Endocrinol Metab.  2017 Jun;32(2):257-264. 10.3803/EnM.2017.32.2.257.

Intermuscular Adipose Tissue Content and Intramyocellular Lipid Fatty Acid Saturation Are Associated with Glucose Homeostasis in Middle-Aged and Older Adults

Affiliations
  • 1Department of Nutrition Science, Purdue University College of Health and Human Sciences, West Lafayette, IN, USA. campbellw@purdue.edu
  • 2Department of Chemistry, Purdue University College of Science, West Lafayette, IN, USA.
  • 3Weldon School of Biomedical Engineering, Purdue University College of Engineering, West Lafayette, IN, USA.

Abstract

BACKGROUND
Insulin resistance is associated with the higher content of intermuscular adipose tissue (IMAT) and the saturation of intramyocellular lipid (IMCL), but a paucity of data exist in humans. This study examined associations among IMAT content, IMCL saturation, and fasting glucose concentration in middle-aged and older adults with overweight or obesity.
METHODS
Seventy-five subjects (26 males, 49 females) were recruited and thigh muscle and IMAT were assessed using magnetic resonance imaging. Vastus lateralis tissue was acquired from a subset of nine subjects and IMCL content and saturation were assessed using nonlinear dual complex microscopy.
RESULTS
The characteristics of the 75 subjects were as follows: age 59±11 years, body mass index 30±5 kg/m², fasting glucose concentration 5.2±0.5 mmol/L, fasting insulin concentration 12.2±7.3 µU/mL, fasting homeostatic model assessment of insulin resistance (HOMA-IR) 2.9±2.0 (mean±SD). IMAT to muscle tissue (MT) volume ratio was positively associated with the saturated fatty acid to unsaturated fatty acid ratio in IMCL. IMAT:MT was positively associated with fasting glucose concentration and HOMA-IR. IMCL saturation was positively associated with fasting glucose concentration while muscle cell area, IMCL area, and % IMCL in muscle cell were not associated with fasting glucose concentration.
CONCLUSION
These results indicate that higher intermuscular fat content and IMCL saturation may impact fasting glucose concentration in middle-aged and older adults with overweight or obesity. The centralization of adipose tissue in the appendicular region of the body may promote insulin resistance.

Keyword

Glucose homeostasis; Intermuscular adipose tissue; Intramyocellular lipid; Overweight and obesity; Middle-aged and older adults

MeSH Terms

Adipose Tissue*
Adult*
Body Mass Index
Fasting
Glucose*
Homeostasis*
Humans
Insulin
Insulin Resistance
Magnetic Resonance Imaging
Male
Microscopy
Muscle Cells
Obesity
Overweight
Quadriceps Muscle
Thigh
Glucose
Insulin

Reference

1. Trombetti A, Reid KF, Hars M, Herrmann FR, Pasha E, Phillips EM, et al. Age-associated declines in muscle mass, strength, power, and physical performance: impact on fear of falling and quality of life. Osteoporos Int. 2016; 27:463–471. PMID: 26194491.
Article
2. Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA. 2014; 311:806–814. PMID: 24570244.
Article
3. Bjorntorp P. Abdominal obesity and the development of noninsulin-dependent diabetes mellitus. Diabetes Metab Rev. 1988; 4:615–622. PMID: 3065014.
4. Coen PM, Goodpaster BH. Role of intramyocelluar lipids in human health. Trends Endocrinol Metab. 2012; 23:391–398. PMID: 22721584.
Article
5. Goodpaster BH, Thaete FL, Kelley DE. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr. 2000; 71:885–892. PMID: 10731493.
Article
6. Manco M, Mingrone G, Greco AV, Capristo E, Gniuli D, De Gaetano A, et al. Insulin resistance directly correlates with increased saturated fatty acids in skeletal muscle triglycerides. Metabolism. 2000; 49:220–224. PMID: 10690948.
Article
7. Pan DA, Lillioja S, Milner MR, Kriketos AD, Baur LA, Bogardus C, et al. Skeletal muscle membrane lipid composition is related to adiposity and insulin action. J Clin Invest. 1995; 96:2802–2808. PMID: 8675650.
Article
8. Vessby B, Tengblad S, Lithell H. Insulin sensitivity is related to the fatty acid composition of serum lipids and skeletal muscle phospholipids in 70-year-old men. Diabetologia. 1994; 37:1044–1050. PMID: 7851683.
Article
9. Li Y, Xu S, Zhang X, Yi Z, Cichello S. Skeletal intramyocellular lipid metabolism and insulin resistance. Biophys Rep. 2015; 1:90–98. PMID: 26942223.
Article
10. Pfeffer CP, Olsen BR, Ganikhanov F, Legare F. Imaging skeletal muscle using second harmonic generation and coherent anti-stokes Raman scattering microscopy. Biomed Opt Express. 2011; 2:1366–1376. PMID: 21559148.
Article
11. Brackmann C, Esguerra M, Olausson D, Delbro D, Krettek A, Gatenholm P, et al. Coherent anti-stokes Raman scattering microscopy of human smooth muscle cells in bioengineered tissue scaffolds. J Biomed Opt. 2011; 16:021115. PMID: 21361678.
Article
12. Day JP, Rago G, Domke KF, Velikov KP, Bonn M. Label-free imaging of lipophilic bioactive molecules during lipid digestion by multiplex coherent anti-stokes Raman scattering microspectroscopy. J Am Chem Soc. 2010; 132:8433–8439. PMID: 20507119.
Article
13. Hellerer T, Axang C, Brackmann C, Hillertz P, Pilon M, Enejder A. Monitoring of lipid storage in Caenorhabditis elegans using coherent anti-stokes Raman scattering (CARS) microscopy. Proc Natl Acad Sci U S A. 2007; 104:14658–14663. PMID: 17804796.
Article
14. Billecke N, Rago G, Bosma M, Eijkel G, Gemmink A, Leproux P, et al. Chemical imaging of lipid droplets in muscle tissues using hyperspectral coherent Raman microscopy. Histochem Cell Biol. 2014; 141:263–273. PMID: 24186059.
Article
15. Evans CL, Xie XS. Coherent anti-stokes Raman scattering microscopy: chemical imaging for biology and medicine. Annu Rev Anal Chem (Palo Alto Calif). 2008; 1:883–909. PMID: 20636101.
Article
16. Slipchenko MN, Le TT, Chen H, Cheng JX. High-speed vibrational imaging and spectral analysis of lipid bodies by compound Raman microscopy. J Phys Chem B. 2009; 113:7681–7686. PMID: 19422201.
Article
17. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985; 28:412–419. PMID: 3899825.
18. Berg HE, Tedner B, Tesch PA. Changes in lower limb muscle cross-sectional area and tissue fluid volume after transition from standing to supine. Acta Physiol Scand. 1993; 148:379–385. PMID: 8213193.
Article
19. Lund H, Christensen L, Savnik A, Boesen J, Danneskiold-Samsoe B, Bliddal H. Volume estimation of extensor muscles of the lower leg based on MR imaging. Eur Radiol. 2002; 12:2982–2987. PMID: 12439580.
Article
20. Tuttle LJ, Sinacore DR, Mueller MJ. Intermuscular adipose tissue is muscle specific and associated with poor functional performance. J Aging Res. 2012; 2012:172957. PMID: 22666591.
Article
21. Thalacker-Mercer AE, Fleet JC, Craig BA, Campbell WW. The skeletal muscle transcript profile reflects accommodative responses to inadequate protein intake in younger and older males. J Nutr Biochem. 2010; 21:1076–1082. PMID: 20149619.
Article
22. Johannsen DL, Conley KE, Bajpeyi S, Punyanitya M, Gallagher D, Zhang Z, et al. Ectopic lipid accumulation and reduced glucose tolerance in elderly adults are accompanied by altered skeletal muscle mitochondrial activity. J Clin Endocrinol Metab. 2012; 97:242–250. PMID: 22049170.
Article
23. Karakelides H, Irving BA, Short KR, O'Brien P, Nair KS. Age, obesity, and sex effects on insulin sensitivity and skeletal muscle mitochondrial function. Diabetes. 2010; 59:89–97. PMID: 19833885.
Article
24. Kuk JL, Saunders TJ, Davidson LE, Ross R. Age-related changes in total and regional fat distribution. Ageing Res Rev. 2009; 8:339–348. PMID: 19576300.
Article
25. Addison O, Marcus RL, Lastayo PC, Ryan AS. Intermuscular fat: a review of the consequences and causes. Int J Endocrinol. 2014; 2014:309570. PMID: 24527032.
Article
26. Boettcher M, Machann J, Stefan N, Thamer C, Haring HU, Claussen CD, et al. Intermuscular adipose tissue (IMAT): association with other adipose tissue compartments and insulin sensitivity. J Magn Reson Imaging. 2009; 29:1340–1345. PMID: 19422021.
Article
27. Yim JE, Heshka S, Albu J, Heymsfield S, Kuznia P, Harris T, et al. Intermuscular adipose tissue rivals visceral adipose tissue in independent associations with cardiovascular risk. Int J Obes (Lond). 2007; 31:1400–1405. PMID: 17452994.
Article
28. Zoico E, Rossi A, Di Francesco V, Sepe A, Olioso D, Pizzini F, et al. Adipose tissue infiltration in skeletal muscle of healthy elderly men: relationships with body composition, insulin resistance, and inflammation at the systemic and tissue level. J Gerontol A Biol Sci Med Sci. 2010; 65:295–299. PMID: 19864639.
Article
29. Straczkowski M, Kowalska I, Baranowski M, Nikolajuk A, Otziomek E, Zabielski P, et al. Increased skeletal muscle ceramide level in men at risk of developing type 2 diabetes. Diabetologia. 2007; 50:2366–2373. PMID: 17724577.
Article
30. Itani SI, Ruderman NB, Schmieder F, Boden G. Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes. 2002; 51:2005–2011. PMID: 12086926.
31. Pickersgill L, Litherland GJ, Greenberg AS, Walker M, Yeaman SJ. Key role for ceramides in mediating insulin resistance in human muscle cells. J Biol Chem. 2007; 282:12583–12589. PMID: 17337731.
Article
32. Lee JS, Pinnamaneni SK, Eo SJ, Cho IH, Pyo JH, Kim CK, et al. Saturated, but not n-6 polyunsaturated, fatty acids induce insulin resistance: role of intramuscular accumulation of lipid metabolites. J Appl Physiol (1985). 2006; 100:1467–1474. PMID: 16357064.
Article
33. Haugaard SB, Madsbad S, Mu H, Vaag A. Desaturation of excess intramyocellular triacylglycerol in obesity: implications for glycemic control. Int J Obes (Lond). 2010; 34:500–510. PMID: 20029372.
Article
34. Ibrahim MM. Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev. 2010; 11:11–18. PMID: 19656312.
Article
35. Preis SR, Massaro JM, Robins SJ, Hoffmann U, Vasan RS, Irlbeck T, et al. Abdominal subcutaneous and visceral adipose tissue and insulin resistance in the Framingham heart study. Obesity (Silver Spring). 2010; 18:2191–2198. PMID: 20339361.
Article
36. Hayashi T, Boyko EJ, McNeely MJ, Leonetti DL, Kahn SE, Fujimoto WY. Visceral adiposity, not abdominal subcutaneous fat area, is associated with an increase in future insulin resistance in Japanese Americans. Diabetes. 2008; 57:1269–1275. PMID: 18299316.
Article
37. Wagenknecht LE, Langefeld CD, Scherzinger AL, Norris JM, Haffner SM, Saad MF, et al. Insulin sensitivity, insulin secretion, and abdominal fat: the Insulin Resistance Atherosclerosis Study (IRAS) Family Study. Diabetes. 2003; 52:2490–2496. PMID: 14514631.
38. Velan SS, Said N, Narasimhan K, Papan C, Bahu A, Vargo JA, et al. Gender differences in musculoskeletal lipid metabolism as assessed by localized two-dimensional correlation spectroscopy. Magn Reson Insights. 2008; 2008:1–6. PMID: 25371653.
Article
39. Horstman AM, Dillon EL, Urban RJ, Sheffield-Moore M. The role of androgens and estrogens on healthy aging and longevity. J Gerontol A Biol Sci Med Sci. 2012; 67:1140–1152. PMID: 22451474.
Article
40. Le TT, Yue S, Cheng JX. Shedding new light on lipid biology with coherent anti-stokes Raman scattering microscopy. J Lipid Res. 2010; 51:3091–3102. PMID: 20713649.
Article
Full Text Links
  • ENM
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr