Reduced blood flow to contracting skeletal muscle in ageing humans: Is it all an effect of sand through the hourglass?

Journal of Physiology

Volumn 594, Issue 8, 2016, Pages 2297-2305

  Nyberg, Michael ^a   Hellsten, Ylva ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; NITRIC OXIDE;

AEROBIC METABOLISM; AGING; CROSS-SECTIONAL STUDY; ENERGY YIELD; HEART OUTPUT; HUMAN; HYPEREMIA; LONGITUDINAL STUDY; MUSCLE BLOOD FLOW; MUSCLE CONTRACTION; OXYGEN TRANSPORT; PHYSICAL ACTIVITY; PHYSICAL INACTIVITY; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SYMPATHETIC TONE; SYSTEMIC CIRCULATION; GROWTH, DEVELOPMENT AND AGING; MICROCIRCULATION; PHYSIOLOGY; SKELETAL MUSCLE; VASCULARIZATION;

AGING; HUMANS; MICROCIRCULATION; MUSCLE CONTRACTION; MUSCLE, SKELETAL;

EID: 84934783126     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/JP270594     Document Type: Review

References (81)

1. Alam M & Smirk FH (1937). Observations in man upon a blood pressure raising reflex arising from the voluntary muscles. J Physiol 89, 372-383.
2. Andersen P & Saltin B (1985). Maximal perfusion of skeletal muscle in man. J Physiol 366, 233-249.
3. Barnes JN, Schmidt JE, Nicholson WT & Joyner MJ (2012). Cyclooxygenase inhibition abolishes age-related differences in cerebral vasodilator responses to hypercapnia. J Appl Physiol 112, 1884-1890.
4. Beere PA, Russell SD, Morey MC, Kitzman DW & Higginbotham MB (1999). Aerobic exercise training can reverse age-related peripheral circulatory changes in healthy older men. Circulation 100, 1085-1094.
5. Bevegard BS & Shepherd JT (1966). Reaction in man of resistance and capacity vessels in forearm and hand to leg exercise. J Appl Physiol 21, 123-132.
6. Bradley SJ, Kingwell BA & McConell GK (1999). Nitric oxide synthase inhibition reduces leg glucose uptake but not blood flow during dynamic exercise in humans. Diabetes 48, 1815-1821.
7. Chavoshan B, Sander M, Sybert TE, Hansen J, Victor RG & Thomas GD (2002). Nitric oxide-dependent modulation of sympathetic neural control of oxygenation in exercising human skeletal muscle. J Physiol 540, 377-386.
8. Conley KE, Jubrias SA, Cress ME & Esselman P (2013). Exercise efficiency is reduced by mitochondrial uncoupling in the elderly. Exp Physiol 98, 768-777.
9. Coyle EF, Sidossis LS, Horowitz JF & Beltz JD (1992). Cycling efficiency is related to the percentage of type I muscle fibers. Med Sci Sports Exerc 24, 782-788.
10. Ershler WB, Sheng S, McKelvey J, Artz AS, Denduluri N, Tecson J, Taub DD, Brant LJ, Ferrucci L & Longo DL (2005). Serum erythropoietin and aging: a longitudinal analysis. J Am Geriatr Soc 53, 1360-1365.
11. Fadel PJ, Farias IM, Gallagher KM, Wang Z & Thomas GD (2012). Oxidative stress and enhanced sympathetic vasoconstriction in contracting muscles of nitrate-tolerant rats and humans. J Physiol 590, 395-407.
12. Frandsen U, Lopez-Figueroa M & Hellsten Y (1996). Localization of nitric oxide synthase in human skeletal muscle. Biochem Biophys Res Commun 227, 88-93.
13. Gaskell WH (1877). Changes of the blood-stream in muscles through stimulation of their nerves. J Anat Physiol 11, 360-402.
14. Gilligan DM, Panza JA, Kilcoyne CM, Waclawiw MA, Casino PR & Quyyumi AA (1994). Contribution of endothelium-derived nitric oxide to exercise-induced vasodilation. Circulation 90, 2853-2858.
15. Gliemann L, Nyberg M & Hellsten Y (2013a). Nitric oxide and reactive oxygen species in limb vascular function: what is the effect of physical activity? Free Radic Res 48, 71-83.
16. Gliemann L, Schmidt JF, Olesen J, Bienso RS, Peronard SL, Grandjean SU, Mortensen SP, Nyberg M, Bangsbo J, Pilegaard H & Hellsten Y (2013b). Resveratrol blunts the positive effects of exercise training on cardiovascular health in aged men. J Physiol 591, 5047-5059.
17. Gomez-Cabrera MC, Domenech E & Vina J (2008). Moderate exercise is an antioxidant: upregulation of antioxidant genes by training. Free Radic Biol Med 44, 126-131.
18. Gonzalez-Alonso J, Mortensen SP, Jeppesen TD, Ali L, Barker H, Damsgaard R, Secher NH, Dawson EA & Dufour SP (2008). Haemodynamic responses to exercise, ATP infusion and thigh compression in humans: insight into the role of muscle mechanisms on cardiovascular function. J Physiol 586, 2405-2417.
19. Gonzalez-Alonso J, Olsen DB & Saltin B (2002). Erythrocyte and the regulation of human skeletal muscle blood flow and oxygen delivery: role of circulating ATP. Circ Res 91, 1046-1055.
20. Hansen J, Thomas GD, Harris SA, Parsons WJ & Victor RG (1996). Differential sympathetic neural control of oxygenation in resting and exercising human skeletal muscle. J Clin Invest 98, 584-596.
21. Hansen J, Thomas GD, Jacobsen TN & Victor RG (1994). Muscle metaboreflex triggers parallel sympathetic activation in exercising and resting human skeletal muscle. Am J Physiol Heart Circ Physiol 266, H2508-H2514.
22. Heinonen I, Saltin B, Kemppainen J, Sipila HT, Oikonen V, Nuutila P, Knuuti J, Kalliokoski K & Hellsten Y (2011). Skeletal muscle blood flow and oxygen uptake at rest and during exercise in humans: a pet study with nitric oxide and cyclooxygenase inhibition. Am J Physiol Heart Circ Physiol 300, H1510-H1517.
23. Hopker JG, Coleman DA, Gregson HC, Jobson SA, Vonder Haar T, Wiles J & Passfield L (2013). The influence of training status, age, and muscle fiber type on cycling efficiency and endurance performance. J Appl Physiol 115, 723-729.
24. Jendzjowsky NG & DeLorey DS (2013). Short-term exercise training enhances functional sympatholysis through a nitric oxide-dependent mechanism. J Physiol 591, 1535-1549.
25. Joseph AM, Adhihetty PJ, Buford TW, Wohlgemuth SE, Lees HA, Nguyen LM, Aranda JM, Sandesara BD, Pahor M, Manini TM, Marzetti E & Leeuwenburgh C (2012). The impact of aging on mitochondrial function and biogenesis pathways in skeletal muscle of sedentary high- and low-functioning elderly individuals. Aging Cell 11, 801-809.
26. Kalliokoski KK, Oikonen V, Takala TO, Sipila H, Knuuti J & Nuutila P (2001). Enhanced oxygen extraction and reduced flow heterogeneity in exercising muscle in endurance-trained men. Am J Physiol Endocrinol Metab 280, E1015-E1021.
27. Kiens B, Essen-Gustavsson B, Christensen NJ & Saltin B (1993). Skeletal muscle substrate utilization during submaximal exercise in man: effect of endurance training. J Physiol 469, 459-478.
28. Kingwell BA, Formosa M, Muhlmann M, Bradley SJ & McConell GK (2002). Nitric oxide synthase inhibition reduces glucose uptake during exercise in individuals with type 2 diabetes more than in control subjects. Diabetes 51, 2572-2580.
29. Kirby BS, Crecelius AR, Voyles WF & Dinenno FA (2012). Impaired skeletal muscle blood flow control with advancing age in humans: attenuated ATP release and local vasodilation during erythrocyte deoxygenation. Circ Res 111, 220-230.
30. Kirby BS, Voyles WF, Carlson RE & Dinenno FA (2008). Graded sympatholytic effect of exogenous ATP on postjunctional α-adrenergic vasoconstriction in the human forearm: implications for vascular control in contracting muscle. J Physiol 586, 4305-4316.
31. Krustrup P, Secher NH, Relu MU, Hellsten Y, Soderlund K & Bangsbo J (2008). Neuromuscular blockade of slow twitch muscle fibres elevates muscle oxygen uptake and energy turnover during submaximal exercise in humans. J Physiol 586, 6037-6048.
32. 2 uptake. Med Sci Sports Exerc 36, 973-982.
33. Lawrenson L, Poole JG, Kim J, Brown C, Patel P & Richardson RS (2003). Vascular and metabolic response to isolated small muscle mass exercise: effect of age. Am J Physiol Heart Circ Physiol 285, H1023-H1031.
34. Layec G, Hart CR, Trinity JD, Le FY, Jeong EK & Richardson RS (2015). Skeletal muscle work efficiency with age: the role of non-contractile processes. Clin Sci (Lond) 128, 213-223.
35. Lazarus NR & Harridge SD (2010). Exercise, physiological function, and the selection of participants for aging research. J Gerontol A Biol Sci Med Sci 65, 854-857.
36. McGuire DK, Levine BD, Williamson JW, Snell PG, Blomqvist CG, Saltin B & Mitchell JH (2001). A 30-year follow-up of the Dallas Bedrest and Training Study: I. Effect of age on the cardiovascular response to exercise. Circulation 104, 1350-1357.
37. 2 during high-intensity whole-body exercise in humans. J Physiol 586, 2621-2635.
38. Mortensen SP, Gonzalez-Alonso J, Damsgaard R, Saltin B & Hellsten Y (2007). Inhibition of nitric oxide and prostaglandins, but not endothelial-derived hyperpolarizing factors, reduces blood flow and aerobic energy turnover in the exercising human leg. J Physiol 581, 853-861.
39. Mortensen SP, Morkeberg J, Thaning P, Hellsten Y & Saltin B (2012a). Two weeks of muscle immobilization impairs functional sympatholysis but increases exercise hyperemia and the vasodilatory responsiveness to infused ATP. Am J Physiol Heart Circ Physiol 302, H2074-H2082.
40. Mortensen SP, Nyberg M, Gliemann L, Thaning P, Saltin B & Hellsten Y (2014). Exercise training modulates functional sympatholysis and α-adrenergic vasoconstrictor responsiveness in hypertensive and normotensive individuals. J Physiol 592, 3063-3073.
41. Mortensen SP, Nyberg M, Winding K & Saltin B (2012b). Lifelong physical activity preserves functional sympatholysis and purinergic signalling in the ageing human leg. J Physiol 590, 6227-6236.
42. Mortensen SP, Thaning P, Nyberg M, Saltin B & Hellsten Y (2011). Local release of ATP into the arterial inflow and venous drainage of human skeletal muscle: insight from ATP determination with the intravascular microdialysis technique. J Physiol 589, 1847-1857.
43. Nyberg M, Blackwell JR, Damsgaard R, Jones AM, Hellsten Y & Mortensen SP (2012a). Lifelong physical activity prevents an age-related reduction in arterial and skeletal muscle nitric oxide bioavailability in humans. J Physiol 590, 5361-5370.
44. Nyberg M, Jensen LG, Thaning P, Hellsten Y & Mortensen SP (2012b). Role of nitric oxide and prostanoids in the regulation of leg blood flow and blood pressure in humans with essential hypertension: effect of high-intensity aerobic training. J Physiol 590, 1481-1494.
45. Nyberg M, Mortensen SP, Cabo H, Gomez-Cabrera MC, Vina J & Hellsten Y (2014). Roles of sedentary aging and lifelong physical activity in exchange of glutathione across exercising human skeletal muscle. Free Radic Biol Med 73C, 166-173.
46. Ogawa T, Spina RJ, Martin WH III, Kohrt WM, Schechtman KB, Holloszy JO & Ehsani AA (1992). Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation 86, 494-503.
47. Panza JA, Casino PR, Badar DM & Quyyumi AA (1993). Effect of increased availability of endothelium-derived nitric oxide precursor on endothelium-dependent vascular relaxation in normal subjects and in patients with essential hypertension. Circulation 87, 1475-1481.
48. Poole JG, Lawrenson L, Kim J, Brown C & Richardson RS (2003). Vascular and metabolic response to cycle exercise in sedentary humans: effect of age. Am J Physiol Heart Circ Physiol 284, H1251-H1259.
49. 2 relationships during submaximal cycle ergometry. J Appl Physiol 84, 599-605.
50. Proctor DN, Miller JD, Dietz NM, Minson CT & Joyner MJ (2001). Reduced submaximal leg blood flow after high-intensity aerobic training. J Appl Physiol 91, 2619-2627.
51. Proctor DN, Newcomer SC, Koch DW, Le KU, MacLean DA & Leuenberger UA (2003). Leg blood flow during submaximal cycle ergometry is not reduced in healthy older normally active men. J Appl Physiol 94, 1859-1869.
52. Proctor DN & Parker BA (2006). Vasodilation and vascular control in contracting muscle of the aging human. Microcirculation 13, 315-327.
53. Proctor DN, Shen PH, Dietz NM, Eickhoff TJ, Lawler LA, Ebersold EJ, Loeffler DL & Joyner MJ (1998b). Reduced leg blood flow during dynamic exercise in older endurance-trained men. J Appl Physiol 85, 68-75.
54. Radegran G & Saltin B (1999). Nitric oxide in the regulation of vasomotor tone in human skeletal muscle. Am J Physiol Heart Circ Physiol 276, H1951-H1960.
55. Ray CA & Mark AL (1995). Sympathetic nerve activity to nonactive muscle of the exercising and nonexercising limb. Med Sci Sports Exerc 27, 183-187.
56. Remensnyder JP, Mitchell JH & Arnoff SJ (1962). Functional sympatholysis during muscular activity. Observations on influence of carotid sinus on oxygen uptake. Circ Res 11, 370-380.
57. 2 extraction compromised? J Appl Physiol 75, 1911-1916.
58. Rosenmeier JB, Fritzlar SJ, Dinenno FA & Joyner MJ (2003). Exogenous NO administration and α-adrenergic vasoconstriction in human limbs. J Appl Physiol 95, 2370-2374.
59. Rosenmeier JB, Hansen J & Gonzalez-Alonso J (2004). Circulating ATP-induced vasodilatation overrides sympathetic vasoconstrictor activity in human skeletal muscle. J Physiol 558, 351-365.
60. Rowell LB (1993). Human Cardiovascular Control Oxford University Press, New York.
61. Rudroff T, Weissman JA, Bucci M, Seppanen M, Kaskinoro K, Heinonen I & Kalliokoski KK (2014). Positron emission tomography detects greater blood flow and less blood flow heterogeneity in the exercising skeletal muscles of old compared with young men during fatiguing contractions. J Physiol 592, 337-349.
62. Sadler W (1869). Arbeiten aus der phys, 12th edn. Anstalt Zu, Leipzig.
63. Saltin B (2007). Exercise hyperaemia: magnitude and aspects on regulation in humans. J Physiol 583, 819-823.
64. Saltin B, Blomqvist G, Mitchell JH, Johnson RL Jr, Wildenthal K & Chapman CB (1968). Response to exercise after bed rest and after training. Circulation 38, VII1-VII78.
65. Saltin B & Mortensen SP (2012). Inefficient functional sympatholysis is an overlooked cause of malperfusion in contracting skeletal muscle. J Physiol 590, 6269-6275.
66. Saltin B, Nazar K, Costill DL, Stein E, Jansson E, Essen B & Gollnick D (1976). The nature of the training response; peripheral and central adaptations of one-legged exercise. Acta Physiol Scand 96, 289-305.
67. Sander M, Chavoshan B, Harris SA, Iannaccone ST, Stull JT, Thomas GD & Victor RG (2000). Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc Natl Acad Sci U S A 97, 13818-13823.
68. Schrage WG, Eisenach JH & Joyner MJ (2007). Ageing reduces nitric-oxide- and prostaglandin-mediated vasodilatation in exercising humans. J Physiol 579, 227-236.
69. Schrage WG, Joyner MJ & Dinenno FA (2004). Local inhibition of nitric oxide and prostaglandins independently reduces forearm exercise hyperaemia in humans. J Physiol 557, 599-611.
70. Schrage WG, Wilkins BW, Johnson CP, Eisenach JH, Limberg JK, Dietz NM, Curry TB & Joyner MJ (2010). Roles of nitric oxide synthase and cyclooxygenase in leg vasodilation and oxygen consumption during prolonged low-intensity exercise in untrained humans. J Appl Physiol 109, 768-777.
71. Seals DR & Victor RG (1991). Regulation of muscle sympathetic nerve activity during exercise in humans. Exerc Sport Sci Rev 19, 313-349.
72. Sprague RS & Ellsworth ML (2012). Erythrocyte-derived ATP and perfusion distribution: role of intracellular and intercellular communication. Microcirculation 19, 430-439.
73. Strange S (1999). Cardiovascular control during concomitant dynamic leg exercise and static arm exercise in humans. J Physiol 514, 283-291.
74. Taddei S, Galetta F, Virdis A, Ghiadoni L, Salvetti G, Franzoni F, Giusti C & Salvetti A (2000). Physical activity prevents age-related impairment in nitric oxide availability in elderly athletes. Circulation 101, 2896-2901.
75. Taddei S, Virdis A, Ghiadoni L, Salvetti G, Bernini G, Magagna A & Salvetti A (2001). Age-related reduction of NO availability and oxidative stress in humans. Hypertension 38, 274-279.
76. Taddei S, Virdis A, Mattei P, Ghiadoni L, Fasolo CB, Sudano I & Salvetti A (1997). Hypertension causes premature aging of endothelial function in humans. Hypertension 29, 736-743.
77. Thomas GD & Victor RG (1998). Nitric oxide mediates contraction-induced attenuation of sympathetic vasoconstriction in rat skeletal muscle. J Physiol 506, 817-826.
78. Trott DW, Gunduz F, Laughlin MH & Woodman CR (2009). Exercise training reverses age-related decrements in endothelium-dependent dilation in skeletal muscle feed arteries. J Appl Physiol 106, 1925-1934.
79. Tschakovsky ME, Sujirattanawimol K, Ruble SB, Valic Z & Joyner MJ (2002). Is sympathetic neural vasoconstriction blunted in the vascular bed of exercising human muscle? J Physiol 541, 623-635.
80. Vallance P, Collier J & Moncada S (1989). Effects of endothelium-derived nitric oxide on peripheral arteriolar tone in man. Lancet 2, 997-1000.
81. Wahren J, Saltin B, Jorfeldt L & Pernow B (1974). Influence of age on the local circulatory adaptation to leg exercise. Scand J Clin Lab Invest 33, 79-86.