Effects of aging and exercise training on skeletal muscle blood flow and resistance artery morphology

Journal of Applied Physiology

Volumn 113, Issue 11, 2012, Pages 1699-1708

  Behnke, Bradley J ^a   Ramsey, Michael W ^b   Stabley, John N ^a   Dominguez II, James M ^a   Davis III, Robert T ^a   McCullough, Danielle J ^a   Muller Delp, Judy M ^a   Delp, Michael D ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b EAST TENNESSEE STATE UNIVERSITY   (United States)

Author keywords

Aging; Blood flow; Oxygen delivery; Resistance artery; Skeletal muscle

Indexed keywords

CITRATE SYNTHASE; OXYGEN;

ADAPTATION; AGE; AGING; ANIMAL; ARTERIAL PRESSURE; ARTERY; ARTICLE; BLOOD; BLOOD FLOW; BLOOD FLOW VELOCITY; COMPARATIVE STUDY; EXERCISE; FAST MUSCLE FIBER; FISCHER 344 RAT; HISTOLOGY; MALE; METABOLISM; MUSCLE CONTRACTION; OXYGEN CONSUMPTION; PHYSIOLOGY; RAT; SEDENTARY LIFESTYLE; SKELETAL MUSCLE; SLOW MUSCLE FIBER; VASCULAR RESISTANCE; VASCULARIZATION;

ADAPTATION, PHYSIOLOGICAL; AGE FACTORS; AGING; ANIMALS; ARTERIAL PRESSURE; ARTERIES; BLOOD FLOW VELOCITY; CITRATE (SI)-SYNTHASE; MALE; MUSCLE CONTRACTION; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; OXYGEN; OXYGEN CONSUMPTION; PHYSICAL EXERTION; RATS; RATS, INBRED F344; REGIONAL BLOOD FLOW; SEDENTARY LIFESTYLE; VASCULAR RESISTANCE;

EID: 84870433770     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01025.2012     Document Type: Article

References (70)

1. Armstrong RB, Hayes DA, Delp MD. Blood flow distribution in rat muscles during preexercise anticipatory response. J Appl Physiol 67: 1855-1861, 1989.
2. Armstrong RB, Laughlin MH. Exercise blood flow patterns within and among rat muscles after training. Am J Physiol Heart Circ Physiol 246: H59-H68, 1984.
3. Babcock MA, Paterson DH, Cunningham DA. Effects of aerobic endurance training on gas exchange kinetics of older men. Med Sci Sports Exerc 26: 447-452, 1994.
4. Beere PA, Russell SD, Morey MC, Kitzman DW, Higginbotham MB. Aerobic exercise training can reverse age-related peripheral circulatory changes in healthy older men. Circulation 100: 1085-1094, 1999.
5. Behnke BJ, Delp MD. Aging blunts the dynamics of vasodilation in isolated skeletal muscle resistance vessels. J Appl Physiol 108: 14-20, 2010.
6. Behnke BJ, Delp MD, Dougherty PJ, Musch TI, Poole DC. Effects of aging on microvascular oxygen pressures in rat skeletal muscle. Respir Physiol Neurobiol 146: 259-268, 2005.
7. Behnke BJ, Delp MD, Poole DC, Musch TI. Aging potentiates the effect of congestive heart failure on muscle microvascular oxygenation. J Appl Physiol 103: 1757-1763, 2007.
8. Behnke BJ, Prisby RD, Lesniewski LA, Donato AJ, Olin HM, Delp MD. Influence of ageing and physical activity on vascular morphology in rat skeletal muscle. J Physiol 575: 617-626, 2006.
9. Bell C, Paterson DH, Kowalchuk JM, Moy AP, Thorp DB, Noble EG, Taylor AW, Cunningham DA. Determinants of oxygen uptake kinetics in older humans following single-limb endurance exercise training. Exp Physiol 86: 659-665, 2001.
10. Copp SW, Ferreira LF, Herspring KF, Musch TI, Poole DC. The effects of aging on capillary hemodynamics in contracting rat spinotrapezius muscle. Microvasc Res 77: 113-119, 2009.
11. DeLorey DS, Kowalchuk JM, Paterson DH. Effect of age on O2 uptake kinetics and the adaptation of muscle deoxygenation at the onset of moderate-intensity cycling exercise. J Appl Physiol 97: 165-172, 2004.
12. Delp MD, Armstrong RB. Blood flow in normal and denervated muscle during exercise in conscious rats. Am J Physiol Heart Circ Physiol 255: H1509-H1515, 1988.
13. Delp MD, Behnke BJ, Spier SA, Wu G, Muller-Delp JM. Ageing diminishes endothelium-dependent vasodilatation and tetrahydrobiopterin content in rat skeletal muscle arterioles. J Physiol 586: 1161-1168, 2008.
14. Delp MD, Duan C. Composition and size of type I, IIA, IID/X, and IIB fibers and citrate synthase activity of rat muscle. J Appl Physiol 80: 261-270, 1996.
15. Delp MD, Laughlin MH. Time course of enhanced endothelium-mediated dilation in aorta of trained rats. Med Sci Sports Exerc 29: 1454-1461, 1997.
16. Delp MD, McAllister RM, Laughlin MH. Exercise training alters endothelium-dependent vasoreactivity of rat abdominal aorta. J Appl Physiol 75: 1354-1363, 1993.
17. Donato AJ, Lesniewski LA, Delp MD. Ageing and exercise training alter adrenergic vasomotor responses of rat skeletal muscle arterioles. J Physiol 579: 115-125, 2007.
18. Donato AJ, Lesniewski LA, Delp MD. The effects of aging and exercise training on endothelin-1 vasoconstrictor responses in rat skeletal muscle arterioles. Cardiovasc Res 66: 393-401, 2005.
19. Donato AJ, Magerko KA, Lawson BR, Durrant JR, Lesniewski LA, Seals DR. SIRT-1 and vascular endothelial dysfunction with ageing in mice and humans. J Physiol 589: 4545-4554, 2011.
20. Donato AJ, Uberoi A, Wray DW, Nishiyama S, Lawrenson L, Richardson RS. Differential effects of aging on limb blood flow in humans. Am J Physiol Heart Circ Physiol 290: H272-H278, 2006.
21. duManoir GR, DeLorey DS, Kowalchuk JM, Paterson DH. Differences in exercise limb blood flow and muscle deoxygenation with age: contributions to O2 uptake kinetics. Eur J Appl Physiol 110: 739-751, 2010.
22. Durrant JR, Seals DR, Connell ML, Russell MJ, Lawson BR, Folian BJ, Donato AJ, Lesniewski LA. Voluntary wheel running restores endothelial function in conduit arteries of old mice: direct evidence for reduced oxidative stress, increased superoxide dismutase activity and down-regulation of NADPH oxidase. J Physiol 587: 3271-3285, 2009.
23. Eskurza I, Monahan KD, Robinson JA, Seals DR. Effect of acute and chronic ascorbic acid on flow-mediated dilatation with sedentary and physically active human ageing. J Physiol 556: 315-324, 2004.
24. Flaim SF, Nellis SH, Toggart EJ, Drexler H, Kanda K, Newman ED. Multiple simultaneous determinations of hemodynamics and flow distribution in conscious rat. J Pharmacol Methods 11: 1-39, 1984.
25. Gavin TP, Ruster RS, Carrithers JA, Zwetsloot KA, Kraus RM, Evans CA, Knapp DJ, Drew JL, McCartney JS, Garry JP, Hickner RC. No difference in the skeletal muscle angiogenic response to aerobic exercise training between young and aged men. J Physiol 585: 231-239, 2007.
26. Herspring KF, Ferreira LF, Copp SW, Snyder BS, Poole DC, Musch TI. Effects of antioxidants on contracting spinotrapezius muscle microvascular oxygenation and blood flow in aged rats. J Appl Physiol 105: 1889-1896, 2008.
27. Hirai DM, Copp SW, Ferguson SK, Holdsworth CT, McCullough DJ, Behnke BJ, Musch TI, Poole DC. Exercise training and muscle microvascular oxygenation: functional role of nitric oxide. J Appl Physiol 113: 557-565, 2012.
28. Hirai DM, Copp SW, Hageman KS, Poole DC, Musch TI. Aging alters the contribution of nitric oxide to regional muscle hemodynamic control at rest and during exercise in rats. J Appl Physiol 111: 989-998, 2011.
29. Hirai DM, Copp SW, Herspring KF, Ferreira LF, Poole DC, Musch TI. Aging impacts microvascular oxygen pressures during recovery from contractions in rat skeletal muscle. Respir Physiol Neurobiol 169: 315-322, 2009.
30. Jackson DN, Moore AW, Segal SS. Blunting of rapid onset vasodilatation and blood flow restriction in arterioles of exercising skeletal muscle with ageing in male mice. J Physiol 588: 2269-2282, 2010.
31. Kirby BS, Voyles WF, Simpson CB, Carlson RE, Schrage WG, Dinenno FA. Endothelium-dependent vasodilatation and exercise hyperaemia in ageing humans: impact of acute ascorbic acid administration. J Physiol 587: 1989-2003, 2009.
32. Lakatta EG. Cardiovascular aging research: the next horizons. J Am Geriatr Soc 47: 613-625, 1999.
33. Lakatta EG. Cardiovascular system. In: Handbook of Physiology. Aging. Bethesda, MD: Am. Physiol. Soc., 1995, sect. 11, p. 413-474.
34. Laughlin MH, Armstrong RB. Muscular blood flow distribution patterns as a function of running speed in rats. Am J Physiol Heart Circ Physiol 243: H296-H306, 1982.
35. Laughlin MH, Roseguini B. Mechanisms for exercise training-induced increases in skeletal muscle blood flow capacity: differences with interval sprint training versus aerobic endurance training. J Physiol Pharmacol 59 Suppl 7: 71-88, 2008.
36. Lawrenson L, Poole JG, Kim J, Brown C, Patel P, Richardson RS. Vascular and metabolic response to isolated small muscle mass exercise: effect of age. Am J Physiol Heart Circ Physiol 285: H1023-H1031, 2003.
37. McCullough DJ, Davis RT 3rd, Dominguez JM 2nd, Stabley JN, Bruells CS, Behnke BJ. Effects of aging and exercise training on spinotrapezius muscle microvascular PO2 dynamics and vasomotor control. J Appl Physiol 110: 695-704, 2011.
38. McGuire DK, Levine BD, Williamson JW, Snell PG, Blomqvist CG, Saltin B, Mitchell JH. A 30-year follow-up of the Dallas Bedrest and Training Study. II. Effect of age on cardiovascular adaptation to exercise training. Circulation 104: 1358-1366, 2001.
39. Muller-Delp J, Spier SA, Ramsey MW, Lesniewski LA, Papadopoulos A, Humphrey JD, Delp MD. Effects of aging on vasoconstrictor and mechanical properties of rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 282: H1843-H1854, 2002.
40. Muller-Delp JM, Spier SA, Ramsey MW, Delp MD. Aging impairs endothelium-dependent vasodilation in rat skeletal muscle arterioles. Am J Physiol Heart Circ Physiol 283: H1662-H1672, 2002.
41. Muller JM, Myers PR, Laughlin MH. Exercise training alters myogenic responses in porcine coronary resistance arteries. J Appl Physiol 75: 2677-2682, 1993.
42. Murias JM, Kowalchuk JM, Paterson DH. Speeding of VO2 kinetics with endurance training in old and young men is associated with improved matching of local O2 delivery to muscle O2 utilization. J Appl Physiol 108: 913-922, 2010.
43. Musch TI, Eklund KE, Hageman KS, Poole DC. Altered regional blood flow responses to submaximal exercise in older rats. J Appl Physiol 96: 81-88, 2004.
44. Naito H, Powers SK, Demirel HA, Aoki J. Exercise training increases heat shock protein in skeletal muscles of old rats. Med Sci Sports Exerc 33: 729-734, 2001.
45. Ogawa T, Spina RJ, Martin WH 3rd, Kohrt WM, Schechtman KB, Holloszy JO, Ehsani AA. Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation 86: 494-503, 1992.
46. Padilla J, Simmons GH, Bender SB, Arce-Esquivel AA, Whyte JJ, Laughlin MH. Vascular effects of exercise: endothelial adaptations beyond active muscle beds. Physiology (Bethesda) 26: 132-145, 2011.
47. Park J, Prisby RD, Behnke BJ, Dominguez JM 2nd, Lesniewski LA, Donato AJ, Muller-Delp JM, Delp MD. Effects of aging, TNF-α and exercise training on angiotensin II-induced vasoconstriction of rat skeletal muscle arterioles. J Appl Physiol 113: 1091-1100, 2012.
48. Paterson DH, Cunningham DA, Koval JJ, St Croix CM. Aerobic fitness in a population of independently living men and women aged 55-86 years. Med Sci Sports Exerc 31: 1813-1820, 1999.
49. Poole DC, Hirai DM, Copp SW, Musch TI. Muscle oxygen transport and utilization in heart failure: implications for exercise (in)tolerance. Am J Physiol Heart Circ Physiol 302: H1050-H1063, 2012.
50. Poole DC, Kindig CA, Behnke BJ. Effects of emphysema on diaphragm microvascular oxygen pressure. Am J Respir Crit Care Med 163: 1081-1086, 2001.
51. Poole JG, Lawrenson L, Kim J, Brown C, Richardson RS. Vascular and metabolic response to cycle exercise in sedentary humans: effect of age. Am J Physiol Heart Circ Physiol 284: H1251-H1259, 2003.
52. Pries AR, Secomb TW, Gaehtgens P. Structural adaptation and stability of microvascular networks: theory and simulations. Am J Physiol Heart Circ Physiol 275: H349-H360, 1998.
53. Proctor DN, Joyner MJ. Skeletal muscle mass and the reduction of VO2 max in trained older subjects. J Appl Physiol 82: 1411-1415, 1997.
54. Proctor DN, Koch DW, Newcomer SC, Le KU, Leuenberger UA. Impaired leg vasodilation during dynamic exercise in healthy older women. J Appl Physiol 95: 1963-1970, 2003.
55. Proctor DN, Shen PH, Dietz NM, Eickhoff TJ, Lawler LA, Ebersold EJ, Loeffler DL, Joyner MJ. Reduced leg blood flow during dynamic exercise in older endurance-trained men. J Appl Physiol 85: 68-75, 1998.
56. Rossiter HB, Howlett RA, Holcombe HH, Entin PL, Wagner HE, Wagner PD. Age is no barrier to muscle structural, biochemical and angiogenic adaptations to training up to 24 months in female rats. J Physiol 565: 993-1005, 2005.
57. Rudic RD, Shesely EG, Maeda N, Smithies O, Segal SS, Sessa WC. Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J Clin Invest 101: 731-736, 1998.
58. Russell JA, Kindig CA, Behnke BJ, Poole DC, Musch TI. Effects of aging on capillary geometry and hemodynamics in rat spinotrapezius muscle. Am J Physiol Heart Circ Physiol 285: H251-H258, 2003.
59. Rywik TM, Blackman MR, Yataco AR, Vaitkevicius PV, Zink RC, Cottrell EH, Wright JG, Katzel LI, Fleg JL. Enhanced endothelial vasoreactivity in endurance-trained older men. J Appl Physiol 87: 2136-2142, 1999.
60. Schrage WG, Eisenach JH, Joyner MJ. Ageing reduces nitric oxideand prostaglandin-mediated vasodilatation in exercising humans. J Physiol 579: 227-236, 2007.
61. Sindler AL, Delp MD, Reyes R, Wu G, Muller-Delp JM. Effects of ageing and exercise training on eNOS uncoupling in skeletal muscle resistance arterioles. J Physiol 587: 3885-3897, 2009.
62. Spier SA, Delp MD, Meininger CJ, Donato AJ, Ramsey MW, Muller-Delp JM. Effects of ageing and exercise training on endothelium-dependent vasodilatation and structure of rat skeletal muscle arterioles. J Physiol 556: 947-958, 2004.
63. Spier SA, Delp MD, Stallone JN, Dominguez JM 2nd, Muller-Delp JM. Exercise training enhances flow-induced vasodilation in skeletal muscle resistance arteries of aged rats: role of PGI2 and nitric oxide. Am J Physiol Heart Circ Physiol 292: H3119-H3127, 2007.
64. Srere P. Citrate synthase. In: Methods in Enzymology. New York: Academic, 1969, p. 1-11.
65. Trott DW, Gunduz F, Laughlin MH, Woodman CR. Exercise training reverses age-related decrements in endothelium-dependent dilation in skeletal muscle feed arteries. J Appl Physiol 106: 1925-1934, 2009.
66. Wahren J, Saltin B, Jorfeldt L, Pernow B. Influence of age on the local circulatory adaptation to leg exercise. Scand J Clin Lab Invest 33: 79-86, 1974.
67. White FC, Bloor CM, McKirnan MD, Carroll SM. Exercise training in swine promotes growth of arteriolar bed and capillary angiogenesis in heart. J Appl Physiol 85: 1160-1168, 1998.
68. Williams DA, Segal SS. Feed artery role in blood flow control to rat hindlimb skeletal muscles. J Physiol 463: 631-646, 1993.
69. Woodman CR, Price EM, Laughlin MH. Aging induces muscle-specific impairment of endothelium-dependent dilation in skeletal muscle feed arteries. J Appl Physiol 93: 1685-1690, 2002.
70. Woodman CR, Price EM, Laughlin MH. Aging impairs nitric oxide and prostacyclin mediation of endothelium-dependent dilation in soleus feed arteries. J Appl Physiol 95: 2164-2170, 2003.