Calcified Tissue International

, Volume 101, Issue 5, pp 479–488 | Cite as

Obese Versus Normal-Weight Late-Adolescent Females have Inferior Trabecular Bone Microarchitecture: A Pilot Case-Control Study

  • Joseph M. Kindler
  • Norman K. Pollock
  • Hannah L. Ross
  • Christopher M. Modlesky
  • Harshvardhan Singh
  • Emma M. Laing
  • Richard D. Lewis
Original Research

Abstract

Though still a topic of debate, the position that skeletal health is compromised with obesity has received support in the pediatric and adult literature. The limited data relating specifically to trabecular bone microarchitecture, however, have been relatively inconsistent. The aim of this pilot cross-sectional case-control study was to compare trabecular bone microarchitecture between obese (OB) and normal-weight (NW) late-adolescent females. A secondary aim was to compare diaphyseal cortical bone outcomes between these two groups. Twenty-four non-Hispanic white females, ages 18–19 years, were recruited into OB (n = 12) or NW (n = 12) groups based on pre-specified criteria for percent body fat (≥32 vs. <30, respectively), body mass index (>90th vs. 20th–79th, respectively), and waist circumference (≥90th vs. 25th–75th, respectively). Participants were also individually matched on age, height, and oral contraceptive use. Using magnetic resonance imaging, trabecular bone microarchitecture was assessed at the distal radius and proximal tibia metaphysis, and cortical bone architecture was assessed at the mid-radius and mid-tibia diaphysis. OB versus NW had lower apparent trabecular thickness (radius and tibia), higher apparent trabecular separation (radius), and lower apparent bone volume to total volume (radius; all P < 0.050). Some differences in radius and tibia trabecular bone microarchitecture were retained after adjusting for insulin resistance or age at menarche. Mid-radius and mid-tibia cortical bone volume and estimated strength were lower in the OB compared to NW after adjusting for fat-free soft tissue mass (all P < 0.050). These trabecular and cortical bone deficits might contribute to the increased fracture risk in obese youth.

Keywords

Obesity Trabecular bone Magnetic resonance imaging Insulin resistance 

Notes

Acknowledgements

The authors would like to acknowledge the staff and students of the Bone and Body Composition Laboratory at the University of Georgia for their assistance in conducting this study. We also thank the participants for their time and commitment to this research.

Funding

This work was supported by Grant HL 87923-03S1 from the National Institutes of Health and the USDA, CSRS, National Institute of Food and Agriculture Hatch Projects GEO00797 and GEO00647.

Compliance with Ethical Standards

Conflict of interest

The authors have nothing to disclose.

Human and Animal Rights and Informed Consent

This study was approved by the Institutional Review Board for Human Subjects at The University of Georgia. Informed consent was obtained from all participants included in the study.

References

  1. 1.
    Cheng S, Volgyi E, Tylavsky FA, Lyytikainen A, Tormakangas T, Xu L, Cheng SM, Kroger H, Alen M, Kujala UM (2009) Trait-specific tracking and determinants of body composition: a 7-year follow-up study of pubertal growth in girls. BMC Med 7:5CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Heaney RP, Abrams S, Dawson-Hughes B, Looker A, Marcus R, Matkovic V, Weaver C (2000) Peak Bone Mass. Osteoporos Int 11:985–1009CrossRefPubMedGoogle Scholar
  3. 3.
    Nishiyama KK, Macdonald HM, Moore SA, Fung T, Boyd SK, McKay HA (2012) Cortical porosity is higher in boys compared with girls at the distal radius and distal tibia during pubertal growth: an HR-pQCT study. J Bone Miner Res 27(2):273–282CrossRefPubMedGoogle Scholar
  4. 4.
    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(4):1199–1207CrossRefPubMedGoogle Scholar
  5. 5.
    Taylor ED, Theim KR, Mirch MC, Ghorbani S, Tanofsky-Kraff M, Adler-Wailes DC, Brady S, Reynolds JC, Calis KA, Yanovski JA (2006) Orthopedic complications of overweight in children and adolescents. Pediatrics 117(6):2167–2174CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Duncan MJ, Stanley M (2012) Functional movement is negatively associated with weight status and positively associated with physical activity in british primary school children. J Obes 2012:697563CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Pollock NK, Laing EM, Baile CA, Hamrick MW, Hall DB, Lewis RD (2007) Is adiposity advantageous for bone strength? A peripheral quantitative computed tomography study in late adolescent females. Am J Clin Nutr 86(5):1530–1538PubMedGoogle Scholar
  8. 8.
    Pollock NK, Laing EM, Hamrick MW, Baile CA, Hall DB, Lewis RD (2011) Bone and fat relationships in postadolescent black females: a pQCT study. Osteoporos Int 22(2):655–665CrossRefPubMedGoogle Scholar
  9. 9.
    Wey HE, Binkley TL, Beare TM, Wey CL, Specker BL (2011) Cross-sectional versus longitudinal associations of lean and fat mass with pQCT bone outcomes in children. J Clin Endocrinol Metab 96(1):106–114CrossRefPubMedGoogle Scholar
  10. 10.
    Evans AL, Paggiosi MA, Eastell R, Walsh JS (2015) Bone density, microstructure and strength in obese and normal weight men and women in younger and older adulthood. J Bone Miner Res 30(5):920–928CrossRefPubMedGoogle Scholar
  11. 11.
    Sornay-Rendu E, Boutroy S, Vilayphiou N, Claustrat B, Chapurlat RD (2013) In obese postmenopausal women, bone microarchitecture and strength are not commensurate to greater body weight: the Os des Femmes de Lyon (OFELY) study. J Bone Miner Res 28(7):1679–1687CrossRefPubMedGoogle Scholar
  12. 12.
    Dimitri P, Jacques RM, Paggiosi M, King D, Walsh J, Taylor ZA, Frangi AF, Bishop N, Eastell R (2015) Leptin may play a role in bone microstructural alterations in obese children. J Clin Endocrinol Metab 100(2):594–602CrossRefPubMedGoogle Scholar
  13. 13.
    Farr JN, Amin S, LeBrasseur NK, Atkinson EJ, Achenbach SJ, McCready LK, Joseph Melton III L, Khosla S (2014) Body composition during childhood and adolescence: relations to bone strength and microstructure. J Clin Endocrinol Metab 99(12):4641–4648CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Hoy CL, Macdonald HM, McKay HA (2013) How does bone quality differ between healthy-weight and overweight adolescents and young adults? Clin Orthop Relat Res 471(4):1214–1225CrossRefPubMedGoogle Scholar
  15. 15.
    Jackowski SA, Faulkner RA, Farthing JP, Kontulainen SA, Beck TJ, Baxter-Jones AD (2009) Peak lean tissue mass accrual precedes changes in bone strength indices at the proximal femur during the pubertal growth spurt. Bone 44(6):1186–1190CrossRefPubMedGoogle Scholar
  16. 16.
    Kindler JM, Lewis RD, Hamrick MW (2015) Skeletal muscle and pediatric bone development. Curr Opin Endocrinol Diabetes Obes 22(6):467–474CrossRefPubMedGoogle Scholar
  17. 17.
    Leonard MB, Zemel BS, Wrotniak BH, Klieger SB, Shults J, Stallings VA, Stettler N (2015) Tibia and radius bone geometry and volumetric density in obese compared to non-obese adolescents. Bone 73:69–76CrossRefPubMedGoogle Scholar
  18. 18.
    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(3):191–197CrossRefPubMedGoogle Scholar
  19. 19.
    Fernandez JR, Redden DT, Pietrobelli A, Allison DB (2004) Waist circumference percentiles in nationally representative samples of African-American, European-American, and Mexican-American children and adolescents. J Pediatr 145(4):439–444CrossRefPubMedGoogle Scholar
  20. 20.
    Anthropometry Procedures Manual, National Health and Nutrition Examination Survey (NHANES), 2007Google Scholar
  21. 21.
    Kindler JM, Ross HL, Laing EM, Modlesky CM, Pollock NK, Baile CA, Lewis RD (2015) Load-specific physical activity scores are related to tibia bone architecture. Int J Sport Nutr Exerc Metab 25(2):136–144CrossRefPubMedGoogle Scholar
  22. 22.
    Weeks BK, Beck BR (2008) The BPAQ: a bone-specific physical activity assessment instrument. Osteoporos Int 19(11):1567–1577CrossRefPubMedGoogle Scholar
  23. 23.
    Levy JC, Matthews DR, Hermans MP (1998) Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care 21(12):2191–2192CrossRefPubMedGoogle Scholar
  24. 24.
    Modlesky CM, Subramanian P, Miller F (2008) Underdeveloped trabecular bone microarchitecture is detected in children with cerebral palsy using high-resolution magnetic resonance imaging. Osteoporos Int 19(2):169–176CrossRefPubMedGoogle Scholar
  25. 25.
    Majumdar S, Genant HK, Grampp S, Newitt DC, Truong VH, Lin JC, Mathur A (1997) Correlation of trabecular bone structure with age, bone mineral density, and osteoporotic status: in vivo studies in the distal radius using high resolution magnetic resonance imaging. J Bone Miner Res 12(1):111–118CrossRefPubMedGoogle Scholar
  26. 26.
    Modlesky CM, Majumdar S, Dudley GA (2008) Trabecular bone microarchitecture in female collegiate gymnasts. Osteoporos Int 19(7):1011–1018CrossRefPubMedGoogle Scholar
  27. 27.
    Johnson DL, Miller F, Subramanian P, Modlesky CM (2009) Adipose tissue infiltration of skeletal muscle in children with cerebral palsy. J Pediatr 154(5):715–720CrossRefPubMedGoogle Scholar
  28. 28.
    Modlesky CM, Kanoff SA, Johnson DL, Subramanian P, Miller F (2009) Evaluation of the femoral midshaft in children with cerebral palsy using magnetic resonance imaging. Osteoporos Int 20(4):609–615CrossRefPubMedGoogle Scholar
  29. 29.
    Suckling J, Sigmundsson T, Greenwood K, Bullmore ET (1999) A modified fuzzy clustering algorithm for operator independent brain tissue classification of dual echo MR images. Magn Reson Imaging 17(7):1065–1076CrossRefPubMedGoogle Scholar
  30. 30.
    Turner CH, Burr DB (2001) Experimental techniques for bone mechanics. CRC Press, Boca RatonCrossRefGoogle Scholar
  31. 31.
    Glass NA, Torner JC, Letuchy EM, Burns TL, Janz KF, Eichenberger Gilmore JM, Schlechte JA, Levy SM (2016) The relationship between greater prepubertal adiposity, subsequent age of maturation, and bone strength during adolescence. J Bone Miner Res 31(7):1455–1465CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Ducher G, Bass SL, Naughton GA, Eser P, Telford RD, Daly RM (2009) Overweight children have a greater proportion of fat mass relative to muscle mass in the upper limbs than in the lower limbs: implications for bone strength at the distal forearm. Am J Clin Nutr 90(4):1104–1111CrossRefPubMedGoogle Scholar
  33. 33.
    Farr JN, Dimitri P (2017) The impact of fat and obesity on bone microarchitecture and strength in children. Calcif Tissue Int 100(5):500–513CrossRefPubMedGoogle Scholar
  34. 34.
    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(6):2562–2572CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Tchernof A, Despres JP (2013) Pathophysiology of human visceral obesity: an update. Physiol Rev 93(1):359–404CrossRefPubMedGoogle Scholar
  36. 36.
    Sayers A, Lawlor DA, Sattar N, Tobias JH (2012) The association between insulin levels and cortical bone: findings from a cross-sectional analysis of pQCT parameters in adolescents. J Bone Miner Res 27(3):610–618CrossRefPubMedGoogle Scholar
  37. 37.
    Breen ME, Laing EM, Hall DB, Hausman DB, Taylor RG, Isales CM, Ding KH, Pollock NK, Hamrick MW, Baile CA, Lewis RD (2011) 25-hydroxyvitamin D, insulin-like growth factor-I, and bone mineral accrual during growth. J Clin Endocrinol Metab 96(1):E89–E98CrossRefPubMedGoogle Scholar
  38. 38.
    Xu L, Wang Q, Wang Q, Lyytikainen A, Mikkola T, Volgyi E, Cheng S, Wiklund P, Munukka E, Nicholson P, Alen M, Cheng S (2011) Concerted actions of insulin-like growth factor 1, testosterone, and estradiol on peripubertal bone growth: a 7-year longitudinal study. J Bone Miner Res 26(9):2204–2211CrossRefPubMedGoogle Scholar
  39. 39.
    Entingh-Pearsall A, Kahn CR (2004) Differential roles of the insulin and insulin-like growth factor-I (IGF-I) receptors in response to insulin and IGF-I. J Biol Chem 279(36):38016–38024CrossRefPubMedGoogle Scholar
  40. 40.
    Duan C, Ren H, Gao S (2010) Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: roles in skeletal muscle growth and differentiation. Gen Comp Endocrinol 167(3):344–351CrossRefPubMedGoogle Scholar
  41. 41.
    Kindler JM, Pollock NK, Laing EM, Oshri A, Jenkins NT, Isales CM, Hamrick MW, Ding KH, Hausman DB, McCabe GP, Martin BR, Hill Gallant KM, Warden SJ, Weaver CM, Peacock M, Lewis RD (2017) Insulin Resistance and the IGF-I-Cortical Bone Relationship in Children Ages 9-13 Years. J Bone Miner Res. doi: 10.1002/jbmr.3132 PubMedGoogle Scholar
  42. 42.
    Kindler JM, Pollock NK, Laing EM, Jenkins NT, Oshri A, Isales C, Hamrick M, Lewis RD (2016) Insulin resistance negatively influences the muscle-dependent IGF-I-bone mass relationship in pre-menarcheal girls. J Clin Endocrinol Metab 101(1):199–205CrossRefPubMedGoogle Scholar
  43. 43.
    Yakar S, Canalis E, Sun H, Mejia W, Kawashima Y, Nasser P, Courtland HW, Williams V, Bouxsein M, Rosen C, Jepsen KJ (2009) Serum IGF-1 determines skeletal strength by regulating subperiosteal expansion and trait interactions. J Bone Miner Res 24(8):1481–1492CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Hamrick MW, McNeil PL, Patterson SL (2010) Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact 10(1):64–70PubMedPubMedCentralGoogle Scholar
  45. 45.
    Kirmani S, Christen D, van Lenthe GH, Fischer PR, Bouxsein ML, McCready LK, Melton LJ 3rd, Riggs BL, Amin S, Muller R, Khosla S (2009) Bone structure at the distal radius during adolescent growth. J Bone Miner Res 24(6):1033–1042CrossRefPubMedGoogle Scholar
  46. 46.
    Cooper C, Dennison EM, Leufkens HG, Bishop N, van Staa TP (2004) Epidemiology of childhood fractures in Britain: a study using the general practice research database. J Bone Miner Res 19(12):1976–1981CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Joseph M. Kindler
    • 1
  • Norman K. Pollock
    • 2
  • Hannah L. Ross
    • 1
  • Christopher M. Modlesky
    • 3
  • Harshvardhan Singh
    • 4
  • Emma M. Laing
    • 1
  • Richard D. Lewis
    • 1
  1. 1.Department of Foods and NutritionThe University of GeorgiaAthensUSA
  2. 2.Department of PediatricsAugusta UniversityAugustaUSA
  3. 3.Department of KinesiologyThe University of GeorgiaAthensUSA
  4. 4.Department of Kinesiology & Applied PhysiologyUniversity of DelawareNewarkUSA

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