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Alterations in Cardiac Electrophysiology After Spinal Cord Injury and Implications for Exercise

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The Physiology of Exercise in Spinal Cord Injury

Abstract

When the spinal cord is injured at or below thoracic level 5 (T5), cardiovascular control is markedly unbalanced as the heart and blood vessels innervated by upper thoracic segments remain under brain stem control, whereas the vasculature of the lower body is affected by unregulated spinal reflexes. As a result, mid-thoracic spinal cord injury (SCI) results in chronic arterial pressure and cardiac volume unloading due to a rapid and sustained reduction in arterial pressure, venous return and end-diastolic volume, secondary to the loss of sympathetic vasoconstrictor tone below the level of the injury. The resulting hypotension and reduced cardiac filling initiates a dramatic and immediate reflex increase in sympathetic outflow and decrease in parasympathetic outflow to the heart. These high levels of sympathetic outflow and reduced parasympathetic outflow following mid-thoracic SCI have been reported to induce calcium overload, left ventricular dysfunction, cardiac injury and ST-segment elevation. The myocardial damage also promotes nerve growth factor-induced sympathetic sprouting, hyper-innervation of the heart and pathological neuroplasticity in the autonomic ganglia, spinal cord and autonomic centers within the brainstem. Pathological neuroplasticity following SCI is associated with many lingering complications such as chronic pain, spasticity, neurogenic bladder, and autonomic dysreflexia. Pathological neuroplasticity is also associated with changes in cardiac electrophysiology and an increased susceptibility to life-threatening ventricular arrhythmias. These complications are exacerbated by the sedentary lifestyle of the typical individual with SCI. Regular exercise may exert a protective effect via an increased plasma volume, increased venous return and a subsequent volume loading of the heart, which in turn maintains contractile function, arterial pressure and reduces sympathetic sprouting, hyper-innervation and pathological neuroplasticity.

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References

  • Alan N, Ramer LM, Inskip JA, Golbidi S, Ramer MS, Laher I, Krassioukov AV (2010) Recurrent autonomic dysreflexia exacerbates vascular dysfunction after spinal cord injury. Spine J 10(12):1108–1117

    Article  PubMed  Google Scholar 

  • Anderson KD (2004) Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma 21(10):1371–1383

    Article  PubMed  Google Scholar 

  • Arnold JM, Feng QP, Delaney GA, Teasell RW (1995) Autonomic dysreflexia in tetraplegic patients: evidence for alpha-adrenoceptor hyper-responsiveness. Clin Auton Res 5(5):267–270

    Article  CAS  PubMed  Google Scholar 

  • 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(9):593–605

    Article  CAS  PubMed  Google Scholar 

  • Bartholdy K, Biering-Sorensen T, Malmqvist L, Ballegaard M, Krassioukov A, Hansen B, Svendsen JH, Kruse A, Welling KL, Biering-Sorensen F (2014) Cardiac arrhythmias the first month after acute traumatic spinal cord injury. J Spinal Cord Med 37(2):162–170

    Article  PubMed  PubMed Central  Google Scholar 

  • Bauman WA, Spungen AM (2008) Coronary heart disease in individuals with spinal cord injury: assessment of risk factors. Spinal Cord 46(7):466–476

    Article  CAS  PubMed  Google Scholar 

  • 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(11):765–771

    Article  CAS  PubMed  Google Scholar 

  • Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415(6868):198–205

    Article  CAS  PubMed  Google Scholar 

  • Billman GE (2009) Cardiac autonomic neural remodeling and susceptibility to sudden cardiac death: effect of endurance exercise training. Am J Physiol Heart Circ Physiol 297(4):H1171–H1193

    Article  CAS  PubMed  Google Scholar 

  • Bourke JP, Richards DA, Ross DL, McGuire MA, Uther JB (1995) Does the induction of ventricular flutter or fibrillation at electrophysiologic testing after myocardial infarction have any prognostic significance? Am J Cardiol 75(7):431–435. doi:S0002914999805761 [pii]

    Google Scholar 

  • Brock JA, Yeoh M, McLachlan EM (2006) Enhanced neurally evoked responses and inhibition of norepinephrine reuptake in rat mesenteric arteries after spinal transection. Am J Physiol Heart Circ Physiol 290(1):H398–H405

    Article  CAS  PubMed  Google Scholar 

  • Brown A, Weaver LC (2011) The dark side of neuroplasticity. Exp Neurol 235(1):133–141

    Article  PubMed  PubMed Central  Google Scholar 

  • Calaresu FR, Yardley CP (1988) Medullary basal sympathetic tone. Annu Rev Physiol 50:511–524

    Article  CAS  PubMed  Google Scholar 

  • Chen C-Y, DiCarlo SE (1997) Endurance exercise training-induced resting bradycardia: a brief review. Sports Med Train Rehabil 8:37–77

    Article  Google Scholar 

  • Clausen JP, Trap-Jensen J, Lassen NA (1970) The effects of training on the heart rate during arm and leg exercise. Scand J Clin Lab Invest 26(3):295–301

    Article  CAS  PubMed  Google Scholar 

  • Claydon VE, Elliott SL, Sheel AW, Krassioukov A (2006) Cardiovascular responses to vibrostimulation for sperm retrieval in men with spinal cord injury. J Spinal Cord Med 29(3):207–216

    Article  PubMed  PubMed Central  Google Scholar 

  • Collins HL, DiCarlo SE (2002a) Acute exercise reduces the response to colon distension in T(5) spinal rats. Am J Physiol Heart Circ Physiol 282(4):1566–1570

    Article  Google Scholar 

  • Collins HL, DiCarlo SE (2002b) TENS attenuates response to colon distension in paraplegic and quadriplegic rats. Am J Physiol Heart Circ Physiol 283(4):1734–1739

    Article  Google Scholar 

  • Collins HL, Rodenbaugh DW, DiCarlo SE (2006) Spinal cord injury alters cardiac electrophysiology and increases the susceptibility to ventricular arrhythmias. Prog Brain Res 152:275–288

    Article  PubMed  Google Scholar 

  • Coote JH (2013) Myths and realities of the cardiac vagus. J Physiol 591(17):4073–4085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corbett JL, Debarge O, Frankel HL, Mathias C (1975) Cardiovascular responses in tetraplegic man to muscle spasm, bladder percussion and head-up tilt. Clin Exp Pharmacol Physiol (Suppl 2):189–193

    Google Scholar 

  • Courtois F, Geoffrion R, Landry E, Belanger M (2004) H-reflex and physiologic measures of ejaculation in men with spinal cord injury. Arch Phys Med Rehabil 85(6):910–918

    Article  PubMed  Google Scholar 

  • Cowan RE, Nash MS (2010) Cardiovascular disease, SCI and exercise: unique risks and focused countermeasures. Disabil Rehabil 32(26):2228–2236

    Article  PubMed  Google Scholar 

  • Cragg JJ, Noonan VK, Krassioukov A, Borisoff J (2013) Cardiovascular disease and spinal cord injury: results from a national population health survey. Neurology 81(8):723–728

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis GM, Shephard RJ (1988) Cardiorespiratory fitness in highly active versus inactive paraplegics. Med Sci Sports Exerc 20(5):463–468

    Article  CAS  PubMed  Google Scholar 

  • 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(1):90–96

    Article  CAS  PubMed  Google Scholar 

  • de Groat WC, Kawatani M, Hisamitsu T, Cheng CL, Ma CP, Thor K, Steers W, Roppolo JR (1990) Mechanisms underlying the recovery of urinary bladder function following spinal cord injury. J Auton Nerv Syst 30(Suppl):S71–S77

    Article  PubMed  Google Scholar 

  • DeVivo MJ, Black KJ, Stover SL (1993) Causes of death during the first 12 years after spinal cord injury. Arch Phys Med Rehabil 74:248–254

    CAS  PubMed  Google Scholar 

  • DeVivo MJ, Shewchuk RM, Stover SL, Black KJ, Go BK (1992) A cross-sectional study of the relationship between age and current health status for persons with spinal cord injuries. Paraplegia 30:820–827

    Article  CAS  PubMed  Google Scholar 

  • DiCarlo SE (1982) Improved cardiopulmonary status after a two-month program of graded arm exercise in a patient with C6 quadriplegia: a case report. Phys Ther 62(4):456–459

    CAS  PubMed  Google Scholar 

  • DiCarlo SE (1988) Effect of arm ergometry training on wheelchair propulsion endurance of individuals with quadriplegia. Phys Ther 68(1):40–44

    CAS  PubMed  Google Scholar 

  • DiCarlo SE, Bishop VS (1999) Exercise and the autonomic nervous system. In: Appenzeller O (ed) Handbook of clinical neurology, the autonomic nervous system. Part 1. Normal functions, Chap 8. Elsevier Science, Amsterdam

    Google Scholar 

  • DiCarlo SE, Supp MD, Taylor HC (1983) Effect of arm ergometry training on physical work capacity of individuals with spinal cord injuries. Phys Ther 63(7):1104–1107

    CAS  PubMed  Google Scholar 

  • DiCarlo SE, Blair RW, Bishop VS, Stone HL (1989) Daily exercise enhances coronary resistance vessel sensitivity to pharmacological activation. J Appl Physiol 66:421–428

    CAS  PubMed  Google Scholar 

  • DiCarlo SE, Collins HL, Howard MG, Chen C-Y, Scislo TJ, Patil RD (1994) Postexertional hypotension: a brief review. Sports Med Train Rehab 5:17–27

    Article  Google Scholar 

  • DiCarlo SE, Patil RD, Collins HL, Chen C-Y (1995) Local modulation of adrenergic responses in the hindlimb vasculature of the intact conscious rat. J Physiol 485(3):817–825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drummond MJ, Glynn EL, Lujan HL, DiCarlo SE, Rasmussen BB (2008) Gene and protein expression associated with protein synthesis and breakdown in paraplegic skeletal muscle. Muscle Nerve 37(4):505–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(3):600–607

    CAS  PubMed  Google Scholar 

  • Ekblom B, Lundberg A (1967) Effect of physical training on school-children with severe motor handicaps. Acta Paediatr Scand (Suppl 177):164–175

    Google Scholar 

  • Engel GL (1978) Psychologic stress, vasodepressor (vasovagal) syncope, and sudden death. Ann Intern Med 89(3):403–412

    Article  CAS  PubMed  Google Scholar 

  • Faghri PD, Yount JP, Pesce WJ, Seetharama S, Votto JJ (2001) Circulatory hypokinesis and functional electric stimulation during standing in persons with spinal cord injury. Arch Phys Med Rehabil 82(11):1587–1595

    Article  CAS  PubMed  Google Scholar 

  • Forrest GP (1991) Atrial fibrillation associated with autonomic dysreflexia in patients with tetraplegia. Arch Phys Med Rehabil 72:592–594

    CAS  PubMed  Google Scholar 

  • Fouad K, Pedersen V, Schwab ME, Brosamle C (2001) Cervical sprouting of corticospinal fibers after thoracic spinal cord injury accompanies shifts in evoked motor responses. Curr Biol 11(22):1766–1770

    Article  CAS  PubMed  Google Scholar 

  • Frattola A, Parati G, Cuspidi C, Albini F, Mancia G (1993) Prognostic value of 24-hour blood pressure variability. J Hypertens 11:1133–1137

    Article  CAS  PubMed  Google Scholar 

  • Fry CS, Drummond MJ, Lujan HL, DiCarlo SE, Rasmussen BB (2012) Paraplegia increases skeletal muscle autophagy. Muscle Nerve 46(5):793–798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(7):408–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gass GC, Camp EM (1979) Physiological characteristics of trained Australian paraplegic and tetraplegic subjects. Med Sci Sports 11(3):256–259

    CAS  PubMed  Google Scholar 

  • Gates PE, Campbell IG, George KP (2002) Absence of training-specific cardiac adaptation in paraplegic athletes. Med Sci Sports Exerc 34(11):1699–1704

    Article  PubMed  Google Scholar 

  • Glaser RM (1985) Exercise and locomotion for the spinal cord injured. Exerc Sport Sci Rev 13:263–303

    Article  CAS  PubMed  Google Scholar 

  • Glaser RM, Davis GM (1988) Wheelchair dependent individuals. Exercise in modern medicine. Williams & Wilkins, Baltimore

    Google Scholar 

  • Glynn EL, Lujan HL, Kramer VJ, Drummond MJ, DiCarlo SE, Rasmussen BB (2008) A chronic increase in physical activity inhibits fed-state mTOR/S6K1 signaling and reduces IRS-1 serine phosphorylation in rat skeletal muscle. Appl Physiol Nutr Metab 33(1):93–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldberg AP (1989) Aerobic and resistive exercise modify risk factors for coronary heart disease. Med Sci Sports Exerc 21 (6):669–674

    Article  CAS  PubMed  Google Scholar 

  • Golden KL, Fan QI, Chen B, Ren J, O’Connor J, Marsh JD (2000) Adrenergic stimulation regulates Na(+)/Ca(2+) exchanger expression in rat cardiac myocytes. J Mol Cell Cardiol 32(4):611–620

    Article  CAS  PubMed  Google Scholar 

  • Golden KL, Ren J, O’Connor J, Dean A, DiCarlo SE, Marsh JD (2001) In vivo regulation of Na/Ca exchanger expression by adrenergic effectors. Am J Physiol Heart Circ Physiol 280:H1376–H1382

    CAS  PubMed  Google Scholar 

  • Goldspink DF, Burniston JG, Ellison GM, Clark WA, Tan LB (2004) Catecholamine-induced apoptosis and necrosis in cardiac and skeletal myocytes of the rat in vivo: the same or separate death pathways? Exp Physiol 89(4):407–416

    Article  CAS  PubMed  Google Scholar 

  • Graitcer PL, Maynard FM (eds) (1991) Centers for Disease Control Cardiovascular-cardiopulmonary secondary disabilities. In: Proceedings of the first colloquium on preventing secondary disabilities among people with spinal cord injuries, CDC, Atlanta, GA, 1990. US Dept of Health and Human Services, Washington DC, pp 47–54

    Google Scholar 

  • 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(6):310–317

    Article  CAS  PubMed  Google Scholar 

  • Gupta N, White KT, Sandford PR (2006) Body mass index in spinal cord injury—a retrospective study. Spinal Cord 44(2):92–94

    Article  CAS  PubMed  Google Scholar 

  • Guttmann L, Frankel HL, Paeslack V (1965) Cardiac irregularities during labour in paraplegic women. Paraplegia 3:144–151

    Article  CAS  PubMed  Google Scholar 

  • Halliwill JR (2001) Mechanisms and clinical implications of post-exercise hypotension in humans. Exerc Sport Sci Rev 29:65–70

    Article  CAS  PubMed  Google Scholar 

  • Halliwill JR, Taylor JA, Eckberg DL (1996) Impaired sympathetic vascular regulation in humans after acute dynamic exercise. J Physiol 495:279–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hector SM, Biering-Sorensen T, Krassioukov A, Biering-Sorensen F (2013) Cardiac arrhythmias associated with spinal cord injury. J Spinal Cord Med 36(6):591–599

    Article  PubMed  PubMed Central  Google Scholar 

  • Helmi M, Lima A, Gommers D, van Bommel J, Bakker J (2013) Inflatable external leg compression prevents orthostatic hypotension in a patient with a traumatic cervical spinal cord injury. Future Cardiol 9(5):645–648

    Article  CAS  PubMed  Google Scholar 

  • Hill CE, Beattie MS, Bresnahan JC (2001) Degeneration and sprouting of identified descending supraspinal axons after contusive spinal cord injury in the rat. Exp Neurol 171(1):153–169

    Article  CAS  PubMed  Google Scholar 

  • Hopman MT, Oeseburg B, Binkhorst RA (1992) The effect of an anti-G suit on cardiovascular responses to exercise in persons with paraplegia. Med Sci Sports Exerc 24(9):984–990

    Article  CAS  PubMed  Google Scholar 

  • Hopman MT, Kamerbeek IC, Pistorius M, Binkhorst RA (1993) The effect of an anti-G suit on the maximal performance of individuals with paraplegia. Int J Sports Med 14(7):357–361

    Article  CAS  PubMed  Google Scholar 

  • Hou S, Duale H, Cameron AA, Abshire SM, Lyttle TS, Rabchevsky AG (2008) Plasticity of lumbosacral propriospinal neurons is associated with the development of autonomic dysreflexia after thoracic spinal cord transection. J Comp Neurol 509(4):382–399

    Article  PubMed  PubMed Central  Google Scholar 

  • Howard MG, DiCarlo SE (1992) Reduced vascular responsiveness after a single bout of dynamic exercise in the conscious rabbit. J Appl Physiol 73:2662–2667

    CAS  PubMed  Google Scholar 

  • Howard MG, DiCarlo SE, Stallone JN (1992) Acute exercise attenuates phenylephrine-induced contraction of rabbit isolated aortic rings. Med Sci Sports Exerc 24:1102–1107

    Article  CAS  PubMed  Google Scholar 

  • 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(4):609–613

    Article  CAS  PubMed  Google Scholar 

  • Inskip JA, Ramer LM, Ramer MS, Krassioukov AV (2009) Autonomic assessment of animals with spinal cord injury: tools, techniques and translation. Spinal Cord 47(1):2–35

    Article  CAS  PubMed  Google Scholar 

  • 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(1):275–285

    Article  PubMed  Google Scholar 

  • Jacobs PL, Nash MS (2004) Exercise recommendations for individuals with spinal cord injury. Sports Med 34(11):727–751

    Article  PubMed  Google Scholar 

  • Jacobs PL, Mahoney ET, Robbins A, Nash M (2002) Hypokinetic circulation in persons with paraplegia. Med Sci Sports Exerc 34(9):1401–1407

    Article  PubMed  Google Scholar 

  • Ji Y, Lalli MJ, Babu GJ, Xu Y, Kirkpatrick DL, Liu LH, Chiamvimonvat N, Walsh RA, Shull GE, Periasamy M (2000) Disruption of a single copy of the SERCA2 gene results in altered Ca2+ homeostasis and cardiomyocyte function. J Biol Chem 275(48):38073–38080

    Article  CAS  PubMed  Google Scholar 

  • Julius S, Valentini M (1998) Consequences of the increased autonomic nervous drive in hypertension, heart failure and diabetes. Blood Press Suppl 3:5–13

    CAS  PubMed  Google Scholar 

  • Kerk JK, Clifford PS, Snyder AC, Prieto TE, O’Hagan KP, Schot PK, Myklebust JB, Myklebust BM (1995) Effect of an abdominal binder during wheelchair exercise. Med Sci Sports Exerc 27(6):913–919

    Article  CAS  PubMed  Google Scholar 

  • 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(6):525–530

    Article  CAS  PubMed  Google Scholar 

  • Kinzer SM, Convertino VA (1989) Role of leg vasculature in the cardiovascular response to arm work in wheelchair-dependent populations. Clin Physiol 9(6):525–533

    Article  CAS  PubMed  Google Scholar 

  • Knutsson E, Lewenhaupt-Olsson E, Thorsen M (1973) Physical work capacity and physical conditioning in paraplegic patients. Paraplegia 11(3):205–216

    Article  CAS  PubMed  Google Scholar 

  • Krassioukov AV, Weaver LC (1995) Reflex and morphological changes in spinal preganglionic neurons after cord injury in rats. Clin Exp Hypertens 17(1–2):361–373

    Article  CAS  PubMed  Google Scholar 

  • Krenz NR, Meakin SO, Krassioukov AV, Weaver LC (1999) Neutralizing intraspinal nerve growth factor blocks autonomic dysreflexia caused by spinal cord injury. J Neurosci 19:7405–7414

    CAS  PubMed  Google Scholar 

  • Laird AS, Carrive P, Waite PM (2009) Effect of treadmill training on autonomic dysreflexia in spinal cord—injured rats. Neurorehabil Neural Repair 23(9):910–920

    Article  PubMed  Google Scholar 

  • Le CT, Price M (1982) Survival from spinal cord injury. J Chronic Dis 35:487–492

    Article  CAS  PubMed  Google Scholar 

  • Levi-Montalcini R (1976) The nerve growth factor: its role in growth, differentiation and function of the sympathetic adrenergic neuron. Prog Brain Res 45:235–258

    Article  CAS  PubMed  Google Scholar 

  • Llewellyn-Smith IJ, Weaver LC (2001) Changes in synaptic inputs to sympathetic preganglionic neurons after spinal cord injury. J Comp Neurol 435(2):226–240

    Article  CAS  PubMed  Google Scholar 

  • Llewellyn-Smith I, Martin C, Fenwick N, DiCarlo S, Lujan H, Schreihofer A (2007) VGLUT1 and VGLUT2 innvervation in autonomic regions of intact and transected rat spinal cord. J Comp Neur 503(6):741–767

    Article  CAS  PubMed  Google Scholar 

  • Loewy A, Spyer K (1990) Vagal preganglionic neurons. In: Loewy A, Spyer K (eds) Central regulation of autonomic functions. Oxford University Press, New York, pp. 68–87

    Google Scholar 

  • 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(6):H3333–H3339

    Article  CAS  PubMed  Google Scholar 

  • Lujan HL, DiCarlo SE (2014) Increasing venous return as a strategy to prevent or reverse cardiac dysfunction following spinal cord injury. J Physiol 592(8):1727–1728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lujan HL, Chen Y, DiCarlo SE (2009) Paraplegia increased cardiac NGF content, sympathetic tonus and the susceptibility to ischemia-induced ventricular tachycardia in conscious rats. Am J Physiol Heart Circ Physiol 296(5):H1364–H1372

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lujan HL, Palani G, DiCarlo SE (2010a) Structural neuroplasticity following T5 spinal cord transection: increased cardiac sympathetic innervation density and SPN arborization. Am J Physiol Regul Integr Comp Physiol 299(4):R985–R995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lujan HL, Palani G, Peduzzi JD, DiCarlo SE (2010b) Targeted ablation of mesenteric projecting sympathetic neurons reduces the hemodynamic response to pain in conscious, spinal cord-transected rats. Am J Physiol Regul Integr Comp Physiol 298(5):R1358–R1365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(8):1332–1341

    Article  PubMed  PubMed Central  Google Scholar 

  • Lujan HL, Janbaih H, DiCarlo SE (2014) Structural remodeling of the heart and its premotor cardioinhibitory vagal neurons following T(5) spinal cord transection. J Appl Physiol 116(9):1148–1155

    Article  PubMed  PubMed Central  Google Scholar 

  • Maiorov DN, Weaver LC, Krassioukov AV (1997) Relationship between sympathetic activity and arterial pressure in conscious spinal rats. Am J Physiol Heart Circ Physiol 272:H625–H631

    CAS  Google Scholar 

  • Marx SO, Reiken S, Hisamatsu Y, Jayaraman T, Burkhoff D, Rosemblit N, Marks AR (2000) PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101(4):365–376

    Article  CAS  PubMed  Google Scholar 

  • Mathias CJ, Frankel HL (1983) Clinical manifestations of malfunctioning sympathetic mechanisms in tetraplegia. J Auton Nerv Sys 7:303–312

    Article  CAS  Google Scholar 

  • Mathias CJ, Frankel HL (1992) The cardiovascular system in tetraplegia and paraplegia. In: Handbook of clinical neurology. Elsevier, Amsterdam, pp. 435–456

    Google Scholar 

  • Mayorov DN, Adams MA, Krassioukov AV (2001) Telemetric blood pressure monitoring in conscious rats before and after compression injury of spinal cord. J Neurotrauma 18(7):727–736

    Article  CAS  PubMed  Google Scholar 

  • McGuire TJ, Kumar VN (1986) Autonomic dysreflexia in the spinal cord injured: what the physician should know about this medical emergency. Postgrad Med 80:81–89

    Article  CAS  PubMed  Google Scholar 

  • McLean KP, Skinner JS (1995) Effect of body training position on outcomes of an aerobic training study on individuals with quadriplegia. Arch Phys Med Rehabil 76(2):139–150

    Article  CAS  PubMed  Google Scholar 

  • Moffitt JA (2010) Editorial Focus: role for neural growth factor in autonomically driven arrhythmogenesis? Focus on: “Structural neuroplasticity following T5 spinal cord transection: increased cardiac sympathetic innervation density and SPN arborization”. Am J Physiol Regul Integr Comp Physiol 299(4):R983–R984

    Article  CAS  PubMed  Google Scholar 

  • Morganroth J, Maron BJ, Henry WL, Epstein SE (1975) Comparative left ventricular dimensions in trained athletes. Ann Intern Med 82(4):521–524

    Article  CAS  PubMed  Google Scholar 

  • Morita S, Inokuchi S, Yamagiwa T, Aoki H, Nakagawa Y, Yamamoto I (2010) Tako-tsubo-like left ventricular dysfunction with ST-segment elevation after central spinal cord injury: a case report. J Emerg Med 39(3):301–304

    Article  PubMed  Google Scholar 

  • Morris JN, Kagen A, Pattison DC, Gardiner MJ (1966) Incidence and prediction of ischemic heart disease in London busmen. Lancet 2:553–559

    Article  CAS  PubMed  Google Scholar 

  • Muller FU, Lewin G, Matus M, Neumann J, Riemann B, Wistuba J, Schutz G, Schmitz W (2003) Impaired cardiac contraction and relaxation and decreased expression of sarcoplasmic Ca2+-ATPase in mice lacking the CREM gene. FASEB J 17(1):103–105

    PubMed  Google Scholar 

  • Naftchi NE (1990) Mechanism of autonomic dysreflexia: contributions of catecholamine and peptide neurotransmitters. Ann New York Acad Sci 579:133–148

    Article  CAS  Google Scholar 

  • Nash MS, Jacobs PL (1998) Cardiac structure and function in exercise trained and sedentary persons with paraplegia. Med Sci Sports Exerc 30(8):1336–1338

    Article  CAS  PubMed  Google Scholar 

  • National Heart Institute (1966) The Framingham heart study: habits and coronary heart disease. U.S. Dept. of Health, Education, and Welfare, Public Health Service, National Heart Institute, Bethesda, MD

    Google Scholar 

  • Naughton JP, Hellerstein HK (1977) Exercise testing and exercise training in coronary heart disease. Academic Press, New York

    Google Scholar 

  • Ondarza AB, Ye Z, Hulsebosch CE (2003) Direct evidence of primary afferent sprouting in distant segments following spinal cord injury in the rat: colocalization of GAP-43 and CGRP. Exp Neurol 184(1):373–380

    Article  CAS  PubMed  Google Scholar 

  • Oscai LB (1973) The role of exercise in weight control. Exerc Sport Sci Rev 1:103–123

    Article  CAS  PubMed  Google Scholar 

  • Paffenbarger RS, Laughlin ME, Gima AS, Black RA (1970) Work activity in longshoreman as related to death from coronary artery disease and stroke. New Engl J Med 282:1109–1114

    Article  PubMed  Google Scholar 

  • Palatini P, Julius S (1997) Association of tachycardia with morbidity and mortality: pathophysiological considerations. J Hum Hypertens 11(Suppl 1):19–27

    Google Scholar 

  • Palatini P, Julius S (1999) Relevance of heart rate as a risk factor in hypertension. Curr Hypertens Rep 1(3):219–224

    Article  CAS  PubMed  Google Scholar 

  • Pan B, Zahner MR, Kulikowicz E, Schramm LP (2007) Effects of corticospinal tract stimulation on renal sympathetic nerve activity in rats with intact and chronically lesioned spinal cords. Am J Physiol Regul Integr Comp Physiol 293(1):178–184

    Article  CAS  Google Scholar 

  • Patil RD, DiCarlo SE, Collins HL (1993) Acute exercise enhances nitric oxide modulation of vascular response to phenylephrine. Am J Physiol Heart Circ Physiol 265:H1184–H1188

    CAS  Google Scholar 

  • Patterson E, Lazzara R, Szabo B, Liu H, Tang D, Li YH, Scherlag BJ, Po SS (2006) Sodium-calcium exchange initiated by the Ca2+ transient: an arrhythmia trigger within pulmonary veins. J Am Coll Cardiol 47(6):1196–1206

    Article  CAS  PubMed  Google Scholar 

  • 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(6):702–714

    Article  CAS  PubMed  Google Scholar 

  • Pine ZM, Miller SD, Alonso JA (1991) Atrial fibrillation associated with autonomic dysreflexia. Am J Phys Med Rehabil 70(5):271–273

    Article  CAS  PubMed  Google Scholar 

  • Pitetti KH, Barrett PJ, Campbell KD, Malzahn DE (1994) The effect of lower body positive pressure on the exercise capacity of individuals with spinal cord injury. Med Sci Sports Exerc 26(4):463–468

    Article  CAS  PubMed  Google Scholar 

  • Pollock ML, Miller HS, Linnerud AC, Laughridge E, Coleman E, Alexander E (1974) Arm pedaling as an endurance training regimen for the disabled. Arch Phys Med Rehabil 55(9):418–424

    CAS  PubMed  Google Scholar 

  • Purves D, Snider WD, Voyvodic JT (1988) Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system. Nature 336(6195):123–128

    Article  CAS  PubMed  Google Scholar 

  • Reeve C (2005) Dedication. In: Weaver L, Polosa C (eds) Progress in brain research, autonomic dysfunction after spinal cord injury. Elsevier Science, The Netherlands, p. ix

    Google Scholar 

  • Reiken S, Gaburjakova M, Guatimosim S, Gomez AM, D’Armiento J, Burkhoff D, Wang J, Vassort G, Lederer WJ, Marks AR (2003) Protein kinase a phosphorylation of the cardiac calcium release channel (ryanodine receptor) in normal and failing hearts. Role of phosphatases and response to isoproterenol. J Biol Chem 278(1):444–453

    Article  CAS  PubMed  Google Scholar 

  • Ressl J, Chrastek J, Jandova R (1977) Haemodynamic effects of physical training in essential hypertension. Lancet (Brux) 32:121–133

    CAS  Google Scholar 

  • Rizzoni D, Muiesan ML, Montani G, Zulli R, Calebich S, Agabiti-Rosei E (1992) Relationship between initial cardiovascular structural changes and daytime and nighttime blood pressure monitoring. Am J Hypertens 5:180–186

    Article  CAS  PubMed  Google Scholar 

  • Rodenbaugh DW, Collins HL, DiCarlo SE (2003a) Increased susceptibility to ventricular arrhythmias in hypertensive paraplegic rats. Clin Exp Hypertens 25(6):349–358

    Article  CAS  PubMed  Google Scholar 

  • Rodenbaugh DW, Collins HL, DiCarlo SE (2003b) Paraplegia differentially increases arterial blood pressure related cardiovascular disease risk factors in normotensive and hypertensive rats. Brain Res 980(8):242–248

    Article  CAS  PubMed  Google Scholar 

  • Rodenbaugh DW, Collins HL, Nowacek DG, DiCarlo SE (2003c) Increased susceptibility to ventricular arrhythmias is associated with changes in Ca2+ regulatory proteins in paraplegic rats. Am J Physiol Heart Circ Physiol 285(6):2605–2613

    Article  Google Scholar 

  • Rosen MR, Reder RF (1981) Does triggered activity have a role in the genesis of cardiac arrhythmias? Ann Intern Med 94(6):794–801

    Article  CAS  PubMed  Google Scholar 

  • Sabbah HN, Shimoyama H, Kono T, Gupta RC, Sharov VG, Scicli G, Levine TB, Goldstein S (1994) Effects of long-term monotherapy with enalapril, metoprolol, and digoxin on the progression of left ventricular dysfunction and dilation in dogs with reduced ejection fraction. Circulation 89(6):2852–2859

    Article  CAS  PubMed  Google Scholar 

  • Sabbah HN, Stanley WC, Sharov VG, Mishima T, Tanimura M, Benedict CR, Hegde S, Goldstein S (2000) Effects of dopamine beta-hydroxylase inhibition with nepicastat on the progression of left ventricular dysfunction and remodeling in dogs with chronic heart failure. Circulation 102(16):1990–1995

    Article  CAS  PubMed  Google Scholar 

  • 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(5 Suppl):Vii1–Vii78

    CAS  PubMed  Google Scholar 

  • Scheuer J, Tipton CM (1977) Cardiovascular adaptations to physical training. Annu Rev Physiol 39:221–251

    Article  CAS  PubMed  Google Scholar 

  • Schwartz PJ, Priori SG, Napolitano C (1993) Role of the autonomic nervous system in sudden cardiac death. In: Josephson ME (ed) Sudden cardiac death. Blackwell Scientific, Cambridge, MA, pp. 16–37

    Google Scholar 

  • Seki S, Sasaki K, Fraser MO, Igawa Y, Nishizawa O, Chancellor MB, de Groat WC, Yoshimura N (2002) Immunoneutralization of nerve growth factor in lumbosacral spinal cord reduces bladder hyperreflexia in spinal cord injured rats. J Urol 168(5):2269–2274

    Article  CAS  PubMed  Google Scholar 

  • Sharov VG, Galakhin KA (1984) Myocardial changes after spinal cord injuries in humans and experimental animals. Arkh Patol 46(5):17–20

    CAS  PubMed  Google Scholar 

  • Shizukuda Y, Buttrick PM, Geenen DL, Borczuk AC, Kitsis RN, Sonnenblick EH (1998) beta-adrenergic stimulation causes cardiocyte apoptosis: influence of tachycardia and hypertrophy. Am J Physiol 275(3 Pt 2):H961–H968

    CAS  PubMed  Google Scholar 

  • Spector PS (2005) Diagnosis and management of sudden cardiac death. Heart 91(3):408–413

    Article  PubMed  PubMed Central  Google Scholar 

  • Stamler J, Stamler R, Neaton JD (1993) Blood pressure, systolic and diastolic, and cardiovascular risks. Arch Intern Med 153:598–615

    Article  CAS  PubMed  Google Scholar 

  • Stauffer ES (1978) Long-term management of traumatic quadriplegia. In: The total care of spinal cord injuries. Little, Brown, Boston, pp. 81–102

    Google Scholar 

  • Steers WD, Ciambotti J, Erdman S, de Groat WC (1990) Morphological plasticity in efferent pathways to the urinary bladder of the rat following urethral obstruction. J Neurosci 10(6):1943–1951

    CAS  PubMed  Google Scholar 

  • Stevenson ET, Davy KP, Jones PP, Desouza CA, Seals DR (1997) Blood pressure risk factors in healthy postmenopausal women: physical activity and hormone replacement. J Appl Physiol 82:652–660

    CAS  PubMed  Google Scholar 

  • 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(1):61–68

    Article  PubMed  Google Scholar 

  • Stiens S, Johnson M, Lyman P (1995) Cardiac rehabilitation in patients with spinal cord injury. Phys Med Rehabil Clin N Am 6(2):263–295

    Google Scholar 

  • Stone HL, Liang IY (1984) Cardiovascular response and control during exercise. Am Rev Respir Dis 129(2 Pt 2):S13–S16

    Article  CAS  PubMed  Google Scholar 

  • Stone HL, Dormer KJ, Foreman RD, Thies R, Blair R (1985) Neural regulation of the cardiovascular system during exercise. Fed Proc 44(7):2271–2278

    CAS  PubMed  Google Scholar 

  • Teasell RW, Arnold JMO, 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

    Article  CAS  PubMed  Google Scholar 

  • Teerlink JR, Pfeffer JM, Pfeffer MA (1994) Progressive ventricular remodeling in response to diffuse isoproterenol-induced myocardial necrosis in rats. Circ Res 75(1):105–113

    Article  CAS  PubMed  Google Scholar 

  • Tipton CM (1991) Exercise, training and hypertension: an update. Exerc Sport Sci Rev 19:447–505

    Article  CAS  PubMed  Google Scholar 

  • VanNess JM, Takata HJ, Overton JM (1996) Attenuated blood pressure responsiveness during post-exercise hypotension. Clin Exp Hypertens 18:891–900

    Article  CAS  PubMed  Google Scholar 

  • Voyvodic JT (1989) Peripheral target regulation of dendritic geometry in the rat superior cervical ganglion. J Neurosci 9(6):1997–2010

    CAS  PubMed  Google Scholar 

  • Washburn RA, Figoni SF (1998) Physical activity and chronic cardiovascular disease prevention in spinal cord injury: a comprehensive literature review. Top Spinal Cord Inj Rehab 3:16–32

    Google Scholar 

  • West CR, Campbell IG, Shave RE, Romer LM (2012a) Effects of abdominal binding on cardiorespiratory function in cervical spinal cord injury. Respir Physiol Neurobiol 180(2-3):275–282

    Article  PubMed  Google Scholar 

  • West CR, Campbell IG, Shave RE, Romer LM (2012b) Resting cardiopulmonary function in Paralympic athletes with cervical spinal cord injury. Med Sci Sports Exerc 44(2):323–329

    Article  PubMed  Google Scholar 

  • West CR, Crawford MA, Poormasjedi-Meibod MS, Currie KD, Fallavollita A, Yuen V, McNeill JH, Krassioukov AV (2014) Passive hind-limb cycling improves cardiac function and reduces cardiovascular disease risk in experimental spinal cord injury. J Physiol 592(Pt 8):1771–1783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wharton JM, Coleman RE, Strauss HC (1992) The role of the autonomic nervous system in sudden cardiac death. Trends Cardiovasc Med 2:65–71

    Article  CAS  PubMed  Google Scholar 

  • Whiteneck GG, Charlifue SW, Frankel HL, Fraser MH, Gardner BP, Gerhart KA, Krishnan KR, Menter RR, Nuseibeh I, Short DJ et al (1992) Mortality, morbidity, and psychosocial outcomes of persons spinal cord injured more than 20 years ago. Paraplegia 30:617–630

    Article  CAS  PubMed  Google Scholar 

  • Wicks JR, Oldridge NB, Cameron NB, Jones NL (1983) Arm cranking and wheelchair ergometry in elite spinal cord injured athletes. Med Sci Sports Exc 15:224–231

    CAS  Google Scholar 

  • Yeoh M, McLachlan EM, Brock JA (2004) Chronic decentralization potentiates neurovascular transmission in the isolated rat tail artery, mimicking the effects of spinal transection. J Physiol 561(Pt 2):583–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zipes DP (1991) The long QT interval syndrome. A Rosetta stone for sympathetic related ventricular tachyarrhythmias [comment]. Circulation 84(3):1414–1419

    Article  CAS  PubMed  Google Scholar 

  • Zipes DP, Mihalick MJ, Robbins GT (1974) Effects of selective vagal and stellate ganglion stimulation of atrial refractoriness. Cardiovasc Res 8(5):647–655

    Article  CAS  PubMed  Google Scholar 

  • Zwiren LD, Bar-Or O (1975) Responses to exercise of paraplegics who differ in conditioning level. Med Sci Sports 7(2):94–98

    CAS  PubMed  Google Scholar 

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Lujan, H.L., DiCarlo, S.E. (2016). Alterations in Cardiac Electrophysiology After Spinal Cord Injury and Implications for Exercise. In: Taylor, J. (eds) The Physiology of Exercise in Spinal Cord Injury. Physiology in Health and Disease. Springer, Boston, MA. https://doi.org/10.1007/978-1-4939-6664-6_5

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