese Children – Altered Bone Structure Leads to Normal Strength Strain Index

Abstract

Obese children have a twofold increased risk of fracture of the forearm compared to non-obese children.

Objective: To investigate bone strength and bone structure of the forearm, and the relationship between muscle and bone in obese children.

Methods: The study-group consisted of 84 (40 female) overweight children (mean (SD)) age 11.8 (3.2) years, BMI 29.0 (5.1) kg/m²). Bone geometry and strength were measured at the proximal radius of the non-dominant forearm (65% measurement site) by means of pQCT (XCT 2000). Bone mineral density and lean mass of the total body was determined by means of DXA (Lunar, DPXL/PED). Results were compared to reference values by calculating age (SDS_CA) and height-age (SDS_HA) dependent standard deviation scores (SDS).

Results: Cortical density, −1.11 (1.74) SDS_HA, −0.45 (1.52) SDS_CA; cortical thickness, −1.46 (1.33) SDS_HA, −1.01 (1.46) SDS_CA; cortical area, −0.42 (1.31) SDS_HA, 0.26 (1.58) SDS_CA; total bone area +2.21 (1.47) SDS_HA, 2.91 (1.80) SDS_CA, marrow area +3.12 (2.29) SDS_HA, 3.37 (2.38) SDS_CA; strength strain index +0.10 (1.10) SDS_HA, 0.95 (1.57) SDS_CA. These changes in bone structure were independent from pubertal stage. Measurements revealed correlations between muscle area and SSI (R²=0.67, p<0.001), and muscle mass and bone mineral content (DXA; R²=0.81, p<0.001).

Conclusion: Low cortical density, normal cortical area and increased total bone area led to a normal strength strain index adjusted both for height and for age. We assume that this normal bone strength is not appropriate for the higher kinetic energy of impact in case of a fall in overweight children.

obesity - children - functional muscle-bone unit - DXA - pQCT

References

• 1 Aksglaede L, Juul A, Olsen LW. et al . Age at Puberty and the Emerging Obesity Epidemic.  PLoS ONE. 2009;  4 e8450
• 2 Bös K, Opper E, Woll A. Fitness in der Grundschule.  Haltung und Bewegung. 2002;  22 5-25
• 3 Cole TJ, Freeman JV, Preece MA. Body mass index reference curves for the UK, 1990.  Arch Dis Child. 1995;  73 25-29
• 4 Davidson PL, Goulding A, Chalmers DJ. Biomechanical analysis of arm fracture in obese boys.  J Paed Child Health. 2003;  39 657-664
• 5 De Schepper J, Van den Broeck M, Jonckheer MH. Study of lumbar spine bone mineral density in obese children.  Acta Paediatr. 1995;  84 313-315
• 6 Fischer S, Milinarsky A, Giadrosich V. et al . X-ray absorptiometry of bone in obese and eutrophic children from Valparaiso, Chile.  J Rheumatol. 2000;  27 1294-1296
• 7 Frost HM, Schönau E. The “muscle-bone unit” in children and adolescents: a 2000 overview.  J Pediatr Endocrinol Metab. 2000;  13 571-590
• 8 Frost HM. Changing concepts in skeletal physiology: Wolff's law, the mechanostat, and the “Utah paradigm”.  Am J Hum Biol. 1998;  10 599-505
• 9 Hasanoglu A, Bideci A, Cinaz P. et al . Bone mineral density in childhood obesity.  J Pediatr Endocrinol Metab. 2000;  3 307-311
• 10 Hasegawa Y, Schneider P, Reiners C. et al . Estimation of the architectural properties of cortical bone using peripheral quantitative computed tomography.  Osteoporos Int. 2000;  11 36-42
• 11 Johnson J, Dawson-Hughes B. Precision and stability of dual-energy X-ray absorptiometry measurements.  Calcif Tissue Int. 1991;  49 174-178
• 12 Klein KO, Larmore KA, de Lancey E. et al . Effect of obesity on estradiol level, and its relationship to leptin, bone maturation, and bone mineral density in children.  J Clin Endocrinol Metab. 1998;  83 3469-3475
• 13 Kurth BM, Schaffrath R. Die Verbreitung von Übergewicht und Adipositas bei Kindern und Jugendlichen.  Bundesgesundheitsbl – Gesundheitsforschung – Gesundheitsschutz. 2007;  50 736-743
• 14 Leonard MB, Shults J, Wilson BA. et al . Obesity during childhood and adolescence augments bone mass and bone dimensions.  Amer J Clin Nutr. 2004;  80 514-523
• 15 McCormick DP, Ponder SW, Fawcett HD. et al . Spinal bone mineral density in 335 normal and obese children and adolescents: evidence for ethnic and sex differences.  J Bone Miner Res. 1991;  6 507-513
• 16 Morano M, Colella D, Robazza C. et al . Physical self-perception and motor performance in normal-weight, overweight and obese children.  Scand J Med Sci Sports. 2010 Jan 31; 
• 17 Pintauro SJ, Nagy TR, Duthie CM. et al . Cross-calibration of fat and lean measurements by dual-energy X-ray absorptiometry to pig carcass analysis in the pediatric body weight range.  Am J Clin Nutr. 1996;  63 293-298
• 18 Popkin BM, Gordon-Larsen P. The nutrition transition: worldwide obesity dynamics and their determinants.  Int J Oes Relat Metab Disord. 2004;  28 (S 03) 2-9
• 19 Prader A, Largo RH, Molinari L. et al . Physical growth of Swiss children from birth to 20 years of age. First Zurich longitudinal study of growth and development.  Helv Paediatr Acta Suppl. 1989;  52 1-125
• 20 Rauch F, Neu CM, Wassmer G. et al . Muscle analysis by measurement of maximal isometric grip force: new reference data and clinical applications in pediatrics.  Pediatr Res. 2002;  51 (4) 505-510
• 21 Sayers A, Tobias JH. Fat mass exerts a greater effect on cortical bone mass in girls than boys.  J Clin Endocrinol Metab. 2010;  95 699-706
• 22 Schönau E, Neu CM, Beck B. et al . Bone mineral content per muscle cross-sectional area as an index of the functional muscle-bone unit.  J Bone Miner Res. 2002;  17 1095-1101
• 23 Schönau E. Problems of bone analysis in childhood and adolescence.  Pediatr Nephrol. 1998;  12 420-429
• 24 Schönau E, Neu CM, Rauch F. et al . The development of bone strength at the proximal radius during childhood and adolescence.  J Clin Endocrinol Metab. 2001;  86 613-618
• 25 Schweizer R, Martin DD, Haase M. et al . Similar effects of long-term exogenous growth hormone (GH) on bone and muscle parameters: a pQCT study of GH-deficient and small-for-gestational-age (SGA) children.  Bone. 2007;  41 875-881
• 26 Schweizer R, Martin DD, Schwarze CP. et al . Cortical bone density is normal in prepubertal children with growth hormone (GH) deficiency, but initially decreases during GH replacement due to early bone remodeling.  J Clin Endocrinol Metab. 2003;  88 5266-5272
• 27 Tanner JM. Normal growth and techniques of growth assessment.  Clin Endocrinol Metab. 1986;  15 411-451
• 28 Troiano RP, Briefel RR, Carroll MD. et al . Energy and fat intakes of children and adolescents in the United States: data from the national health and nutrition examination surveys.  Am J Clin Nutr. 2000;  72 1343-1353
• 29 Van der Sluis I, de Ridder MA, Boot AM. et al . Reference data for bone density and body composition measured with dual energy X ray absorptiometry in white children and young adults.  Arch Dis Child. 2002;  87 341-347
• 30 Wetzsteon RJ, Petit MA, Macdonald HM. et al . Bone structure and volumetric BMD in overweight children: a longitudinal study.  J Bone Mineral Res. 2008;  23 1946-1953
• 31 Wosje KS, Knipstein BL, Kalkwarf HJ. Measurement error of DXA: Interpretation of fat and lean mass changes in obese and non-obese children.  J Clin Densitom. 2006;  9 (3) 335-340
• 32 Wey HE, Binkley TL, Beare TM. et al . Cross-sectional versus longitudinal associations of lean and fat mass with pQCT bone outcomes in children.  J Clin Endocrinol Metab. 2011;  96 106-114

APPENDIX

DISKUS-Study Group

Perikles Simon, Gutenberg University, Sports Medicine, Mainz, Germany;

Andre Lacroix, Jochen Hansel, Andreas Nieß, University Hospital for Internal Medicine, Sports Medicine, Tuebingen, Germany; Katrin Giel, Markus Schrauth †, Paul Enck, Stephan Zipfel, University Hospital for Internal Medicine, Department of Psychosomatic Medicine and Psychotherapy, Tuebingen, Germany; Jürgen Machmann, Fabian Springer, Verena Ballweg, Fritz Schick, Eberhard-Karls-University, Section on Experimental Radiology, Department of Diagnostic Radiology, Tuebingen, Germany; Michael S. Urschitz, Department of Neonatology, University Children's Hospital, Tuebingen, Germany; Andreas Neu, Hans Peter Haber, Department of Paediatrics, University Children's Hospital, Tuebingen, Germany; Huu Phuc Nguyen, Eberhard-Karls-University, Department of Medical Genetics, Tuebingen, Germany.

Correspondence