Archives of Osteoporosis

, 13:79 | Cite as

Age and sex effects on the relationship between body composition and hip geometric structure in males and females from East China

  • Yanping Du
  • Hanmin Zhu
  • Songbai Zheng
  • Xiaoying Zhu
  • Xuemei Zhang
  • Sihong Xue
  • Huilin Li
  • Wei Hong
  • Wenjing Tang
  • Minmin Chen
  • Qun ChengEmail author
Original Article



The study finds bone mineral density is the principal determinant of hip geometry and lean mass is a better determinant than fat mass in Chinese. Moreover, the impact of fat on skeleton differs with age, with a negative effect in young people but a more positive effect in elderly.


The aim of this study was to examine whether the correlation between body composition including bone mineral density (BMD), lean mass (LM) and fat mass (FM), and hip geometric structure change with aging in males and females from East China.


It was a cross-section study. A total of 1168 healthy male and 1066 healthy females in Shanghai were divided into six groups based on their age and sex. All participants were evaluated by assessing the BMD of lumber spine and proximal hip, total LM, total FM, and geometric parameters of the hip such as the cross-sectional area (CSA), average cortical thickness (ACT), and the buckling ratio (BR) at the narrow neck (NN), the intertrochanter (IT), and the shaft (FS).


Among the three body composition, the correlation between hip BMD and hip geometric structure was strongest. LM showed significantly positive correlations with CSA. FM showed negative or little positive correlation with hip geometry in the young group. However, the degree of the contribution of FM to hip geometric structure became substantially positive with aging. Limb LM produced the largest positive contribution to CSA and ACT at all three regions in young males. However, in older males the trunk LM produced the largest positive contribution to CSA and ACT.


Among all body composition parameters, hip BMD showed the largest correlation with hip geometric structure, with LM showing the second largest. The impact of FM and LM on hip geometry changed with aging and with different distributions of lean mass and fat mass.


Body composition Lean mass Fat mass Hip geometry Age Sex 



bone mineral density


lean mass


fat mass


cross-sectional area


average cortical thickness


buckling ratio


narrow neck







We like to thank a bunch to Yang Fei about her work on statistical analysis of data in this study, and we also like to thank all participants of the study and the involved laboratory staff.

Authors’ contributions

YPD, HMZ, and SBZ involved in the design of the study and interpretation of data.

XYZ, XMZ, and SHX participated in acquisition of data and analyzed the data.

WH performed the statistical analysis.

WJT, MMC, and HLL participated in the subjects recruitment and study implementation and coordination.

QC and YPD helped to draft the manuscript.

QC was in charge of the entire project.

All authors read and approved the final manuscript.


This study was supported by the National Natural Science Foundation of China (NSFC; No. 81471089), Shanghai science and technology commission (16411954600), and Shanghai Hospital Development Center (SHDC12016201).

Compliance with ethical standards

Ethics and consent statement

All of the subjects provided written informed consent before participating in the study, and the program was approved by the Huadong Hospital Ethics Committee (Project NO.2014K004).

Conflicts of interest



  1. 1.
    Looker A, Flegal K, Melton LR III (2007) Impact of increased overweight on the projected prevalence of osteoporosis in older women. Osteoporos Int 18:307–313CrossRefGoogle Scholar
  2. 2.
    De Laet C, Kanis JA, Odén A, Johanson H, Johnell O, Delmas P et al (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int 16:1330–1338CrossRefGoogle Scholar
  3. 3.
    Leslie WD, Weiler HA, Lix LM, Nyomba BL (2008) Body composition and bone density in Canadian White and Aboriginal women: the First Nations Bone Health Study. Bone 42:990–995CrossRefGoogle Scholar
  4. 4.
    Makovey J, Naganathan V, Sambrook P (2005) Gender differences in relationships between body composition components, their distribution and bone mineral density: a cross-sectional opposite sex twin study. Osteoporos Int 16:1495–1505CrossRefGoogle Scholar
  5. 5.
    Cui LH, Shin MH, Kweon SS, Park KS, Lee YH, Chung EK, Nam HS, Choi JS (2007) Relative contribution of body composition to bone mineral density at different sites in men and women of South Korea. J Bone Miner Metab 25:165–171CrossRefGoogle Scholar
  6. 6.
    Cummings SR, Cawthon PM, Ensrud KE, Cauley JA, Fink HA, Orwoll ES (2006) Osteoporotic Fractures in Men (MrOS) Research Groups; Study of Osteoporotic Fractures Research Groups BMD and risk of hip and nonvertebral fractures in older men: a prospective study and comparison with older women. J Bone Miner Res 21:1550–1556CrossRefGoogle Scholar
  7. 7.
    Hernandez CJ, Keaveny TM (2006) A biomechanical perspective on bone quality. Bone 39:1173–1181CrossRefGoogle Scholar
  8. 8.
    Seeman E, Delmas PD (2006) Bone quality–the material and structural basis of bone strength and fragility. N Engl J Med 354:2250–2261CrossRefGoogle Scholar
  9. 9.
    Beck TJ, Ruff CB, Warden KE, Scott WW Jr, Rao GU (1990) Predicting femoral neck strength from bone mineral data. A structural approach. Invest Radiol 25:6–18CrossRefGoogle Scholar
  10. 10.
    Travison TG, Araujo AB, Esche GR, Beck TJ, McKinlay JB (2008) Lean mass and not fat mass is associated with male proximal femur strength. J Bone Miner Res 23:189–198CrossRefGoogle Scholar
  11. 11.
    Hu WW, Zhang H, Wang C, Gu JM, Yue H, Ke YW et al (2012) Lean mass predicts hip geometry and bone mineral density in Chinese men and women and age comparisons of body composition. J Clin Densitom 15:434–442CrossRefGoogle Scholar
  12. 12.
    Cheng Q, Zhu YX, Zhang MX, Li LH, Du PY, Zhu MH (2012) Age and sex effects on the association between body composition and bone mineral density in healthy Chinese men and women. Menopause 19:448–455CrossRefGoogle Scholar
  13. 13.
    Takada J, Beck TJ, Iba K, Yamashita T (2007) Structural trends in the aging proximal femur in Japanese postmenopausal women. Bone 41:97–102CrossRefGoogle Scholar
  14. 14.
    Beck TJ, Petit MA, Wu G (2009) Does obesity really make the femur stronger? BMD, geometry, and fracture incidence in the Women’s Health Initiative -observational study. J Bone Miner Res 24:1369–1379CrossRefGoogle Scholar
  15. 15.
    Petit MA, Beck TJ, Shults J, Zemel BS, Foster BJ, Leonard MB (2005) Proximal femur bone geometry is appropriately adapted to lean mass in overweight children and adolescents. Bone 36:568–576CrossRefGoogle Scholar
  16. 16.
    Daly RM, Stenevi-Lundgren S, Linden C, Karlsson MK (2008) Muscle determinants of bone mass, geometry and strength in prepubertal girls. Med Sci Sports Exerc 40:1135–1141CrossRefGoogle Scholar
  17. 17.
    Semanick LM, Beck TJ, Cauley JA, Wheeler VW, Patrick AL, Bunker CH, Zmuda JM (2005) Association of body composition and physical activity with proximal femur geometry in middle-aged and elderly Afro-Caribbean men: the Tobago bone health study. Calcif Tissue Int 77:160–166CrossRefGoogle Scholar
  18. 18.
    Wu S, Lei SF, Chen XD, Tan LJ, Jian WX, Deng FY et al (2007) The contributions of lean tissue mass and fat mass to bone geometric adaptation at the femoral neck in Chinese overweight adults. Ann Hum Biol 34:344–353CrossRefGoogle Scholar
  19. 19.
    Hong X, Arguelles LM, Liu X, Tsai HJ, Hsu YH, Wang B, Zhang S, Li Z, Tang G, Liu X, Yang J, Xu X, Langman C, Wang X (2010) Percent fat mass is inversely associated with bone mass and hip geometry in rural Chinese adolescents. J Bone Miner Res 25:1544–1554CrossRefGoogle Scholar
  20. 20.
    Rosen CJ, Ackert-Bicknell C, Beamer WG, Nelson T, Adamo M, Cohen P, Bouxsein ML, Horowitz MC (2005) Allelic differences in a quantitative trait locus affecting insulin-like growth factor-I impact skeletal acquisition and body composition. Pediatr Nephrol 20:255–260CrossRefGoogle Scholar
  21. 21.
    Fairbrother UL, Tankó LB, Walley AJ, Christiansen C, Froguel P, Blakemore AI (2007) Leptin receptor genotype at Gln223Arg is associated with body composition, BMD, and vertebral fracture in postmenopausal Danish women. J Bone Miner Res 22:544–550CrossRefGoogle Scholar
  22. 22.
    Huang QY, Shen H, Deng HY, Conway T, Davies KM, Li JL, Recker RR, Deng HW (2003) Linkage and association of the CA repeat polymorphism of the IL6 gene, obesity-related phenotypes, and bone mineral density (BMD) in two independent Caucasian populations. J Hum Genet 48:430–437CrossRefGoogle Scholar
  23. 23.
    Rawad E, Christophe J, Elie M (2009) Total body, lumbar spine and hip bone mineral density in overweight adolescent girls: decreased or increased? J Bone Miner Metab 27:629–633CrossRefGoogle Scholar
  24. 24.
    Napoli N, Faccio R, Shrestha V, Bucchieri S, Rini GB, Armamento-Villareal R (2007) Estrogen metabolism modulates bone density in men. Calcif Tissue Int 80:227–232CrossRefGoogle Scholar
  25. 25.
    Ichikawa S, Koller DL, Peacock M, Johnson ML, Lai D, Hui SL, Johnston CC, Foroud TM, Econs MJ (2005) Polymorphisms in the estrogen receptorA (ESR2) gene are associated with bone mineral density in Caucasian men and women. J Clin Endocrinol Metab 90:5921–5927CrossRefGoogle Scholar
  26. 26.
    Hong JH, Hwang ES, McManus MT, Amsterdam A, Tian Y, Kalmukova R, Mueller E, Benjamin T, Spiegelman BM, Sharp PA, Hopkins N, Yaffe MB (2005) TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 309:1074–1078CrossRefGoogle Scholar
  27. 27.
    Pei L, Tontonoz P (2004) Fat’s loss is bone’s gain. J Clin Invest 113:805–806CrossRefGoogle Scholar
  28. 28.
    Pereira-Santos M, Costa PR, Assis AM et al (2015) Obesity and vitamin D deficiency: a systematic review and meta-analysis. Obes Rev 16:341–349CrossRefGoogle Scholar
  29. 29.
    Frost HM (2003) Bone’s mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275:1081–1101CrossRefGoogle Scholar
  30. 30.
    Fricke O, Schoenau E (2007) The “functional muscle – bone unit”: probing the relevance of mechanical signals for bone development in children and adolescents. Growth Hormon IGF Res 17:1–9CrossRefGoogle Scholar
  31. 31.
    Forwood MR, Li L, Kelly WL, Bennett MB (2001) Growth hormone is permissive for skeletal adaptation to mechanical loading. J Bone Miner Res 16:2284–2290CrossRefGoogle Scholar
  32. 32.
    Mukherjee A, Murray RD, Shalet SM (2004) Impact of growth hormone status on body composition and the skeleton. Horm Res 62(Suppl 3):35–41PubMedGoogle Scholar
  33. 33.
    Baker JR, Bemben MG, Anderson MA, Bemben DA (2006) Effects of age on testosterone responses to resistence exercise and musculoskeletal variables in men. J Strength Cond Res 20(4):874–881PubMedGoogle Scholar
  34. 34.
    Venken K, Movérare-Skrtic S, Kopchick JJ, Coschigano KT, Ohlsson C, Boonen S, Bouillon R, Vanderschueren D (2007) Impact of androgens, growth hormone, and IGF-I on bone and muscle in male mice during puberty. J Bone Miner Res 22:72–82CrossRefGoogle Scholar
  35. 35.
    Lee KC, Jessop H, Suswillo R, Zaman G, Lanyon LE (2004) The adaptive response of bone to mechanical loading in female transgenic mice is deficient in the absence of estrogen receptor-alpha and -beta. J Endocrinol 182:192–201Google Scholar
  36. 36.
    Mcclelland GB, Kraft CS, Mitchaud D, Russell JC, Mueller CR, Moyes CD (2004) Leptin and the control of respiratory gene expression in muscle. Biochim Biophys Acta 1688(1):86–93CrossRefGoogle Scholar
  37. 37.
    Holloway WR, Collier FM, Aitken CJ, Myers DE, Hodge JM, Malakellis M et al (2002) Leptin inhibits osteoclast generation. J Bone Miner Res 17:200–209CrossRefGoogle Scholar
  38. 38.
    Ruohola JP, Laaksi L, Ylikomi T, Haataja R, Mattila VM, Sahi T et al (2006) Association between serum 25(OH)D concentrations and bone stress fractures in Finnish young men. J Bone Miner Res 21:1483–1488CrossRefGoogle Scholar
  39. 39.
    Heinonen I, Kemppainen J, Kaskinoro K, Langberg H, Knuuti J, Boushel R, Kjaer M, Kalliokoski KK (2013) Bone blood flow and metabolism in humans: effect of muscular exercise and other physiological perturbations. J Bone Miner Res 28:1068–1074CrossRefGoogle Scholar
  40. 40.
    Matsuoka T, Ahlberg PE, Kessaris N, Palma I, Dennehy U, Richardson WD et al (2005) Neural crest origins of the neck and shoulder. Nature 436:347–355CrossRefGoogle Scholar
  41. 41.
    Arabi A, Tamim H, Nabulsi M, Maalouf J, Khalife H, Choucair M et al (2004) Sex differences in the effect of body-composition variables on bone mass in healthy children and adolescents. Am J Clin Nutr 80(5):1428–1435CrossRefGoogle Scholar
  42. 42.
    Suominen H (2006) Muscle training for bone strength. Aging Clin Exp Res 18:85–93CrossRefGoogle Scholar
  43. 43.
    Lemieux S, Prud’homme D, Bouchard C, Tremblay A, Després JP (1993) Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr 58:463–467CrossRefGoogle Scholar
  44. 44.
    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 94:3387–3393CrossRefGoogle Scholar
  45. 45.
    Cartier A, Lemieux I, Alméras N, Tremblay A, Bergeron J, Després JP (2008) Visceral obesity and plasma glucose-insulin homeostasis: contributions of interleukin-6 and tumor necrosis factor-alpha in men. J Clin Endocrinol Metab 93:1931–1938CrossRefGoogle Scholar
  46. 46.
    Ding C, Parameswaran V, Udayan R, Burgess J, Jones G (2008) Circulating levels of inflammatory markers predict change in bone mineral density and resorption in older adults: a longitudinal study. J Clin Endocrinol Metab 93:1952–1958CrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Authors and Affiliations

  • Yanping Du
    • 1
  • Hanmin Zhu
    • 1
  • Songbai Zheng
    • 1
  • Xiaoying Zhu
    • 1
  • Xuemei Zhang
    • 1
  • Sihong Xue
    • 1
  • Huilin Li
    • 1
  • Wei Hong
    • 1
  • Wenjing Tang
    • 1
  • Minmin Chen
    • 1
  • Qun Cheng
    • 1
    Email author
  1. 1.Department of Osteoporosis and Bone Disease, Research Section of Geriatric Metabolic Bone Disease, Shanghai Geriatric InstituteFudan University Affiliated Huadong HospitalShanghaiChina

Personalised recommendations