Passive hind-limb cycling improves cardiac function and reduces cardiovascular disease risk in experimental spinal cord injury

Journal of Physiology

Volumn 592, Issue 8, 2014, Pages 1771-1783

  West, Christopher R ^a   Crawford, Mark A ^a   Poormasjedi Meibod, Malihe Sadat ^a   Currie, Katharine D ^a   Fallavollita, Andre ^a   Yuen, Violet ^a   Mcneill, John H ^a   Krassioukov, Andrei V ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b Vancouver Costal Health   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN; LIPID; MESSENGER RNA; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; LOW DENSITY LIPOPROTEIN; MADH3 PROTEIN, RAT; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; CYCLING; DOWN REGULATION; EX VIVO STUDY; HEART FUNCTION; HEART LEFT VENTRICLE CONTRACTILITY; HEART LEFT VENTRICLE FUNCTION; HEART LEFT VENTRICLE SIZE; HEART PROTECTION; HINDLIMB; IN VIVO STUDY; LIPID BLOOD LEVEL; MALE; NONHUMAN; PASSIVE MOVEMENT; PRIORITY JOURNAL; RAT; RISK REDUCTION; SPINAL CORD INJURY; UPREGULATION; ANIMAL; BLOOD; CARDIOVASCULAR DISEASES; COMPLICATION; ECHOGRAPHY; GENETICS; HEART CONTRACTION; HEART MUSCLE; HEART VENTRICLE; HEART VENTRICLE FUNCTION; HEMODYNAMICS; METABOLISM; MOVEMENT (PHYSIOLOGY); PATHOPHYSIOLOGY; PHYSIOLOGY; WISTAR RAT;

ANIMALS; CARDIOVASCULAR DISEASES; COLLAGEN; HEART VENTRICLES; HEMODYNAMICS; HINDLIMB; LIPOPROTEINS, LDL; MALE; MOVEMENT; MYOCARDIAL CONTRACTION; MYOCARDIUM; RATS; RATS, WISTAR; SMAD3 PROTEIN; SPINAL CORD INJURIES; TRANSFORMING GROWTH FACTOR BETA; VENTRICULAR FUNCTION;

EID: 84898460289     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.268367     Document Type: Article

References (56)

1. Alan N, Ramer LM, Inskip JA, Golbidi S, Ramer MS, Laher I & Krassioukov AV (2011). Recurrent autonomic dysreflexia exacerbates vascular dysfunction after spinal cord injury. Spine J 10, 1108-1117.
2. Ashley EA, Laskin JJ, Olenik LM, Burnham R, Steadward RD, Cumming DC & Wheeler GD (1993). Evidence of autonomic dysreflexia during functional electrical stimulation in individuals with spinal cord injuries. Paraplegia 31, 593-605.
3. Bauman WA, Adkins RH, Spungen AM & Waters RL (1999). The effect of residual neurological deficit on oral glucose tolerance in persons with chronic spinal cord injury. Spinal Cord 37, 765-771.
4. Bauman WA & Spungen AM (2008). Coronary heart disease in individuals with spinal cord injury: assessment of risk factors. Spinal Cord 46, 466-476.
5. Bujak M, Ren G, Kweon HJ, Dobaczewski M, Reddy A, Taffet G, Wang X-F & Frangogiannis NG (2007). Essential role of Smad3 in infarct healing and in the pathogenesis of cardiac remodeling. Circulation 116, 2127-2138.
6. Cowan RE & Nash MS (2010). Cardiovascular disease, SCI and exercise: unique risks and focused countermeasures. Disabil Rehabil 32, 2228-2236.
7. Cragg JJ, Noonan VK, Krassioukov A & Borisoff J (2013). Cardiovascular disease and spinal cord injury: results from a national population health survey. Neurology 81, 723-728.
8. Cybulski GR, Penn RD & Jaeger RJ (1984). Lower extremity functional neuromuscular stimulation in cases of spinal cord injury. Neurosurgery 15, 132-146.
9. Davis GM, Shephard RJ & Leenen FH (1987). Cardiac effects of short term arm crank training in paraplegics: echocardiographic evidence. Eur J Appl Physiol Occup Physiol 56, 90-96.
10. de Groot PC, Hjeltnes N, Heijboer AC, Stal W & Birkeland K (2003). Effect of training intensity on physical capacity, lipid profile and insulin sensitivity in early rehabilitation of spinal cord injured individuals. Spinal Cord 41, 673-679.
11. de Groot PC, van Dijk A, Dijk E & Hopman MT (2006). Preserved cardiac function after chronic spinal cord injury. Arch Phys Med Rehabil 87, 1195-1200.
12. Després JP, Moorjani S, Lupien PJ, Tremblay A, Nadeau A & Bouchard C (1990). Regional distribution of body fat, plasma lipoproteins, and cardiovascular disease. Arteriosclerosis 10, 497-511.
13. Edwards LA, Bugaresti JM & Buchholz AC (2008). Visceral adipose tissue and the ratio of visceral to subcutaneous adipose tissue are greater in adults with than in those without spinal cord injury, despite matching waist circumferences. Am J Clin Nutr 87, 600-607.
14. Eltorai I, Kim R, Vulpe M, Kasravi H & Ho W (1992). Fatal cerebral hemorrhage due to autonomic dysreflexia in a tetraplegic patient: case report and review. Paraplegia 30, 355-360.
15. Figoni SF, Rodgers MM, Glaser RM, Hooker SP, Feghri PD, Ezenwa BN, Mathews T, Suryaprasad AG & Gupta SC (1990). Physiologic responses of paraplegics and quadriplegics to passive and active leg cycle ergometry. J Am Paraplegia Soc 13, 33-39.
16. Friedewald WT, Levy RI & Fredrickson DS (1972). Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18, 499-502.
17. Garshick E, Kelley A, Cohen SA, Garrison A, Tun CG, Gagnon D & Brown R (2005). A prospective assessment of mortality in chronic spinal cord injury. Spinal Cord 43, 408-416.
18. Gater DR, Jr (2007). Obesity after spinal cord injury. Phys Med Rehabil Clin N Am 18, 333-351, vii.
19. Gates PE, Campbell IG & George KP (2002). Absence of training-specific cardiac adaptation in paraplegic athletes. Med Sci Sports Exerc 34, 1699-1704.
20. Groah SL, Weitzenkamp D, Sett P, Soni B & Savic G (2001). The relationship between neurological level of injury and symptomatic cardiovascular disease risk in the aging spinal injured. Spinal Cord 39, 310-317.
21. Gupta N, White KT & Sandford PR (2006). Body mass index in spinal cord injury - a retrospective study. Spinal Cord 44, 92-94.
22. Hooker SP & Wells CL (1989). Effects of low- and moderate-intensity training in spinal cord-injured persons. Med Sci Sports Exerc 21, 18-22.
23. Hopman MT, Oeseburg B & Binkhorst RA (1992). Cardiovascular responses in paraplegic subjects during arm exercise. Eur J Appl Physiol Occup Physiol 65, 73-78.
24. Houle JD, Morris K, Skinner RD, Garcia-Rill E & Peterson CA (1999). Effects of fetal spinal cord tissue transplants and cycling exercise on the soleus muscle in spinalized rats. Muscle Nerve 22, 846-856.
25. Huonker M, Schmid A, Sorichter S, Schmidt-Trucksab A, Mrosek P & Keul J (1998). Cardiovascular differences between sedentary and wheelchair-trained subjects with paraplegia. Med Sci Sports Exerc 30, 609-613.
26. Hutchinson KJ, Gomez-Pinilla F, Crowe MJ, Ying Z & Basso DM (2004). Three exercise paradigms differentially improve sensory recovery after spinal cord contusion in rats. Brain 127, 1403-1414.
27. Inskip J, Plunet W, Ramer L, Ramsey JB, Yung A, Kozlowski P, Ramer M & Krassioukov A (2010). Cardiometabolic risk factors in experimental spinal cord injury. J Neurotrauma 27, 275-285.
28. Kehat I & Molkentin JD (2010). Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation 122, 2727-2735.
29. Kessler KM, Pina I, Green B, Burnett B, Laighold M, Bilsker M, Palomo AR & Myerburg RJ (1986). Cardiovascular findings in quadriplegic and paraplegic patients and in normal subjects. Am J Cardiol 58, 525-530.
30. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM & Itescu S (2001). Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7, 430-436.
31. Krassioukov AV & Weaver LC (1996). Morphological changes in sympathetic preganglionic neurons after spinal cord injury in rats. Neuroscience 70, 211-225.
32. Levine BD, Zuckerman JH & Pawelczyk JA (1997). Cardiac atrophy after bed-rest deconditioning: a nonneural mechanism for orthostatic intolerance. Circulation 96, 517-525.
33. Lin G, Craig GP, Zhang L, Yuen VG, Allard M, McNeill JH & MacLeod KM (2007). Acute inhibition of Rho-kinase improves cardiac contractile function in streptozotocin-diabetic rats. Cardiovasc Res 75, 51-58.
34. Lujan HL & DiCarlo SE (2007). T5 spinal cord transection increases susceptibility to reperfusion-induced ventricular tachycardia by enhancing sympathetic activity in conscious rats. Am J Physiol Heart Circ Physiol 293, H3333-3339.
35. Lujan HL, Janbaih H & Dicarlo SE (2012). Dynamic interaction between the heart and its sympathetic innervation following T5 spinal cord transection. J Appl Physiol 113, 1332-1341.
36. Lujan HL, Palani G & DiCarlo SE (2010). Structural neuroplasticity following T5 spinal cord transection: increased cardiac sympathetic innervation density and SPN arborization. Am J Physiol Regul Integr Comp Physiol 299, R985-R995.
37. Mihl C, Dassen WR & Kuipers H (2008). Cardiac remodelling: concentric versus eccentric hypertrophy in strength and endurance athletes. Neth Heart J 16, 129-133.
38. Morganroth J, Maron BJ, Henry WL & Epstein SE (1975). Comparative left ventricular dimensions in trained athletes. Ann Intern Med 82, 521-524.
39. Nash MS, Bilsker MS, Kearney HM, Ramirez JN, Applegate B & Green BA (1995). Effects of electrically-stimulated exercise and passive motion on echocardiographically-derived wall motion and cardiodynamic function in tetraplegic persons. Paraplegia 33, 80-89.
40. Nash MS, Bilsker S, Marcillo AE, Isaac SM, Botelho LA, Klose KJ, Green BA, Rountree MT & Shea JD (1991). Reversal of adaptive left ventricular atrophy following electrically-stimulated exercise training in human tetraplegics. Paraplegia 29, 590-599.
41. Nash MS & Jacobs PL (1998). Cardiac structure and function in exercise trained and sedentary persons with paraplegia. Med Sci Sports Exerc 30, 1336-1338.
42. Perhonen MA, Franco F, Lane LD, Buckey JC, Blomqvist CG, Zerwekh JE, Peshock RM, Weatherall PT & Levine BD (2001). Cardiac atrophy after bed rest and spaceflight. J Appl Physiol 91, 645-653.
43. Phillips AA, Cote AT & Warburton DE (2011). A systematic review of exercise as a therapeutic intervention to improve arterial function in persons living with spinal cord injury. Spinal Cord 49, 702-714.
44. Pluim BM, Zwinderman AH, van der Laarse A & van der Wall EE (2000). The athlete's heart: a meta-analysis of cardiac structure and function. Circulation 101, 336-344.
45. Rabchevsky AG, Patel SP, Lyttle TS, Eldahan KC, O'Dell CR, Zhang Y, Popovich PG, Kitzman PH & Donohue KD (2012). Effects of gabapentin on muscle spasticity and both induced as well as spontaneous autonomic dysreflexia after complete spinal cord injury. Front Physiol 3, 329.
46. Ramsey JB, Ramer LM, Inskip JA, Alan N, Ramer MS & Krassioukov AV (2010). Care of rats with complete high-thoracic spinal cord injury. J Neurotrauma 27, 1709-1722.
47. Sandrow-Feinberg HR, Izzi J, Shumsky JS, Zhukareva V & Houle JD (2009). Forced exercise as a rehabilitation strategy after unilateral cervical spinal cord contusion injury. J Neurotrauma 26, 721-731.
48. Solomonow M, Reisin E, Aguilar E, Baratta RV, Best R & D'Ambrosia R (1997). Reciprocating gait orthosis powered with electrical muscle stimulation (RGO II). Part II: Medical evaluation of 70 paraplegic patients. Orthopedics 20, 411-418.
49. Stewart BG, Tarnopolsky MA, Hicks AL, McCartney N, Mahoney DJ, Staron RS & Phillips SM (2004). Treadmill training-induced adaptations in muscle phenotype in persons with incomplete spinal cord injury. Muscle Nerve 30, 61-68.
50. Teasell RW, Arnold JM, Krassioukov A & Delaney GA (2000). Cardiovascular consequences of loss of supraspinal control of the sympathetic nervous system after spinal cord injury. Arch Phys Med Rehabil 81, 506-516.
51. Ter Woerds W, De Groot PC, van Kuppevelt DH & Hopman MT (2006). Passive leg movements and passive cycling do not alter arterial leg blood flow in subjects with spinal cord injury. Phys Ther 86, 636-645.
52. Vague J (1947). La différenciation sexuelle, facteur déterminant des formes de l'obésité. Presse Med 55, 339-344.
53. Washburn RA, Savage DD, Dearwater SR, LaPorte RE, Anderson SJ, Brenes G, Adams LL, Lee HK, Holland J, Cowan M, et al (1986). Echocardiographic left ventricular mass and physical activity: quantification of the relation in spinal cord injured and apparently healthy active men. Am J Cardiol 58, 1248-1253.
54. West CR, Campbell IG, Shave RE & Romer LM (2012a). Resting cardiopulmonary function in Paralympic athletes with cervical spinal cord injury. Med Sci Sports Exerc 44, 323-329.
55. West CR, Mills P & Krassioukov AV (2012b). Influence of the neurological level of spinal cord injury on cardiovascular outcomes in humans: a meta-analysis. Spinal Cord 50, 484-492.
56. Zhang Q, Fung JW, Auricchio A, Chan JY, Kum LC, Wu LW & Yu CM (2006). Differential change in left ventricular mass and regional wall thickness after cardiac resynchronization therapy for heart failure. Eur Heart J 27, 1423-1430.