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The effects of muscle mass and muscle quality on cardio-metabolic risk in peripubertal girls: a longitudinal study from childhood to early adulthood

International Journal of Obesity volume 42, pages 648–654 (2018)Cite this article

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Abstract

Background:

Increased cardio-metabolic risk is well documented in children and adolescents with obesity and normal weight obesity (NWO). However, the associations of muscle mass and muscle quality with cardio-metabolic risk, independent of weight status from childhood to adulthood, has not been examined.

Methods:

A total of 236 girls were followed from pre-puberty to early adulthood. Fat mass (FM) and lean mass (LM) of the whole body were assessed by a dual-energy X-ray absorptiometry; muscle cross-sectional area (mCSA), muscle density (mDen; skeletal muscle fat content) of the lower leg by the peripheral quantitative computerized tomography; and blood glucose, insulin, triglycerides and high-density lipoprotein cholesterol by enzymatic photometric methods. Study participants were categorized based on body mass index (BMI) and percentage body fat (%BF) as overweight and/or obese (BMI⩾30 with %BF⩾30), normal weight obese (BMI 18.5–24.9 with %BF⩾30) and normal weight lean (BMI 18.5–24.9 with %BF <30).

Results:

Girls with overweight and/or obesity from age of 11 to age 18 had greater LM and larger mCSA, but lower mDen and skeletal muscle mass index than the normal-weight girls (P<0.001 for all). Girls with NWO had similar mCSA and muscle mass but lower mDen and skeletal muscle index (SMI) than their normal-weight lean peers from childhood to early adulthood (P<0.001 all). In all girls, mDen and SMI were inversely associated with cardio-metabolic risk score (r2=0.012, P<0.05 and r2=0.201, P<0.001, respectively). However, after adjusting for whole-body FM or android abdominal FM, all associations disappeared.

Conclusions:

Skeletal muscle size and muscle mass are not associated with cardio-metabolic risk factors during pubertal growth after adjusting for measures of adiposity. Ectopic fat accumulation in the skeletal muscle and increased adiposity, particularly in the abdominal area in childhood, are significant contributors to increased cardio-metabolic risk in adulthood, irrespective of body weight status.

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References

  1. Juonala M, Magnussen CG, Berenson GS, Venn A, Burns TL, Sabin MA et al. Childhood adiposity, adult adiposity, and cardiovascular risk factors. N Engl J Med 2011; 365: 1876–1885.

    Article  CAS  Google Scholar 

  2. Franks PW, Hanson RL, Knowler WC, Sievers ML, Bennett PH, Looker HC . Childhood obesity, other cardiovascular risk factors, and premature death. N Engl J Med 2010; 362: 485–493.

    Article  CAS  Google Scholar 

  3. Raitakari OT, Juonala M, Viikari JS . Obesity in childhood and vascular changes in adulthood: insights into the Cardiovascular Risk in Young Finns Study. Int J Obes 2005; 29 (Suppl 2): S101–S104.

    Article  Google Scholar 

  4. Flegal KM, Ogden CL . Childhood obesity: are we all speaking the same language? Adv Nutr 2011; 2: 159S–166SS.

    Article  Google Scholar 

  5. Chinn S . Definitions of childhood obesity: current practice. Eur J Clin Nutr 2006; 60: 1189–1194.

    Article  CAS  Google Scholar 

  6. Garn SM, Leonard WR, Hawthorne VM . Three limitations of the body mass index. Am J Clin Nutr 1986; 44: 996–997.

    Article  CAS  Google Scholar 

  7. Javed A, Jumean M, Murad MH, Okorodudu D, Kumar S, Somers VK et al. Diagnostic performance of body mass index to identify obesity as defined by body adiposity in children and adolescents: a systematic review and meta-analysis. Pediatr Obes 2015; 10: 234–244.

    Article  CAS  Google Scholar 

  8. Wiklund P, Tormakangas T, Shi Y, Wu N, Vainionpaa A, Alen M et al. Normal-weight obesity and cardiometabolic risk: a 7-year longitudinal study in girls from prepuberty to early adulthood. Obesity 2017; 25: 1077–1082.

    Article  CAS  Google Scholar 

  9. Madeira FB, Silva AA, Veloso HF, Goldani MZ, Kac G, Cardoso VC et al. Normal weight obesity is associated with metabolic syndrome and insulin resistance in young adults from a middle-income country. PLoS One 2013; 8: e60673.

    Article  CAS  Google Scholar 

  10. Romero-Corral A, Somers VK, Sierra-Johnson J, Korenfeld Y, Boarin S, Korinek J et al. Normal weight obesity: a risk factor for cardiometabolic dysregulation and cardiovascular mortality. Eur Heart J 2010; 31: 737–746.

    Article  Google Scholar 

  11. Batsis JA, Sahakyan KR, Rodriguez-Escudero JP, Bartels SJ, Somers VK, Lopez-Jimenez F . Normal weight obesity and mortality in United States subjects &gt;/=60 years of age (from the Third National Health and Nutrition Examination Survey). Am J Cardiol 2013; 112: 1592–1598.

    Article  Google Scholar 

  12. Wolfe RR . The underappreciated role of muscle in health and disease. Am J Clin Nutr 2006; 84: 475–482.

    Article  CAS  Google Scholar 

  13. Coen PM, Dube JJ, Amati F, Stefanovic-Racic M, Ferrell RE, Toledo FG et al. Insulin resistance is associated with higher intramyocellular triglycerides in type I but not type II myocytes concomitant with higher ceramide content. Diabetes 2010; 59: 80–88.

    Article  CAS  Google Scholar 

  14. McGregor RA, Cameron-Smith D, Poppitt SD . It is not just muscle mass: a review of muscle quality, composition and metabolism during ageing as determinants of muscle function and mobility in later life. Longev Healthspan 2014; 3: 9.

    Article  Google Scholar 

  15. Wells JC . Sexual dimorphism of body composition. Best Pract Res Clin Endocrinol Metab 2007; 21: 415–430.

    Article  Google Scholar 

  16. Guo SS, Wu W, Chumlea WC, Roche AF . Predicting overweight and obesity in adulthood from body mass index values in childhood and adolescence. Am J Clin Nutr 2002; 76: 653–658.

    Article  CAS  Google Scholar 

  17. Baker JL, Olsen LW, Sorensen TI . Childhood body-mass index and the risk of coronary heart disease in adulthood. N Engl J Med 2007; 357: 2329–2337.

    Article  CAS  Google Scholar 

  18. Xu L, Nicholson P, Wang Q, Alen M, Cheng S . Bone and muscle development during puberty in girls: a seven-year longitudinal study. J Bone Miner Res 2009; 24: 1693–1698.

    Article  Google Scholar 

  19. Cheng S, Volgyi E, Tylavsky FA, Lyytikainen A, Tormakangas T, Xu L et al. Trait-specific tracking and determinants of body composition: a 7-year follow-up study of pubertal growth in girls. BMC Med 2009; 7: 5.

    Article  Google Scholar 

  20. Volgyi E, Alen M, Xu L, Lyytikainen A, Wang Q, Munukka E et al. Effect of long-term leisure time physical activity on lean mass and fat mass in girls during adolescence. J Appl Physiol 2011; 110: 1211–1218.

    Article  Google Scholar 

  21. Janssen I, Heymsfield SB, Ross R . Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 2002; 50: 889–896.

    Article  Google Scholar 

  22. De Lorenzo A, Martinoli R, Vaia F, Di Renzo L . Normal weight obese (NWO) women: an evaluation of a candidate new syndrome. Nutr Metab Cardiovasc Dis 2006; 16: 513–523.

    Article  CAS  Google Scholar 

  23. Goldstein H . Efficient statistical modelling of longitudinal data. Ann Hum Biol 1986; 13: 129–141.

    Article  CAS  Google Scholar 

  24. Chiarelli F, Marcovecchio ML . Insulin resistance and obesity in childhood. Eur J Endocrinol 2008; 159 (Suppl 1): S67–S74.

    Article  CAS  Google Scholar 

  25. Weiss R, Kaufman FR . Metabolic complications of childhood obesity: identifying and mitigating the risk. Diabetes Care 2008; 31 (Suppl 2): S310–S316.

    Article  Google Scholar 

  26. Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY et al. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation 2007; 116: 39–48.

    Article  Google Scholar 

  27. Kim BC, Kim MK, Han K, Lee SY, Lee SH, Ko SH et al. Low muscle mass is associated with metabolic syndrome only in nonobese young adults: the Korea National Health and Nutrition Examination Survey 2008-2010. Nutr Res 2015; 35: 1070–1078.

    Article  CAS  Google Scholar 

  28. Kim JH, Park YS . Low muscle mass is associated with metabolic syndrome in Korean adolescents: the Korea National Health and Nutrition Examination Survey 2009-2011. Nutr Res 2016; 36: 1423–1428.

    Article  CAS  Google Scholar 

  29. Moon SS . Low skeletal muscle mass is associated with insulin resistance, diabetes, and metabolic syndrome in the Korean population: the Korea National Health and Nutrition Examination Survey (KNHANES) 2009-2010. Endocr J 2014; 61: 61–70.

    Article  CAS  Google Scholar 

  30. Srikanthan P, Karlamangla AS . Relative muscle mass is inversely associated with insulin resistance and prediabetes. Findings from the third National Health and Nutrition Examination Survey. J Clin Endocrinol Metab 2011; 96: 2898–2903.

    Article  CAS  Google Scholar 

  31. Tomlinson DJ, Erskine RM, Morse CI, Winwood K, Onambele-Pearson G . The impact of obesity on skeletal muscle strength and structure through adolescence to old age. Biogerontology 2016; 17: 467–483.

    Article  CAS  Google Scholar 

  32. Barbat-Artigas S, Filion ME, Plouffe S, Aubertin-Leheudre M . Muscle quality as a potential explanation of the metabolically healthy but obese and sarcopenic obese paradoxes. Metab Syndr Relat Disord 2012; 10: 117–122.

    Article  Google Scholar 

  33. Bennett B, Larson-Meyer DE, Ravussin E, Volaufova J, Soros A, Cefalu WT et al. Impaired insulin sensitivity and elevated ectopic fat in healthy obese vs. nonobese prepubertal children. Obesity 2012; 20: 371–375.

    Article  CAS  Google Scholar 

  34. Larson-Meyer DE, Newcomer BR, Ravussin E, Volaufova J, Bennett B, Chalew S et al. Intrahepatic and intramyocellular lipids are determinants of insulin resistance in prepubertal children. Diabetologia 2011; 54: 869–875.

    Article  CAS  Google Scholar 

  35. Fonvig CE, Bille DS, Chabanova E, Nielsen TR, Thomsen HS, Holm JC . Muscle fat content and abdominal adipose tissue distribution investigated by magnetic resonance spectroscopy and imaging in obese children and youths. Pediatr Rep 2012; 4: e11.

    Article  Google Scholar 

  36. Weiss R, Dufour S, Taksali SE, Tamborlane WV, Petersen KF, Bonadonna RC et al. Prediabetes in obese youth: a syndrome of impaired glucose tolerance, severe insulin resistance, and altered myocellular and abdominal fat partitioning. Lancet 2003; 362: 951–957.

    Article  CAS  Google Scholar 

  37. Virtue S, Vidal-Puig A . Adipose tissue expandability, lipotoxicity and the metabolic syndrome—an allostatic perspective. Biochim Biophys Acta 2010; 1801: 338–349.

    Article  CAS  Google Scholar 

  38. Graves L, Garnett SP, Cowell CT, Baur LA, Ness A, Sattar N et al. Waist-to-height ratio and cardiometabolic risk factors in adolescence: findings from a prospective birth cohort. Pediatr Obes 2014; 9: 327–338.

    Article  CAS  Google Scholar 

  39. Brambilla P, Bedogni G, Heo M, Pietrobelli A . Waist circumference-to-height ratio predicts adiposity better than body mass index in children and adolescents. Int J Obes 2013; 37: 943–946.

    Article  CAS  Google Scholar 

  40. Schmidt MD, Dwyer T, Magnussen CG, Venn AJ . Predictive associations between alternative measures of childhood adiposity and adult cardio-metabolic health. Int J Obes 2011; 35: 38–45.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported financially by the Academy of Finland (Grant 24302031 and 135038), the University of Jyväskylä, Finland, the National Nature Science Foundation of China (Grant 31571219) and the Shanghai Jiao Tong University Zhiyuan Foundation (Grant CP2014013).

Author Contributions

SC and PW designed the study, participated in data collection and analyzed data and wrote the manuscript. Both authors read and approved the final manuscript.

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Authors and Affiliations

  1. Exercise, Health and Technology Center, Shanghai Jiao Tong University, Shanghai, China

    S Cheng

  2. Faculty of Sport Sciences, University of Jyväskylä, Jyväskylä, Finland

    S Cheng & P Wiklund

  3. The Key Laboratory of Systems Biomedicine, Ministry of Education, Shanghai Center for Systems Biomedicine, Shanghai Jiao Tong University, Shanghai, China

    S Cheng

  4. Department of Epidemiology and Biostatistics, Centre for Environment and Health, School of Public Health, Imperial College London, London, UK

    P Wiklund

  5. Center for Life-Course Health Research, Faculty of Medicine, University of Oulu, Oulu, Finland

    P Wiklund

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Correspondence to P Wiklund.

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Cheng, S., Wiklund, P. The effects of muscle mass and muscle quality on cardio-metabolic risk in peripubertal girls: a longitudinal study from childhood to early adulthood. Int J Obes 42, 648–654 (2018). https://doi.org/10.1038/ijo.2017.267

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