Skeletal muscle capillary density and microvascular function are compromised with aging and type 2 diabetes

Journal of Applied Physiology

Volumn 116, Issue 8, 2014, Pages 998-1005

  Groen, Bart B L ^a   Hamer, Henrike M ^a   Snijders, Tim ^a   Van Kranenburg, Janneau ^a   Frijns, Dionne ^a   Vink, Hans ^b   Van Loon, Luc J C ^a  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Glucose; Insulin; Muscle; SDF technology; Vascularization

Indexed keywords

GLYCOSYLATED HEMOGLOBIN; HEMOGLOBIN A1C PROTEIN, HUMAN;

ADULT; AGED; AGING; CAPILLARY; CASE CONTROL STUDY; CLINICAL TRIAL; GLUCOSE TOLERANCE TEST; GLYCOCALYX; HUMAN; INSULIN RESISTANCE; MALE; METABOLISM; MICROVASCULATURE; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SKELETAL MUSCLE; VASCULAR ENDOTHELIUM; VASCULARIZATION; YOUNG ADULT;

ADULT; AGED; AGING; CAPILLARIES; CASE-CONTROL STUDIES; DIABETES MELLITUS, TYPE 2; ENDOTHELIUM, VASCULAR; GLUCOSE TOLERANCE TEST; GLYCOCALYX; HEMOGLOBIN A, GLYCOSYLATED; HUMANS; INSULIN RESISTANCE; MALE; MICROVESSELS; MUSCLE, SKELETAL; YOUNG ADULT;

EID: 84901236208     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00919.2013     Document Type: Article

References (55)

1. Ainsworth BE, Haskell WL, Herrmann SD, Meckes N, Bassett DR Jr, Tudor-Locke C, Greer JL, Vezina J, Whitt-Glover MC, Leon AS. 2011 Compendium of Physical Activities: a second update of codes and MET values. Med Sci Sports Exerc 43: 1575-1581, 2011.
2. Baron AD. Insulin resistance and vascular function. J Diabetes Complications 16: 92-102, 2002.
3. Bastow MD, Rawlings J, Allison SP. Benefits of supplementary tube feeding after fractured neck of femur: a randomised controlled trial. Br Med J (Clin Res Ed) 287: 1589-1592, 1983.
4. Bell JA, Fujita S, Volpi E, Cadenas JG, Rasmussen BB. Short-term insulin and nutritional energy provision do not stimulate muscle protein synthesis if blood amino acid availability decreases. Am J Physiol Endo-crinol Metab 289: E999-E1006, 2005.
5. Boer C, Koning N, Van Teeffelen J, Vonk A, Vink H. Changes in microcirculatory perfusion during cardiac surgery are paralleled by alterations in glycocalyx integrity. Critical Care 17: 2013.
6. Brandes R, Fleming I, Busse R. Endothelial aging. Cardiovasc Res 66: 286-294, 2005.
7. Broekhuizen LN, Lemkes BA, Mooij HL, Meuwese MC, Verberne H, Holleman F, Schlingemann RO, Nieuwdorp M, Stroes ES, Vink H. Effect of sulodexide on endothelial glycocalyx and vascular permeability in patients with type 2 diabetes mellitus. Diabetologia 53: 2646-2655, 2010.
8. Broekhuizen LN, Mooij HL, Kastelein JJ, Stroes ES, Vink H, Nieuwdorp M. Endothelial glycocalyx as potential diagnostic and therapeutic target in cardiovascular disease. Curr Opin Lipidol 20: 57-62, 2009.
9. Burd NA, Wall BT, van Loon LJ. The curious case of anabolic resistance: old wives' tales or new fables? J Appl Physiol 112: 1233-1235, 2012.
10. Cade W. Diabetes-related microvascular and macrovascular diseases in the physical therapy setting. Phys Ther 88: 1322-1335, 2008.
11. Clark MG. Impaired microvascular perfusion: a consequence of vascular dysfunction and a potential cause of insulin resistance in muscle. Am J Physiol Endocrinol Metab 295: E732-E750, 2008.
12. Cuthbertson D, Smith K, Babraj J, Leese G, Waddell T, Atherton P, Wackerhage H, Taylor PM, Rennie MJ. Anabolic signaling deficits underlie amino acid resistance of wasting, aging muscle. FASEB J 19: 422-424, 2005.
13. De Boer MP, Meijer RI, Wijnstok NJ, Jonk AM, Houben AJ, Stehouwer CD, Smulders YM, Eringa EC, Serne EH. Microvascular dysfunction: a potential mechanism in the pathogenesis of obesity-associated insulin resistance and hypertension. Microcirculation 19: 5-18, 2012.
14. Donati A, Damiani E, Domizi R, Romano R, Adrario E, Pelaia P, Ince C, Singer M. Alteration of the sublingual microvascular glycocalyx in critically ill patients. Microvasc Res 90: 86-89, 2013.
15. Egan B, Zierath J. Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab 17: 162-184, 2013.
16. Eskens BJ, Mooij HL, Cleutjens JP, Roos JM, Cobelens JE, Vink H, Vanteeffelen JW. Rapid insulin-mediated increase in microvascular gly-cocalyx accessibility in skeletal muscle may contribute to insulin-mediated glucose disposal in rats. PLos One 8: e55399, 2013.
17. Fujita S, Glynn EL, Timmerman KL, Rasmussen BB, Volpi E. Sup-raphysiological hyperinsulinaemia is necessary to stimulate skeletal muscle protein anabolism in older adults: evidence of a true age-related insulin resistance of muscle protein metabolism. Diabetologia 52: 1889-1898, 2009.
18. Fujita S, Rasmussen BB, Cadenas JG, Grady JJ, Volpi E. Effect of insulin on human skeletal muscle protein synthesis is modulated by insulin-induced changes in muscle blood flow and amino acid availability. Am J Physiol Endocrinol Metab 291: E745-E754, 2006.
19. Guillet C, Boirie Y. Insulin resistance: a contributing factor to age-related muscle mass loss? Diabetes Metab 31, Spec No 2: 5S20-25S26, 2005.
20. Hepple RT. A new measurement of tissue capillarity: the capillary-to-fibre perimeter exchange index. Can J Appl Physiol: 11-22, 1997.
21. Hepple RT, Mackinnon SL, Goodman JM, Thomas SG, Plyley MJ. Resistance and aerobic training in older men: effects on VO2peak and the capillary supply to skeletal muscle. J Appl Physiol 82: 1305-1310, 1997.
22. 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 50: 889-896, 2002.
23. Katsanos CS, Kobayashi H, Sheffield-Moore M, Aarsland A, Wolfe RR. Aging is associated with diminished accretion of muscle proteins after the ingestion of a small bolus of essential amino acids. Am J Clin Nutr 82: 1065-1073, 2005.
24. Koopman R, van Loon LJ. Aging, exercise, and muscle protein metabolism. J Appl Physiol 106: 2040-2048, 2009.
25. Koopman R, Verdijk LB, Beelen M, Gorselink M, Kruseman AN, Wagenmakers AJ, Kuipers H, van Loon LJ. Co-ingestion of leucine with protein does not further augment post-exercise muscle protein synthesis rates in elderly men. Br J Nutr 99: 571-580, 2008.
26. Larsson L, Sjödin B, Karlsson J. Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22-65 years. Acta Physiol Scand 103: 31-39, 1978.
27. Leenders M, Verdijk L, Van der Hoeven L, Adam J, Van Kranenburg J, Nilwik R, Van Loon LJC. Patients with type 2 diabetes show a greater decline in muscle mass, muscle strength, and functional capacity with aging. J Am Med Dir Assoc 14: 585-592, 2013.
28. Levy JC, Matthews DR, Hermans MP. Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care 21: 2191-2192, 1998.
29. Lillioja S, Young AA, Culter CL, Ivy JL, Abbott WG, Zawadzki JK, Yki-Jarvinen H, Christin L, Secomb TW, Bogardus C. Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest 80: 415-424, 1987.
30. Lima A, Bakker J. Noninvasive monitoring of peripheral perfusion. Intens Care Med 31: 1316-1326, 2005.
31. Luft J. The structure and properties of the cell surface coat. Int Rev Cytol 45: 291-382, 1976.
32. Marin P, Andersson B, Krotkiewski M, Bjorntorp P. Muscle fiber composition and capillary density in women and men with NIDDM. Diabetes Care 17: 382-386, 1994.
33. Martens R, Vink H, van Oostenbrugge R, Staals J. Sublingual micro-vascular glycocalyx dimensions in lacunar stroke patients. Cerebrovasc Dis 35: 451-454, 2013.
34. Meneilly G, Elliot T, Bryer-Ash M, Floras J. Insulin-mediated increase in blood flow is impaired in the elderly. J Clin Endocrinol Metab 80: 1899-1903, 1995.
35. Nieuwdorp M, Meuwese MC, Mooij HL, Ince C, Broekhuizen LN, Kastelein JJ, Stroes ES, Vink H. Measuring endothelial glycocalyx dimensions in humans: a potential novel tool to monitor vascular vulnerability. J Appl Physiol 104: 845-852, 2008.
36. Nieuwdorp M, van Haeften TW, Gouverneur MC, Mooij HL, van Lieshout MH, Levi M, Meijers JC, Holleman F, Hoekstra JB, Vink H, Kastelein JJ, Stroes ES. Loss of endothelial glycocalyx during acute hyperglycemia coincides with endothelial dysfunction and coagulation activation in vivo. Diabetes 55: 480-486, 2006.
37. Nilwik R, Snijders T, Leenders M, Groen B, van Kranenburg J, Verdijk L, van Loon L. The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp Gerontol 48: 492-498, 2013.
38. Park SW, Goodpaster BH, Lee JS, Kuller LH, Boudreau R, de Rekeneire N, Harris TB, Kritchevsky S, Tylavsky FA, Nevitt M, Cho YW, Newman AB. Excessive loss of skeletal muscle mass in older adults with type 2 diabetes. Diabetes Care 32: 1993-1997, 2009.
39. Phillips B, Williams J, Atherton PJ, Smith K, Hildebrandt W, Rankin D, Greenhaff PL, Macdonald IA, Rennie M. Resistance exercise training improves age-related declines in leg vascular conductance and rejuvenates acute leg blood flow responses to feeding and exercise. J Appl Physiol 112: 347-353, 2012.
40. Praet SF, Jonkers RA, Schep G, Stehouwer CD, Kuipers H, Keizer HA, van Loon LJ. Long-standing, insulin-treated type 2 diabetes patients with complications respond well to short-term resistance and interval exercise training. Eur J Endocrinol 158: 163-172, 2008.
41. Rodriguez-Manas L, El-Assar M, Vallejo S, Lopez-Doriga P, Solis J, Petidier R, Montes M, Nevado J, Castro M, Gomez-Guerrero C, Peiro C, Sanchez-Ferrer CF. Endothelial dysfunction in aged humans is related with oxidative stress and vascular inflammation. Aging Cell 8: 226-238, 2009.
42. Ryan NA, Zwetsloot KA, Westerkamp LM, Hickner RC, Pofahl WE, Gavin TP. Lower skeletal muscle capillarization and VEGF expression in aged vs. young men. J Appl Physiol 100: 178-185, 2006.
43. Schnitzer JE. Transport functions of the glycocalyx, specific proteins, and caveolae in endothelium. In: Whole Organ Approaches to Cellular Metabolism, edited by Bassingthwaighte J, Goresky CA, Linehan JH. New York: Springer, 1998, p. 31-69.
44. Snoeijs M, Vink H, Voesten N, Christiaans M, Daemen JWH, Pep-pelenbosch A, Tordoir J, Peutz-Kootstra C, Buurman W, Schurink G, van Heurn L. Acute ischemic injury to the renal microvasculature in human kidney transplantation. Am J Physiol Renal Physiol 299: F1134-F1140, 2010.
45. Solomon TP, Haus JM, Li Y, Kirwan JP. Progressive hyperglycemia across the glucose tolerance continuum in older obese adults is related to skeletal muscle capillarization and nitric oxide bioavailability. J Clin Endocrinol Metab 96: 1377-1384, 2011.
46. Timmerman KL, Lee JL, Dreyer HC, Dhanani S, Glynn EL, Fry CS, Drummond MJ, Sheffield-Moore M, Rasmussen BB, Volpi E. Insulin stimulates human skeletal muscle protein synthesis via an indirect mechanism involving endothelial-dependent vasodilation and mammalian target of rapamycin complex 1 signaling. J Clin Endocrinol Metab 95: 3848-3857, 2010.
47. van Golen R, van Gulik T, Heger M. Mechanistic overview of reactive species-induced degradation of the endothelial glycocalyx during hepatic ischemia/reperfusion injury. Free Radic Biol Med 52: 1382-1402, 2012.
48. Verdijk L, Koopman R, Schaart G, Meijer K, Savelberg H, van Loon L. Satellite cell content is specifically reduced in type II skeletal muscle fibers in the elderly. Am J Physiol Endocrinol Metab 292: E151-E157, 2007.
49. Villela N, Kramer-Aguiar L, Bottino D, Wiernsperger N, Bouskela E. Metabolic disturbances linked to obesity: the role of impaired tissue perfusion. Arqu Bras Endocrinol Metabol 53: 238-245, 2009.
50. Vincent MA, Clerk LH, Lindner JR, Klibanov AL, Clark MG, Rattigan S, Barrett EJ. Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes 53: 1418-1423, 2004.
51. Vlahu CA, Lemkes BA, Struijk DG, Koopman MG, Krediet RT, Vink H. Damage of the endothelial glycocalyx in dialysis patients. J Am Soc Nephrol 23: 1900-1908, 2012.
52. Vollmar B, Menger M. The hepatic microcirculation: mechanistic contributions and therapeutic targets in liver injury and repair. Physiol Rev 89: 1269-1339, 2009.
53. Walrand S, Short KR, Bigelow ML, Sweatt AJ, Hutson SM, Nair KS. Functional impact of high protein intake on healthy elderly people. Am J Physiol Endocrinol Metab 295: E921-E928, 2008.
54. Weinbaum S, Tarbell JM, Damiano ER. The structure and function of the endothelial glycocalyx layer. Annu Rev Biomed Eng 9: 121-167, 2007.
55. Wilkinson SB, Tarnopolsky MA, Macdonald MJ, Macdonald JR, Armstrong D, Phillips SM. Consumption of fluid skim milk promotes greater muscle protein accretion after resistance exercise than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. Am J Clin Nutr 85: 1031-1040, 2007.