Skip to main content
Log in

Relationships between the lean mass index and bone mass and reference values of muscular status in healthy Chinese children and adolescents

  • Original Article
  • Published:
Journal of Bone and Mineral Metabolism Aims and scope Submit manuscript

Abstract

This study aimed to analyze the relationships between the lean mass index (LMI) and bone outcomes in Chinese children and adolescents using dual-energy X-ray absorptiometry (DXA) and to establish sex-specific reference percentile curves for the assessment of muscle status. A total of 1541 Chinese children and adolescents between the ages of 5 and 19 years were recruited from southern China. Body composition was measured by DXA (Lunar Prodigy) to acquire total body and total body less head (TBLH) measures. LMI was calculated as the LM (kg) divided by the height in meters squared. Strong sex gaps were observed after age 14 in total body LMI and appendicular LMI (p < 0.001). LM and LMI values continued to increase for boys up to age 14 compared to girls who plateaued after age 12. For each sex group, total body bone mineral content (BMC) and TBLH BMC were highly correlated with total body LMI and appendicular LMI (r = 0.856–0.916 in boys, and r = 0.651–0.804 in girls, p < 0.001). The appendicular LMI was more strongly associated with total body BMC and TBLH BMC than was total body LMI. The correlations between the BMC values and the LM measures were stronger than the fat mass results. We also present sex-specific percentile curves for LM–age and LMI–age relationships, which could be useful for identifying the LM deficits in this population.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Mazess RB, Barden HS, Bisek JP, Hanson J (1990) Dual-energy X-ray absorptiometry for total-body and regional bone-mineral and soft-tissue composition. Am J Clin Nutr 51:1106–1112

    CAS  PubMed  Google Scholar 

  2. Andreoli A, Scalzo G, Masala S, Tarantino U, Guglielmi G (2009) Body composition assessment by dual-energy X-ray absorptiometry (DXA). Radiol Med (Torino) 114:286–300

    Article  CAS  Google Scholar 

  3. Blake GM, Naeem M, Boutros M (2006) Comparison of effective dose to children and adults from dual X-ray absorptiometry examinations. Bone 38:935–942

    Article  PubMed  Google Scholar 

  4. Ellis KJ, Shypailo RJ, Pratt JA, Pond WG (1994) Accuracy of dual-energy X-ray absorptiometry for body-composition measurements in children. Am J Clin Nutr 60:660–665

    CAS  PubMed  Google Scholar 

  5. Kim J, Wang Z, Heymsfield SB, Baumgartner RN, Gallagher D (2002) Total-body skeletal muscle mass: estimation by a new dual-energy X-ray absorptiometry method. Am J Clin Nutr 76:378–383

    CAS  PubMed  Google Scholar 

  6. Humphries IR, Hua V, Ban L, Gaskin KJ, Howman-Giles R (2000) Validation of estimates of body composition by dual-energy X-ray absorptiometry in fluid overload conditions. Ann N Y Acad Sci 904:101–103

    Article  CAS  PubMed  Google Scholar 

  7. Pietrobelli A, Formica C, Wang Z, Heymsfield SB (1996) Dual-energy X-ray absorptiometry body composition model: review of physical concepts. Am J Physiol 271:E941–E951

    CAS  PubMed  Google Scholar 

  8. Janssen I, Heymsfield SB, Wang ZM, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol 89:81–88

    CAS  PubMed  Google Scholar 

  9. Chen Z, Wang Z, Lohman T, Heymsfield SB, Outwater E, Nicholas JS, Bassford T, LaCroix A, Sherrill D, Punyanitya M, Wu G, Going S (2007) Dual-energy X-ray absorptiometry is a valid tool for assessing skeletal muscle mass in older women. J Nutr 137:2775–2780

    CAS  PubMed  Google Scholar 

  10. Heymsfield SB, Smith R, Aulet M, Bensen B, Lichtman S, Wang J, Pierson RN Jr (1990) Appendicular skeletal muscle mass: measurement by dual-photon absorptiometry. Am J Clin Nutr 52:214–218

    CAS  PubMed  Google Scholar 

  11. VanItallie TB, Yang MU, Heymsfield SB, Funk RC, Boileau RA (1990) Height-normalized indices of the body’s fat-free mass and fat mass: potentially useful indicators of nutritional status. Am J Clin Nutr 52:953–959

    CAS  PubMed  Google Scholar 

  12. Wells JC (2000) A Hattori chart analysis of body mass index in infants and children. Int J Obes Relat Metab Disord 24:325–329

    Article  CAS  PubMed  Google Scholar 

  13. Wells JC (2001) A critique of the expression of paediatric body composition data. Arch Dis Child 85:67–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, Garry PJ, Lindeman RD (1998) Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol 147:755–763

    Article  CAS  PubMed  Google Scholar 

  15. Gerasimidis K, Keane O, Macleod I, Flynn DM, Wright CM (2010) A four-stage evaluation of the Paediatric Yorkhill Malnutrition Score in a tertiary paediatric hospital and a district general hospital. Br J Nutr 104:751–756

    Article  CAS  PubMed  Google Scholar 

  16. Cederholm TE, Bauer JM, Boirie Y, Schneider SM, Sieber CC, Rolland Y (2011) Toward a definition of sarcopenia. Clin Geriatr Med 27:341–353

    Article  PubMed  Google Scholar 

  17. Goulding A, Taylor RW, Grant AM, Jones S, Taylor BJ, Williams SM (2009) Relationships of appendicular LMI and total body LMI to bone mass and physical activity levels in a birth cohort of New Zealand five-year olds. Bone 45:455–459

    Article  PubMed  Google Scholar 

  18. Csakvary V, Erhardt E, Vargha P, Oroszlan G, Bodecs T, Torok D, Toldy E, Kovacs GL (2012) Association of lean and fat body mass, bone biomarkers and gonadal steroids with bone mass during pre- and midpuberty. Horm Res Paediatr 78:203–211

    Article  CAS  PubMed  Google Scholar 

  19. Guo B, Xu Y, Gong J, Tang Y, Shang J, Xu H (2015) Reference data and percentile curves of body composition measured with dual energy X-ray absorptiometry in healthy Chinese children and adolescents. J Bone Miner Metab 33:530–539

    Article  PubMed  Google Scholar 

  20. Kelly TL, Wilson KE, Heymsfield SB (2009) Dual energy X-ray absorptiometry body composition reference values from NHANES. PLoS One 4:e7038

    Article  PubMed  PubMed Central  Google Scholar 

  21. Wells JC, Williams JE, Chomtho S, Darch T, Grijalva-Eternod C, Kennedy K, Haroun D, Wilson C, Cole TJ, Fewtrell MS (2012) Body-composition reference data for simple and reference techniques and a 4-component model: a new UK reference child. Am J Clin Nutr 96:1316–1326

    Article  CAS  PubMed  Google Scholar 

  22. Schautz B, Later W, Heller M, Muller MJ, Bosy-Westphal A (2012) Total and regional relationship between lean and fat mass with increasing adiposity—impact for the diagnosis of sarcopenic obesity. Eur J Clin Nutr 66:1356–1361

    Article  CAS  PubMed  Google Scholar 

  23. Weber DR, Moore RH, Leonard MB, Zemel BS (2013) Fat and lean BMI reference curves in children and adolescents and their utility in identifying excess adiposity compared with BMI and percentage body fat. Am J Clin Nutr 98:49–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Nakao T, Komiya S (2003) Reference norms for a fat-free mass index and fat mass index in the Japanese child population. J Physiol Anthropol Appl Hum Sci 22:293–298

    Article  Google Scholar 

  25. Wells JC, Coward WA, Cole TJ, Davies PS (2002) The contribution of fat and fat-free tissue to body mass index in contemporary children and the reference child. Int J Obes Relat Metab Disord 26:1323–1328

    Article  CAS  PubMed  Google Scholar 

  26. Maynard LM, Wisemandle W, Roche AF, Chumlea WC, Guo SS, Siervogel RM (2001) Childhood body composition in relation to body mass index. Pediatrics 107:344–350

    Article  CAS  PubMed  Google Scholar 

  27. Xiong KY, He H, Zhang YM, Ni GX (2012) Analyses of body composition charts among younger and older Chinese children and adolescents aged 5 to 18 years. BMC Public Health 12:835

    Article  PubMed  PubMed Central  Google Scholar 

  28. Nelson DA, Barondess DA (1997) Whole body bone, fat and lean mass in children: comparison of three ethnic groups. Am J Phys Anthropol 103:157–162

    Article  CAS  PubMed  Google Scholar 

  29. Li H, Ji CY, Zong XN, Zhang YQ (2009) Height and weight standardized growth charts for Chinese children and adolescents aged 0 to 18 years. Zhonghua Er Ke Za Zhi 47:487–492

    PubMed  Google Scholar 

  30. Ministry of Education of the People’s Republic of China (2007) Report on the physical fitness and health surveillance of Chinese school students. Higher Education Press, Beijing

    Google Scholar 

  31. Cole TJ, Green PJ (1992) Smoothing reference centile curves: the LMS method and penalized likelihood. Stat Med 11:1305–1319

    Article  CAS  PubMed  Google Scholar 

  32. Schutte JE, Townsend EJ, Hugg J, Shoup RF, Malina RM, Blomqvist CG (1984) Density of lean body mass is greater in blacks than in whites. J Appl Physiol 56:1647–1649

    Article  CAS  PubMed  Google Scholar 

  33. Eissa MA, Dai S, Mihalopoulos NL, Day RS, Harrist RB, Labarthe DR (2009) Trajectories of fat mass index, fat free-mass index, and waist circumference in children: Project HeartBeat. Am J Prev Med 37:S34–S39

    Article  PubMed  PubMed Central  Google Scholar 

  34. Hull HR, Thornton J, Wang J, Pierson RN Jr, Kaleem Z, Pi-Sunyer X, Heymsfield S, Albu J, Fernandez JR, Vanitallie TB, Gallagher D (2011) Fat-free mass index: changes and race/ethnic differences in adulthood. Int J Obes (Lond) 35:121–127

    Article  CAS  Google Scholar 

  35. Libman IM, LaPorte RE, Becker D, Dorman JS, Drash AL, Kuller L (1998) Was there an epidemic of diabetes in nonwhite adolescents in Allegheny County, Pennsylvania. Diabetes Care 21:1278–1281

    Article  CAS  PubMed  Google Scholar 

  36. (2000) Type 2 diabetes in children and adolescents. American Diabetes Association. Diabetes Care 23:381–389

  37. Bacha F, Saad R, Gungor N, Janosky J, Arslanian SA (2003) Obesity, regional fat distribution, and syndrome X in obese black versus white adolescents: race differential in diabetogenic and atherogenic risk factors. J Clin Endocrinol Metab 88:2534–2540

    Article  CAS  PubMed  Google Scholar 

  38. van der Sluis IM, de Ridder MA, Boot AM, Krenning EP, de Muinck Keizer-Schrama SM (2002) Reference data for bone density and body composition measured with dual energy X ray absorptiometry in white children and young adults. Arch Dis Child 87:341–347 (discussion 341–347)

    Article  PubMed  PubMed Central  Google Scholar 

  39. Demerath EW, Schubert CM, Maynard LM, Sun SS, Chumlea WC, Pickoff A, Czerwinski SA, Towne B, Siervogel RM (2006) Do changes in body mass index percentile reflect changes in body composition in children? Data from the Fels Longitudinal Study. Pediatrics 117:e487–e495

    Article  PubMed  Google Scholar 

  40. Martin LG, Grossman MS, Connor TB, Levitsky LL, Clark JW, Camitta FD (1979) Effect of androgen on growth hormone secretion and growth in boys with short stature. Acta Endocrinol (Copenh) 91:201–212

    CAS  Google Scholar 

  41. Frost HM (2003) Bone’s mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275:1081–1101

    Article  PubMed  Google Scholar 

  42. Heymsfield SB, McManus C, Stevens V, Smith J (1982) Muscle mass: reliable indicator of protein-energy malnutrition severity and outcome. Am J Clin Nutr 35:1192–1199

    CAS  PubMed  Google Scholar 

  43. Bauer JM, Sieber CC (2008) Sarcopenia and frailty: a clinician’s controversial point of view. Exp Gerontol 43:674–678

    Article  CAS  PubMed  Google Scholar 

  44. Wells JC (2003) Body composition in childhood: effects of normal growth and disease. Proc Nutr Soc 62:521–528

    Article  CAS  PubMed  Google Scholar 

  45. Tothill P, Avenell A, Love J, Reid DM (1994) Comparisons between Hologic, Lunar and Norland dual-energy X-ray absorptiometers and other techniques used for whole-body soft tissue measurements. Eur J Clin Nutr 48:781–794

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to express their gratitude to all participating children and their parents. We are grateful to Dr. Qi Zhou, GE Healthcare Shanghai, and Dr. Jing Xiang, First Hospital of Jiaxing, for their useful comments and suggestions. We also thank the staff members of the Department of Nuclear Medicine, First Affiliated Hospital of Jinan University for excellent technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hao Xu.

Ethics declarations

Conflict of interest

No conflict of interest was declared.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, B., Wu, Q., Gong, J. et al. Relationships between the lean mass index and bone mass and reference values of muscular status in healthy Chinese children and adolescents. J Bone Miner Metab 34, 703–713 (2016). https://doi.org/10.1007/s00774-015-0725-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00774-015-0725-8

Keywords

Navigation