Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Body mass index as a phenotypic expression of adiposity: quantitative contribution of muscularity in a population-based sample

Abstract

Objective:

Although widely applied as a phenotypic expression of adiposity in population and gene-search studies, body mass index (BMI) is also acknowledged to reflect muscularity even though relevant studies directly measuring skeletal muscle (SM) mass are lacking. The current study aimed to fill this important gap by applying advanced imaging methods to test the hypothesis that, after controlling first for adiposity, SM mass is also a significant determinant of BMI in a population-based sample.

Design:

Whole-body magnetic resonance imaging scans were completed in Coronary Artery Risk Development in Young Adults study subjects aged 33–45 years. Physical activity (PA) levels, alcohol intake and adequacy of food intake were assessed by standardized questionnaires.

Subjects:

The study included 58 African-American (AA) and 78 Caucasian (C) men; and 63 AA and 64 C women.

Measurements:

Whole-body adipose tissue (AT) and SM volumes.

Results:

AT was significantly predicted by not only BMI, but also PA and alcohol intake with total model R2's of 0.68 (P<0.0001) for men and 0.89 (P<0.0001) for women. Men had more SM than AT at all levels of BMI whereas SM predominated in women at lower BMIs (C<26 kg/m2; AA<28 kg/m2). In men, both AT and SM contributed a similar proportion of between-subject variation in BMI. In contrast, in women AT contributed 30% more than SM to the variation in BMI. Developed allometric models indicated SM associations with AT, PA and race after adjusting for height. There was little association of age, lifestyle factors or race with BMI after controlling for both AT and SM.

Conclusion:

Variation in muscularity provides a mechanistic basis for the previously observed nonspecificity of BMI as a phenotypic expression of adiposity. These quantitative observations have important implications when choosing adiposity measures in population and gene-search studies.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2

Similar content being viewed by others

References

  1. National Institutes of Health, National Heart, Lung, and Blood Institute. Clinical Guidelines on the Identification, Evaluation, and Treatment of Overweight and Obesity in Adults—The Evidence Report. Obes Res 1998; 6 (Suppl 2): 51S–209S.

    Google Scholar 

  2. Quetelet LAJ . A Treatise on Man and the Development of His Faculties. Edinburgh: William and Robert Chambers. In: 1973, Comparative statistics in the 19th century. Gregg International Publisher: Farnborough, 1842.

    Google Scholar 

  3. Keys A, Fidanza F, Karvonen MJ, Kimura N, Taylor HL . Indices of relative weight and obesity. J Chron Dis 1972; 25: 329–343.

    Article  CAS  PubMed  Google Scholar 

  4. Flegal KM, Shepherd JA, Looker AC, Graubard BI, Borrud LG, Ogden CL et al. Comparisons of percentage body fat, body mass index, waist circumference, and waist-stature ratio in adults. Am J Clin Nutr 2009; 89: 500–508.

    Article  CAS  PubMed  Google Scholar 

  5. Gallagher D, Visser M, Sepúlveda D, Pierson RN, Harris T, Heymsfield SB . How useful is body mass index for comparison of body fatness across age, sex, and ethnic groups? Am J Epidemiol 1996; 143: 228–239.

    Article  CAS  PubMed  Google Scholar 

  6. Gallagher D, Heymsfield SB, Heo M, Jebb SA, Murgatroyd PR, Sakamoto Y . Healthy percentage body fat ranges: an approach for developing guidelines based on body mass index. Am J Clin Nutr 2000; 72: 694–701.

    Article  CAS  PubMed  Google Scholar 

  7. Gurrici S, Hartriyanti Y, Hautvast JG, Deurenberg P . Differences in the relationship between body fat and body mass index between two different Indonesian ethnic groups: the effect of body build. Eur J Clin Nutr 1999; 53: 468–472.

    Article  CAS  PubMed  Google Scholar 

  8. Ode JJ, Pivarnik JM, Reeves MJ, Knous JL . Body mass index as a predictor of percent fat in college athletes and nonathletes. Med Sci Sports Exerc 2007; 39: 403–409.

    Article  PubMed  Google Scholar 

  9. Larsson I, Henning B, Lindroos AK, Näslund I, Sjöström CD, Sjöström L . Optimized predictions of absolute and relative amounts of body fat from weight, height, other anthropometric predictors, and age. Am J Clin Nutr 2006; 83: 252–259.

    Article  CAS  PubMed  Google Scholar 

  10. Deurenberg P, Deurenberg-Yap M, Guricci S . Asians are different from Caucasians and from each other in their body mass index/body fat percent relationships. Obes Rev 2002; 3: 141–146.

    Article  CAS  PubMed  Google Scholar 

  11. Deurenberg P, Yap M, van Staveren WA . Body mass index and percent body fat: a meta analysis among different ethnic groups. Int J Obes 1998; 22: 1164–1171.

    Article  CAS  Google Scholar 

  12. Rush EC, Goedecke JH, Jennings C, Micklesfield L, Dugas L, Lambert EV et al. BMI, fat and muscle differences in urban women of five ethnicities from two countries. Int J Obes 2007; 31: 1232–1239.

    Article  CAS  Google Scholar 

  13. Rush E, Plank L, Chandu V, Laulu M, Simmons D, Swinburn B et al. Body size, body composition, and fat distribution: a comparison of young New Zealand men of European, Pacific Island, and Asian Indian ethnicities. N Z Med J 2004; 117: U1203.

    PubMed  Google Scholar 

  14. Romero-Corral A, Somers VK, Sierra-Johnson J, Thomas RJ, Collazo-Clavell ML, Korinek J et al. Accuracy of body mass index in diagnosing obesity in the adult general population. Int J Obes 2008; 32: 959–966.

    Article  CAS  Google Scholar 

  15. Heymsfield SB, Gallagher D, Kotler DP, Wang Z, Allison DB, Heshka S . Body-size dependence of resting energy expenditure can be attributed to non-energetic homogeneity of fat-free mass. Am J Physiol Endocrinol Metab 2002; 282: E132–E138.

    Article  CAS  PubMed  Google Scholar 

  16. Wang Z, Heo M, Lee RC, Kotler DP, Withers RT, Heymsfield SB . Muscularity in adult humans: proportion of adipose tissue-free body mass as skeletal muscle. Am J Hum Biol 2001; 13: 612–619.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  18. Friedman GD, Cutter GR, Donahue RP, Hughes GH, Hulley SB, Jacobs Jr DR et al. CARDIA: study design, recruitment, and some characteristics of the examined subjects. J Clin Epidemiol 1988; 41: 1105–1116.

    Article  CAS  PubMed  Google Scholar 

  19. Tien PC, Benson C, Zolopa AR, Sidney S, Osmond D, Grunfeld C . The study of fat redistribution and metabolic change in HIV infection (FRAM): methods, design, and sample characteristics. Am J Epidemiol 2006; 163: 860–869.

    Article  PubMed  Google Scholar 

  20. Hughes GH, Cutter G, Donahue R, Friedman GD, Hulley S, Hunkeler E et al. Recruitment in the Coronary Artery Disease Risk Development in Young Adults (CARDIA) Study. Control Clin Trials 1987; 8: 68S–73S.

    Article  CAS  PubMed  Google Scholar 

  21. Hill JO, Sidney S, Lewis CE, Tolan K, Scherzinger AL, Stamm ER . Racial differences in amounts of visceral adipose tissue in young adults: the CARDIA (Coronary Artery Risk Development in Young Adults) study. Am J Clin Nutr 1999; 69: 381–387.

    Article  CAS  PubMed  Google Scholar 

  22. Gallagher D, Belmonte D, Deurenberg P, Wang Z, Krasnow N, Pi-Sunyer FX et al. Organ-tissue mass measurement allows modeling of REE and metabolically active tissue mass. Am J Physiol 1998; 275: E249–E258.

    CAS  PubMed  Google Scholar 

  23. Bacchetti P, Gripshover B, Grunfeld C, Heymsfield S, McCreath H, Osmond D et al. J Acquir Immune Defic Syndr 2005; 40: 121–131.

  24. Bacchetti P, Cofrancesco J, Heymsfield S, Lewis CE, Scherzer R, Shlipak M et al. Fat distribution in women with HIV infection. J Acquir Immune Defic Syndr 2006; 42: 562–571.

    Article  Google Scholar 

  25. Sidney S, Jacobs Jr DR, Haskell WL, Armstrong MA, Dimicco A, Oberman A et al. Comparison of two methods of assessing physical activity in the Coronary Artery Risk Development in Young Adults (CARDIA) study. Am J Epidemiol 1991; 133: 1231–1245.

    Article  CAS  PubMed  Google Scholar 

  26. Hoegerman GS, Lewis CE, Flack J, Raczynski JM, Caveny J, Gardin JM . Lack of association of recreational cocaine and alcohol use with left ventricular mass in young adults. The Coronary Artery Risk Development in Young Adults (CARDIA) study. J Am Coll Cardiol 1995; 25: 895–900.

    Article  CAS  PubMed  Google Scholar 

  27. Heymsfield SB, Gallagher D, Mayer L, Beetsch J, Pietrobelli A . Scaling of human body composition to stature: new insights into body mass index. Am J Clin Nutr 2007; 86: 82–91.

    Article  CAS  PubMed  Google Scholar 

  28. Scherzer R, Bacchetti P, Shlipak MG, Kotler D, Lewis CE, Shen W et al. Simple anthropometric measures correlate with metabolic risk indicators as well as MRI-measured adipose tissue depots in both HIV-infected and control subjects. Am J Clin Nutr 2008; 87: 1809–1817.

    Article  CAS  PubMed  Google Scholar 

  29. Efron B, Tibshirani R . An Introduction to the Bootstrap. Chapman and Hall: London, 1993.

    Book  Google Scholar 

  30. Flegal KM . Epidemiologic aspects of overweight and obesity in the United States. Physiol Behav 2005; 86: 599–602.

    Article  CAS  PubMed  Google Scholar 

  31. Thorleifsson G, Walters GB, Gudbjartsson DF, Steinthorsdottir V, Sulem P, Helgadottir A et al. Genome-wide association yields new sequence variants at seven loci that associate with measures of obesity. Nat Genet 2009; 41: 18–24.

    Article  CAS  PubMed  Google Scholar 

  32. Rothman KJ . BMI-related errors in the measurement of obesity. Int J Obes 2008; 32 (Suppl 3): S56–S59.

    Article  Google Scholar 

  33. Baumgartner RN, Waters DL, Gallagher D, Morley JE, Garry PJ . Predictors of skeletal muscle mass in elderly men and women. Mech Ageing Dev 1999; 107: 123–136.

    Article  CAS  PubMed  Google Scholar 

  34. Jones Jr A, Shen W, St-Onge MP, Gallagher D, Heshka S, Wang Z et al. Body-composition differences between African American and white women: relation to resting energy requirements. Am J Hum Biol 2001; 13: 612–619.

    Article  Google Scholar 

  35. Van Itallie TB . Obesity: adverse effects on health and longevity. Am J Clin Nutr 1979; 32 (12 Suppl): 2723–2733.

    Article  CAS  PubMed  Google Scholar 

  36. Subcommittee on Military Weight Management, Committee on Military Nutrition Research. Weight Management State of the Science and Opportunities for Military Programs Institute of Medicine. National Academies Press: Washington, DC, 2004.

  37. Haddock CK, Poston WS, Klesges RC, Talcott GW, Lando H, Dill PL . An examination of body weight standards and the association between weight and health behaviours in the United States Air Force. Milit Med 1999; 164: 51–54.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Dr Heymsfield contributed to the article in its conception and design, analysis and interpretation of the data, drafting and critically revising the article. Dr Scherzer contributed to the article by analysis and interpretation of the data, drafting and critical revising the article. Dr Pietrobelli contributed to the article by analysis and interpretation of the data and critical review of the article. Dr Lewis was involved in the acquisition of the data, critical revision, obtaining funding and administrative support. Dr Grunfeld contributed to the conception and design, acquisition, analysis and interpretation of the data, drafting and critically revising the article. This work was supported by NIH Grants: K23, AI 66943; RO1, DK57508, HL74814 and HL 53359; CFAR, AI50410 and NIH GCRC Grants M01- RR00036, RR00046, RR00051, RR00052, RR00054, RR00083, RR0636 and RR0086.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S B Heymsfield.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heymsfield, S., Scherzer, R., Pietrobelli, A. et al. Body mass index as a phenotypic expression of adiposity: quantitative contribution of muscularity in a population-based sample. Int J Obes 33, 1363–1373 (2009). https://doi.org/10.1038/ijo.2009.184

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ijo.2009.184

Keywords

This article is cited by

Search

Quick links