A systematic review of exercise as a therapeutic intervention to improve arterial function in persons living with spinal cord injury

Spinal Cord

Volumn 49, Issue 6, 2011, Pages 702-714

  Phillips, A A ^a   Cote, A T ^a   Warburton, D E R ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

exercise; spinal cord injury; Systematic review; vascular function

Indexed keywords

ARM EXERCISE; ARTERIAL STIFFNESS; BLOOD VESSEL COMPLIANCE; BODY WEIGHT; CARDIOVASCULAR FUNCTION; ELASTICITY; ELECTRICALLY STIMULATED RESISTANCE EXERCISE; FUNCTIONAL ELECTRICAL STIMULATION; HUMAN; KINESIOTHERAPY; KNEE FUNCTION; LEG EXERCISE; LONG TERM CARE; MUSCLE EXCITATION; PASSIVE EXERCISE; PRIORITY JOURNAL; RESISTANCE TRAINING; REVIEW; SPINAL CORD INJURY; SYSTEMATIC REVIEW; TREADMILL EXERCISE; UPPER BODY WHEELING;

CARDIOVASCULAR DISEASES; COMORBIDITY; EXERCISE THERAPY; HUMANS; SPINAL CORD INJURIES;

EID: 79958042271     PISSN: 13624393     EISSN: 14765624     Source Type: Journal    
DOI: 10.1038/sc.2010.193     Document Type: Review

References (83)

1. DeVivo MJ, Black KJ, Stover SL. Causes of death during the first 12 years after spinal cord injury. Arch Phys Med Rehabil 1993; 74: 248-254. (Pubitemid 23083797)
2. Nakanishi N, Kawashimo H, Nakamura K, Suzuki K, Yoshida H, Uzura S et al. Association of alcohol consumption with increase in aortic stiffness: a 9-year longitudinal study in middle-aged Japanese men. Ind Health 2001; 39: 24-28. (Pubitemid 32157902)
3. Garshick E, Kelley A, Cohen SA, Garrison A, Tun CG, Gagnon D et al. A prospective assessment of mortality in chronic spinal cord injury. Spinal Cord 2005; 43: 408-416. (Pubitemid 41039541)
4. Wilmer W, Nichols MFOR. Mcdonald's Blood Flow in Arteries: Theoretical, Experimental and Clinical Principles. Lea & Febiger: Philadelphia, PA, 2007.
5. Glasser SP, Arnett DK, McVeigh GE, Finkelstein SM, Bank AJ, Morgan DJ et al. Vascular compliance and cardiovascular disease: a risk factor or a marker? Am J Hypertens 1997; 10 (Part 1): 1175-1189. (Pubitemid 27486352)
6. Safar H, Mourad JJ, Safar M, Blacher J. Aortic pulse wave velocity, an independent marker of cardiovascular risk. Arch Mal Coeur Vaiss 2002; 95: 1215-1218. (Pubitemid 36091020)
7. Vaitkevicius PV, Fleg JL, Engel JH, O'Connor FC, Wright JG, Lakatta LE et al. Effects of age and aerobic capacity on arterial stiffness in healthy adults. Circulation 1993; 88 (Part 1): 1456-1462. (Pubitemid 23296891)
8. Ohmori K, Emura S, Takashima T. Risk factors of atherosclerosis and aortic pulse wave velocity. Angiology 2000; 51: 53-60. (Pubitemid 30059051)
9. Kesse-Guyot E, Vergnaud AC, Fezeu L, Zureik M, Blacher J, Peneau S et al. Associations between dietary patterns and arterial stiffness, carotid artery intima-media thickness and atherosclerosis. Eur J Cardiovasc Prev Rehabil 2010; 17: 718-724.
10. Tang W, Cheng LT, Lu XH, Wang T. Effect of nutrition on arterial stiffness in peritoneal dialysis patients. Am J Nephrol 2009; 30: 120-125.
11. Jatoi NA, Jerrard-Dunne P, Feely J, Mahmud A. Impact of smoking and smoking cessation on arterial stiffness and aortic wave reflection in hypertension. Hypertension 2007; 49: 981-985. (Pubitemid 351664328)
12. Yufu K, Takahashi N, Hara M, Saikawa T, Yoshimatsu H. Measurement of the brachial-ankle pulse wave velocity and flow-mediated dilatation in young, healthy smokers. Hypertens Res 2007; 30: 607-612. (Pubitemid 47278318)
13. Mahmud A, Feely J. Divergent effect of acute and chronic alcohol on arterial stiffness. Am J Hypertens 2002; 15: 240-243. (Pubitemid 34226189)
14. Mattace-Raso FU, van der Cammen TJ, van den Elzen AP, Schalekamp MA, Asmar R, Reneman RS et al. Moderate alcohol consumption is associated with reduced arterial stiffness in older adults: the Rotterdam study. J Gerontol A Biol Sci Med Sci 2005; 60: 1479-1483. (Pubitemid 41798459)
15. Tsuchikura S, Shoji T, Kimoto E, Shinohara K, Hatsuda S, Koyama H et al. Central versus peripheral arterial stiffness in association with coronary, cerebral and peripheral arterial disease. Atherosclerosis 2010; 211: 480-485.
16. Gando Y, Yamamoto K, Murakami H, Ohmori Y, Kawakami R, Sanada K et al. Longer time spent in light physical activity is associated with reduced arterial stiffness in older adults. Hypertension 2010; 56: 540-546.
17. Theisen D, Vanlandewijck Y, Sturbois X, Francaux M. Blood distribution adaptations in paraplegics during posture changes: peripheral and central reflex responses. Eur J Appl Physiol 2000; 81: 463-469. (Pubitemid 30189972)
18. Gao SA, Ambring A, Lambert G, Karlsson AK. Autonomic control of the heart and renal vascular bed during autonomic dysreflexia in high spinal cord injury. Clin Auton Res 2002; 12: 457-464. (Pubitemid 36207670)
19. Jacobs PL, Nash MS. Exercise recommendations for individuals with spinal cord injury. Sports Med 2004; 34: 727-751. (Pubitemid 39382182)
20. Brown R, Macefield VG. Assessing the capacity of the sympathetic nervous system to respond to a cardiovascular challenge in human spinal cord injury. Spinal Cord 2008; 46: 666-672.
21. Kooijman M, Rongen GA, Smits P, Hopman MT. Preserved alpha-adrenergic tone in the leg vascular bed of spinal cord-injured individuals. Circulation 2003; 108: 2361-2367. (Pubitemid 37413543)
22. Wecht JM, Radulovic M, Lessey J, Spungen AM, Bauman WA. Common carotid and common femoral arterial dynamics during head-up tilt in persons with spinal cord injury. J Rehabil Res Dev 2004; 41: 89-94. (Pubitemid 38325975)
23. de Groot PC, Bleeker MW, van Kuppevelt DH, van der Woude LH, Hopman MT. Rapid and extensive arterial adaptations after spinal cord injury. Arch Phys Med Rehabil 2006; 87: 688-696.
24. Taylor PN, Ewins DJ, Fox B, Grundy D, Swain ID. Limb blood flow, cardiac output and quadriceps muscle bulk following spinal cord injury and the effect of training for the Odstock functional electrical stimulation standing system. Paraplegia 1993; 31: 303-310. (Pubitemid 23262623)
25. Rowell LB. Human Cardiovascular Control. Oxford University Press: London, 1993.
26. Pollack AA, Taylor BE, Myers TT, Wood EH. The effect of exercise and body position on the venous pressure at the ankle in patients having venous valvular defects. J Clin Invest 1949; 28: 559-563.
27. Folkow B, Gaskell P, Waaler BA. Blood flow through limb muscles during heavy rhythmic exercise. Acta Physiol Scand 1970; 80: 61-72.
28. Radegran G, Saltin B. Muscle blood flow at onset of dynamic exercise in humans. Am J Physiol 1998; 274 (Part 2): H314-H322.
29. LaBarbera M. Principles of design of fluid transport systems in zoology. Science 1990; 249: 992-1000. (Pubitemid 20286814)
30. Martin TP, Stein RB, Hoeppner PH, Reid DC. Influence of electrical stimulation on the morphological and metabolic properties of paralyzed muscle. J Appl Physiol 1992; 72: 1401-1406.
31. Hopman MT, van Asten WN, Oeseburg B. Changes in blood flow in the common femoral artery related to inactivity and muscle atrophy in individuals with long-standing paraplegia. Adv Exp Med Biol 1996; 388: 379-383. (Pubitemid 26317551)
32. Mangoni AA, Mircoli L, Giannattasio C, Mancia G, Ferrari AU. Effect of sympathectomy on mechanical properties of common carotid and femoral arteries. Hypertension 1997; 30: 1085-1088. (Pubitemid 27476163)
33. Lacolley P, Glaser E, Challande P, Boutouyrie P, Mignot JP, Duriez M et al. Structural changes and in situ aortic pressure-diameter relationship in long-term chemical-sympathectomized rats. Am J Physiol 1995; 269 (Part 2): H407-H416.
34. Aliev G, Ralevic V, Burnstock G. Depression of endothelial nitric oxide synthase but increased expression of endothelin-1 immu-noreactivity in rat thoracic aortic endothelium associated with long-term, but not short-term, sympathectomy. Circ Res 1996; 79: 317-323. (Pubitemid 26255885)
35. Warburton DE, Nicol CW, Bredin SS. Health benefits of physical activity: the evidence. CMAJs 2006; 174: 801-809.
36. Warburton DER, Krassioukov A, Sproule S. Cardiovascular health and exercise rehabilitation in spinal cord injury. Top Spinal Cord Injury Rehabil 2007; 13: 98-122. (Pubitemid 46982073)
37. Gando Y, Kawano H, Yamamoto K, Sanada K, Tanimoto M, Oh T et al. Age and cardiorespiratory fitness are associated with arterial stiffening and left ventricular remodelling. J Hum Hypertens 2010; 24: 197-206.
38. Vivodtzev I, Minet C, Wuyam B, Borel JC, Vottero G, Monneret D et al. Significant improvement in arterial stiffness after endurance training in patients with COPD. Chest 2010; 137: 585-592.
39. Trzos E, Kurpesa M, Rechcinski T, Wierzbowska-Drabik K, Krzeminska-Pakula M. The influence of physical rehabilitation on arterial compliance in patients after myocardial infarction. Cardiol J 2007; 14: 366-371. (Pubitemid 47456120)
40. Kinzer SM, Convertino VA. Role of leg vasculature in the cardiovascular response to arm work in wheelchair-dependent populations. Clin Physiol 1989; 9: 525-533. (Pubitemid 20014992)
41. Hopman MT, Verheijen PH, Binkhorst RA. Volume changes in the legs of paraplegic subjects during arm exercise. J Appl Physiol 1993; 75: 2079-2083. (Pubitemid 23352379)
42. Moseley AM, Herbert RD, Sherrington C, Maher CG. Evidence for physiotherapy practice: a survey of the Physiotherapy Evidence Database (PEDro). Aust J Physiother 2002; 48: 43-49. (Pubitemid 34240086)
43. Eng JJ, Teasell RJ, Miller WC, Wolfe DL, Townson AF, Aubut J et al. Spinal cord injury rehabilitation program: method of the SCIRE systematic review. Top Spinal Cord Injury 2007, 1-10. (Pubitemid 46982068)
44. Sackett DL, Rosenberg WMC, Gray JAM, Haynes BR, Richardson WS. Evidence based medicine: what it is and what it isn't. BMJ 1996; 312: 71-72.
45. Krassioukov A, Warburton DE, Teasell R, Eng JJ. A systematic review of the management of autonomic dysreflexia after spinal cord injury. Arch Phys Med Rehabil 2009; 90: 682-695.
46. Hing W, Bigelow R, Bremner T. Mulligan's mobilization with movement: a systematic review. J Man Manip Ther 2008; 17: E39-E66.
47. Hartling L, Brison RJ, Crumley ET, Klassen TP, Pickett W. A systematic review of interventions to prevent childhood farm injuries. Pediatrics 2004; 114: e483-e496. (Pubitemid 41529744)
48. Hignett S. Systematic review of patient handling activities starting in lying, sitting and standing positions. J Adv Nurs 2003; 41: 545-552. (Pubitemid 37255944)
49. Ballaz L, Fusco N, Cretual A, Langella B, Brissot R. Peripheral vascular changes after home-based passive leg cycle exercise training in people with paraplegia: a pilot Study. Arch Phys Med Rehabil 2008; 89: 2162-2166.
50. Foley NC, Teasell RW, Bhogal SK, Speechley MR. Stroke rehabilitation evidence-based review: methodology. Top Stroke Rehabil 2003; 10: 1-7. (Pubitemid 36576989)
51. Bidart Y, Maury M. The circulatory behaviour in complete chronic paraplegia. II-circulatory adjustments to local metabolic needs. b-Muscular circulation. Paraplegia 1973a; 11: 1-24.
52. Bidart Y, Maury M. The circulatory behaviour in complete chronic paraplegia. IV-The loss of vasomotor adjustments to general needs. b-Study of arteriolar motricity. Paraplegia 1973b; 11: 1-24.
53. Ter Woerds WT, De Groot PCE, Van Kuppevelt DHJM, Hopman MTE. Passive leg movements and passive cycling do not alter arterial leg blood flow in subjects with spinal cord injury. Phys Ther 2006; 86: 636-645.
54. Dela F, Mohr T, Jensen CMR, Haahr HL, Secher NH, Biering-Sorensen F et al. Cardiovascular control during exercise: insights from spinal cord-injured humans. Circulation 2003; 107: 2127-2133. (Pubitemid 36532195)
55. Nash MS, Montefusco CM, Rhodes BA. Peripheral vascular response to exercise-induced and postocclusive reactive hyper-emia in quadriplegics. Surg Forum 1990; 41: 498-499.
56. Olive JL, Slade JM, Dudley GA, McCully KK. Blood flow and muscle fatigue in SCI individuals during electrical stimulation. J Appl Physiol 2003; 94: 701-708. (Pubitemid 36158249)
57. Ballaz L, Fusco N, Cretual A, Langella B, Brissot R. Acute peripheral blood flow response induced by passive leg cycle exercise in people with spinal cord Injury. Arch Phys Med Rehabil 2007; 88: 471-476. (Pubitemid 46482436)
58. Burkett LN, Chisum J, Pierce J, Pomeroy K, Fisher J, Martin M. Blood flow and lactic acid levels in exercising paralyzed wheelchair bound individuals. Adapt Phys Activ Q 1988; 5: 60-73.
59. Phillips W, Burkett LN, Munro R, Davis M, Pomeroy K. Relative changes in blood flow with functional electrical stimulation during exercise of the paralyzed lower limbs. Paraplegia 1995; 33: 90-93.
60. Svensson M, Siösteen H, Wetterqvist H, Sullivan L. Influence of physiotherapy on leg blood flow in patients with complete spinal cord injury lesions. Physiother Theory Pract 1995; 11: 97-107.
61. Seifert J, Lob G, Stoephasius E, Probst J, Brendel W. Blood flow in muscles of paraplegic patients under various conditions measured by a double isotope technique. Paraplegia 1972; 10: 185-191.
62. Griffin L, Decker MJ, Hwang JY, Wang B, Kitchen K, Ding Z et al. Functional electrical stimulation cycling improves body composition, metabolic and neural factors in persons with spinal cord injury. J Electromyogr Kinesiol 2009; 19: 614-622.
63. Devillard X, Rimaud D, Roche F, Calmels P. Effects of training programs for spinal cord injury. Ann Readapt Med Phys 2007; 50: 490-498, 480-489. (Pubitemid 46908849)
64. Ditor DS, MacDonald MJ, Kamath MV, Bugaresti J, Adams M, McCartney N et al. The effects of body-weight supported treadmill training on cardiovascular regulation in individuals with motor-complete SCI. Spinal Cord 2005; 43: 664-673. (Pubitemid 41718909)
65. Zbogar D, Eng JJ, Krassioukov AV, Scott JM, Esch BTA, Warburton DER. The effects of functional electrical stimulation leg cycle ergometry training on arterial compliance in individuals with spinal cord injury. Spinal Cord 2008; 46: 722-726.
66. Nash MS, Jacobs PL, Montalvo BM, Klose KJ, Guest RS, Needham-Shropshire BM. Evaluation of a training program for persons with SCI paraplegia using the Parasteprho1 ambulation system: Part 5. Lower extremity blood flow and hyperemic responses to occlusion are augmented by ambulation training. Arch Phys Med Rehabil 1997; 78: 808-814. (Pubitemid 27375085)
67. Stoner L, Sabatier MJ, Mahoney ET, Dudley GA, McCully KK. Electrical stimulation-evoked resistance exercise therapy improves arterial health after chronic spinal cord injury. Spinal Cord 2007; 45: 49-56. (Pubitemid 46067400)
68. Sabatier MJ, Stoner L, Mahoney ET, Black C, Elder C, Dudley GA et al. Electrically stimulated resistance training in SCI individuals increases muscle fatigue resistance but not femoral artery size or blood flow. Spinal Cord 2006; 44: 227-233.
69. Jae SY, Heffernan KS, Lee M, Fernhall B. Arterial structure and function in physically active persons with spinal cord injury. J Rehabil Med 2008; 40: 535-538.
70. Nash MS, Montalvo BM, Applegate B. Lower extremity blood flow and responses to occlusion ischemia differ in exercise-trained and sedentary tetraplegic persons. Arch Phys Med Rehabil 1996; 77: 1260-1265. (Pubitemid 26424839)
71. Gerrits HL, de Haan A, Sargeant AJ, van Langen H, Hopman MT. Peripheral vascular changes after electrically stimulated cycle training in people with spinal cord injury. Arch Phys Med Rehabil 2001; 82: 832-839. (Pubitemid 32520796)
72. De Groot P, Crozier J, Rakobowchuk M, Hopman M, Macdonald M. Electrical stimulation alters FMD and arterial compliance in extremely inactive legs. Med Sci Sports Exerc 2005; 37: 1356-1364. (Pubitemid 41209290)
73. Hopman MT, Groothuis JT, Flendrie M, Gerrits KH, Houtman S. Increased vascular resistance in paralyzed legs after spinal cord injury is reversible by training. J Appl Physiol 2002; 93: 1966-1972. (Pubitemid 35379321)
74. Thijssen DH, Ellenkamp R, Smits P, Hopman MT. Rapid vascular adaptations to training and detraining in persons with spinal cord injury. Arch Phys Med Rehabil 2006; 87: 474-481.
75. Thijssen DHJ, Heesterbeek P, Van Kuppevelt DJM, Duysens J, Hopman MTE. Local vascular adaptations after hybrid training in spinal cord-injured subjects. Med Sci Sports Exerc 2005; 37: 1112-1118. (Pubitemid 40981671)
76. Tordi N, Mourot L, Chapuis A, Parratte B, Regnard J. Effects of a primary rehabilitation programme on arterial vascular adaptations in an individual with paraplegia. Ann Phys Rehabil Med 2009; 52: 66-73.
77. Krahn G, McCarthy M, Westwood D, Powers L. Evaluation of an innovative methodology to recruit research participants with spinal cord injury through durable medical equipment suppliers. Arch Phys Med Rehabil 2008; 89: 1341-1349. (Pubitemid 351884983)
78. Dearwater SR, LaPorte RE, Cauley JA, Brenes G. Assessment of physical activity in inactive populations. Med Sci Sports Exerc 1985; 17: 651-655. (Pubitemid 16209433)
79. Buchholz AC, McGillivray CF, Pencharz PB. Physical activity levels are low in free-living adults with chronic paraplegia. Obes Res 2003; 11: 563-570. (Pubitemid 41202418)
80. Groothuis JT, Hopman MT. Does passive cycling induce changes in peripheral blood flow in persons with spinal cord injury? Arch Phys Med Rehabil 2007; 88: 1740. (Pubitemid 350151409)
81. Wong S, Krassioukov AV, Bredin SSD, Warburton DER. Temporal changes in cardiac output during arm cycle versus hybrid exercise in persons with spinal cord injury and able-bodied individuals. Med Sci Sports Exerc 2009; 41: s131.
82. Gonzalez-Alonso J, Mortensen SP, Jeppesen TD, Ali L, Barker H, Damsgaard R et al. Haemodynamic responses to exercise, ATP infusion and thigh compression in humans: insight into the role of muscle mechanisms on cardiovascular function. J Physiol 2008; 586: 2405-2417. (Pubitemid 351619188)
83. Ballaz L. Does passive cycling induce changes in peripheral blood flow in persons with spinal cord injury? The author responds. Arch Phys Med Rehabil 2007; 88: 1741.