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Fat-free mass and glucose homeostasis: is greater fat-free mass an independent predictor of insulin resistance?

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Abstract

Background

A greater fat-free mass (FFM) is purported to be associated with protective effects on insulin resistance (IR). However, recent studies suggested negative associations between FFM and IR.

Objectives

(1) To explore the direction of the association between FFM and IR in a large heterogeneous sample after controlling for confounding factors. (2) To determine cut off values of FFM associated with an increased risk of IR.

Methods

Outcome variables were measured in 7044 individuals (48.6% women, 20–79 years; NHANES, 1999–2006): body composition [fat mass (FM), FFM and appendicular FFM (aFFM); DXA], FFM index [FFMI: FFM/height (kg/m2)], appendicular FFMI [aFFM/height (kg/m2)] and insulin resistance (HOMA-IR). Multivariate regression analyses were performed to determine the independent predictors of HOMA-IR in younger (20–49 years) and older (50–79 years) men and women. ROC analyses were used to determine FFM cut-offs to identify a higher risk of insulin resistance (HOMA-IR > 75th percentile).

Results

aFFMI was an independent predictor of IR in younger (men: β = 0.21; women: β = 0.31; all p ≤ 0.001) and older (men: β = 0.11; women: β = 0.37; all p ≤ 0.001) individuals. Thresholds for aFFMI at which the risk of IR was significantly increased were 8.96 and 8.39 kg/m2 in younger and older men, and 7.22 and 6.64 kg/m2 in younger and older women, respectively.

Conclusion

Independently of age, a greater aFFMI was an independent predictor of IR. These results suggest revisiting how we envision the link between FFM and IR and explore potential mechanisms.

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References

  1. Cameron AJ, Shaw JE, Zimmet PZ (2004) The metabolic syndrome: prevalence in worldwide populations. Endocrinol Metab Clin N Am 33:351–375

    Article  Google Scholar 

  2. Balkau B et al (2003) The incidence and persistence of the NCEP (National Cholesterol Education Program) metabolic syndrome. The French D.E.S.I.R. study. Diabetes Metab 29:526–532

    Article  PubMed  CAS  Google Scholar 

  3. Pararasa C, Bailey CJ, Griffiths HR (2015) Ageing, adipose tissue, fatty acids and inflammation. Biogerontology 16:235–248

    Article  PubMed  CAS  Google Scholar 

  4. Lipscombe LL, Hux JE (2007) Trends in diabetes prevalence, incidence, and mortality in Ontario, Canada 1995–2005: a population-based study. Lancet 369:750–756

    Article  PubMed  Google Scholar 

  5. Cleasby ME, Jamieson PM, Atherton PJ (2016) Insulin resistance and sarcopenia: mechanistic links between common co-morbidities. J Endocrinol 229:R67–R81

    Article  PubMed  CAS  Google Scholar 

  6. Yang J (2014) Enhanced skeletal muscle for effective glucose homeostasis. Prog Mol Biol Transl Sci 121:133–163

    Article  PubMed  CAS  Google Scholar 

  7. Miller WJ, Sherman WM, Ivy JL (1984) Effect of strength training on glucose tolerance and post-glucose insulin response. Med Sci Sports Exerc 16:539–543

    PubMed  CAS  Google Scholar 

  8. Szczypaczewska M, Nazar K, Kaciuba-Uscilko H (1989) Glucose tolerance and insulin response to glucose load in body builders. Int J Sports Med 10:34–37

    Article  PubMed  CAS  Google Scholar 

  9. Albright A et al (2000) American College of Sports Medicine position stand. Exercise and type 2 diabetes. Med Sci Sports Exerc 32:1345–1360

    Article  PubMed  CAS  Google Scholar 

  10. Canadian Diabetes Association Clinical Practice Guidelines Expert (2013) Physical activity and diabetes. Can J Diabetes 37:S40–S44

    Google Scholar 

  11. Perreault K et al (2016) Association between fat free mass and glucose homeostasis: common knowledge revisited. Ageing Res Rev 28:46–61

    Article  PubMed  Google Scholar 

  12. Aubertin-Leheudre M et al (2006) Effect of sarcopenia on cardiovascular disease risk factors in obese postmenopausal women. Obesity (Silver Spring) 14:2277–2283

    Article  Google Scholar 

  13. Goulet ED et al (2007) No difference in insulin sensitivity between healthy postmenopausal women with or without sarcopenia: a pilot study. Appl Physiol Nutr Metab 32:426–433

    Article  PubMed  CAS  Google Scholar 

  14. Barsalani R, Brochu M, Dionne IJ (2013) Is there a skeletal muscle mass threshold associated with the deterioration of insulin sensitivity in sedentary lean to obese postmenopausal women? Diabetes Res Clin Pract 102:123–128

    Article  PubMed  CAS  Google Scholar 

  15. Brochu M et al (2008) Contribution of the lean body mass to insulin resistance in postmenopausal women with visceral obesity: a Monet study. Obesity (Silver Spring) 16:1085–1093

    Article  CAS  Google Scholar 

  16. Lebon J et al (2012) Is a small muscle mass index really detrimental for insulin sensitivity in postmenopausal women of various body composition status? J Musculoskelet Neuronal Interact 12:116–126

    PubMed  CAS  Google Scholar 

  17. Goulet ED et al (2009) Frailty in the elderly is associated with insulin resistance of glucose metabolism in the postabsorptive state only in the presence of increased abdominal fat. Exp Gerontol 44:740–744

    Article  PubMed  CAS  Google Scholar 

  18. Glouzon BK et al (2015) Muscle mass and insulin sensitivity in postmenopausal women after 6-month exercise training. Climacteric 18:846–851

    Article  PubMed  CAS  Google Scholar 

  19. Myette-Cote E et al (2015) Changes in glucose disposal after a caloric restriction-induced weight loss program in obese postmenopausal women: characteristics of positive and negative responders in a Montreal–Ottawa New Emerging Team study. Menopause 22:96–103

    Article  PubMed  Google Scholar 

  20. Kuk JL et al (2008) Whole-body skeletal muscle mass is not related to glucose tolerance or insulin sensitivity in overweight and obese men and women. Appl Physiol Nutr Metab 33:769–774

    Article  PubMed  CAS  Google Scholar 

  21. Curtin LR et al (2012) The National Health and Nutrition Examination Survey: sample design, 1999–2006. Vital Health Stat 2:1–39

    Google Scholar 

  22. Hoaglin DC, Iglewicz B (1987) Fine-tuning some resistant rules for outlier labeling. J Am Stat Assoc 82:1147–1149

    Article  Google Scholar 

  23. Hoaglin DC, Iglewicz B, Tukey JW (1986) Performance of some resistant rules for outlier labeling. J Am Stat Assoc 81:991–999

    Article  Google Scholar 

  24. Deschenes MR (2004) Effects of aging on muscle fibre type and size. Sports Med 34:809–824

    Article  PubMed  Google Scholar 

  25. Karelis AD et al (2005) The metabolically healthy but obese individual presents a favorable inflammation profile. J Clin Endocrinol Metab 90:4145–4150

    Article  PubMed  CAS  Google Scholar 

  26. Schutz Y, Kyle UU, Pichard C (2002) Fat-free mass index and fat mass index percentiles in Caucasians aged 18–98 y. Int J Obes Relat Metab Disord 26:953–960

    Article  PubMed  CAS  Google Scholar 

  27. Kyle UG et al (2003) Body composition interpretation. Contributions of the fat-free mass index and the body fat mass index. Nutrition 19:597–604

    Article  PubMed  Google Scholar 

  28. Kyle UG et al (2004) Aging, physical activity and height-normalized body composition parameters. Clin Nutr 23:79–88

    Article  PubMed  Google Scholar 

  29. Brochu M et al (1999) Are aerobically fit older individuals more physically active in their free-living time? A doubly labeled water approach. J Clin Endocrinol Metab 84:3872–3876

    PubMed  CAS  Google Scholar 

  30. Gallagher D et al (1997) Appendicular skeletal muscle mass: effects of age, gender, and ethnicity. J Appl Physiol (1985) 83:229–239

    Article  CAS  Google Scholar 

  31. Prevention Cf.D.C.a. and N.C.f.H. Statistic (2017) National Health and Nutrition Examination Survey (NHANES) Questionnaire (or examination protocol, or laboratory protocol) 2011–2012. https://wwwn.cdc.gov/nchs/nhanes/ContinuousNhanes/Default.aspx?BeginYear=2011. Accessed 14 Dec 2017

  32. Willi C et al (2007) Active smoking and the risk of type 2 diabetes: a systematic review and meta-analysis. JAMA 298:2654–2664

    Article  PubMed  CAS  Google Scholar 

  33. Carlsson S, Hammar N, Grill V (2005) Alcohol consumption and type 2 diabetes meta-analysis of epidemiological studies indicates a U-shaped relationship. Diabetologia 48:1051–1054

    Article  PubMed  CAS  Google Scholar 

  34. Marin P et al (1994) Muscle fiber composition and capillary density in women and men with NIDDM. Diabetes Care 17:382–386

    Article  PubMed  CAS  Google Scholar 

  35. Nyholm B et al (1997) Evidence of an increased number of type IIb muscle fibers in insulin-resistant first-degree relatives of patients with NIDDM. Diabetes 46:1822–1828

    Article  PubMed  CAS  Google Scholar 

  36. Prior SJ et al (2009) Reduced skeletal muscle capillarization and glucose intolerance. Microcirculation 16:203–212

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  37. Lillioja S et al (1987) Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Investig 80:415–424

    Article  PubMed  CAS  Google Scholar 

  38. Snijders T et al (2017) Muscle fiber capillarization as determining factor on indices of insulin sensitivity in humans. Physiol Rep 5:e13278

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  39. Goodpaster BH et al (2000) Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 49:467–472

    Article  PubMed  CAS  Google Scholar 

  40. Roden M (2004) How free fatty acids inhibit glucose utilization in human skeletal muscle. News Physiol Sci 19:92–96

    PubMed  CAS  Google Scholar 

  41. Summers SA (2006) Ceramides in insulin resistance and lipotoxicity. Prog Lipid Res 45:42–72

    Article  PubMed  CAS  Google Scholar 

  42. Addison O et al (2014) Intermuscular fat: a review of the consequences and causes. Int J Endocrinol 2014:309570

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  43. Park SW et al (2009) Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care 32:1993–1997

    Article  PubMed  PubMed Central  Google Scholar 

  44. Lee CG et al (2011) Insulin sensitizers may attenuate lean mass loss in older men with diabetes. Diabetes Care 34:2381–2386

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  45. Park SW et al (2007) Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: the health, aging, and body composition study. Diabetes Care 30:1507–1512

    Article  PubMed  Google Scholar 

  46. Atlantis E et al (2009) Inverse associations between muscle mass, strength, and the metabolic syndrome. Metabolism 58:1013–1022

    Article  PubMed  CAS  Google Scholar 

  47. Kalyani RR et al (2012) Glucose and insulin measurements from the oral glucose tolerance test and relationship to muscle mass. J Gerontol A Biol Sci Med Sci 67:74–81

    Article  PubMed  CAS  Google Scholar 

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Author information

Author notes

  1. Ahmed Ghachem and Jean-Christophe Lagacé contributed equally to this work.

Authors and Affiliations

  1. Faculty of Physical Activity Sciences, University of Sherbrooke, 2500, Boul. de l’Université, Sherbrooke, QC, J1K2R1, Canada

    Ahmed Ghachem, Jean-Christophe Lagacé, Martin Brochu & Isabelle J. Dionne

  2. Research Centre on Aging, Social Services and Health Centre, University Institute of Geriatrics of Sherbrooke, 1036, Belvédère Sud, Sherbrooke, QC, J1H 4C4, Canada

    Ahmed Ghachem, Jean-Christophe Lagacé, Martin Brochu & Isabelle J. Dionne

Authors
  1. Ahmed Ghachem
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  2. Jean-Christophe Lagacé
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  3. Martin Brochu
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  4. Isabelle J. Dionne
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Contributions

A.G and J-C.L, both contributed to the review of literature, database design, statistical analysis, interpretation of the data and drafting of the manuscript. M.B and I.D contributed to the drafting and revision of the manuscript. All of the authors approved the final manuscript prior to submission and they are guarantors of this work and take responsibility for the integrity of the data and the accuracy of the data analysis.

Corresponding author

Correspondence to Isabelle J. Dionne.

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All authors declare no conflict of interest.

Ethical approval

The protocol was approved by the National Center for Health Statistics.

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All participants provided written and informed consent.

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Ghachem, A., Lagacé, JC., Brochu, M. et al. Fat-free mass and glucose homeostasis: is greater fat-free mass an independent predictor of insulin resistance?. Aging Clin Exp Res 31, 447–454 (2019). https://doi.org/10.1007/s40520-018-0993-y

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  • DOI: https://doi.org/10.1007/s40520-018-0993-y

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