Skip to main content
SpringerLink
Log in

Cardiovascular Dysfunction Following Spinal Cord Injury

  • Chapter
  • First Online:
Neurological Aspects of Spinal Cord Injury

Abstract

Cardiovascular issues following spinal cord injury (SCI) are of paramount importance considering they are the leading cause of death in this population. The disruption of autonomic pathways leads to a highly unstable cardiovascular system, with impaired blood pressure and heart rate regulation. In addition to low resting blood pressure, on a daily basis, the majority of those with SCI suffer from transient episodes of aberrantly low and high blood pressure (termed orthostatic hypotension and autonomic dysreflexia, respectively). In fact autonomic issues, including the resolution of autonomic dysreflexia, are frequently ranked by individuals with SCI to be of greater priority than regaining motor function. Due to a combination of these autonomic disturbances and a myriad of lifestyle factors, the pernicious process of cardiovascular disease is accelerated after SCI. Unfortunately, these secondary consequences of SCI are only beginning to receive appropriate clinical attention. Immediately after high-level SCI, major cardiovascular abnormalities present in the form of neurogenic shock. After subsiding, new issues related to blood pressure instability arise, including orthostatic hypotension and autonomic dysreflexia. The present chapter reviews autonomic control over the cardiovascular system before injury and the mechanisms underlying cardiovascular abnormalities after SCI, while also detailing the end-organ consequences including those of the heart, as well as the systemic and cerebral vasculature. The tertiary impact of cardiovascular dysfunction will also be discussed, such as the potential impediment of rehabilitation, impaired cognitive function, and limitations to exercise capacity. In the recent past, our understanding of autonomic dysfunction has been greatly enhanced; however, it is vital to further develop our understanding of the long-term consequences of these conditions, which give us insight to cardiovascular disease morbidity and mortality in this population.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Phillips AA, Cote AT, Bredin SS, Krassioukov AV, Warburton DE (2012) Aortic stiffness increased in spinal cord injury when matched for physical activity. Med Sci Sports Exerc 44:2065–2070

    Article  PubMed  Google Scholar 

  2. Miyatani M, Masani K, Oh PI, Miyachi M, Popovic MR, Craven BC (2009) Pulse wave velocity for assessment of arterial stiffness among people with spinal cord injury: a pilot study. J Spinal Cord Med 32:72–78

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  PubMed  PubMed Central  Google Scholar 

  4. Krassioukov A (2009) Autonomic function following cervical spinal cord injury. Respir Physiol Neurobiol 169:157–164

    Article  PubMed  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. Krassioukov A, Claydon VE, Krassioukov A, Claydon VE (2006) The clinical problems in cardiovascular control following spinal cord injury: an overview. Prog Brain Res 152:223–229

    Article  PubMed  Google Scholar 

  7. Claydon VE, Krassioukov AV (2006) Orthostatic hypotension and autonomic pathways after spinal cord injury. J Neurotrauma 23:1713–1725

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  9. DeVivo MJ, Krause JS, Lammertse DP (1999) Recent trends in mortality and causes of death among persons with spinal cord injury. Arch Phys Med Rehabil 80:1411–1419

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Kirshblum S, Waring W (2014) Updates for the international standards for neurological classification of spinal cord injury. Phys Med Rehabil Clin N Am 25:505–517

    Article  PubMed  Google Scholar 

  12. Krassioukov A, Biering-Sorensen CF, Donovan W, Kennelly M, Kirshblum S, Krogh K, Alexander MS, Vogel L, Wecht J (2012) International Standards to document remaining Autonomic Function after Spinal Cord Injury (ISAFSCI), first edition 2012. Top Spinal Cord Inj Rehabil 18:282–296

    Article  PubMed  Google Scholar 

  13. Phillips AA, Krassioukov AV, Ainslie P, Warburton DER (2012) Baroreflex function following spinal cord injury. J Neurotrauma 29:2431–2445

    Article  PubMed  Google Scholar 

  14. Krassioukov A, Weaver LC (1996) Anatomy of the autonomic nervous system. Phys Med Rehabil 10:1–14

    Google Scholar 

  15. Krassioukov AVV, Weaver LCC (1996) Morphological changes in sympathetic preganglionic neurons after spinal cord injury in rats. Neuroscience 70:211–225

    Article  CAS  PubMed  Google Scholar 

  16. Suzuki N, Hardebo JE, Owman C (1990) Origins and pathways of choline acetyltransferase-positive parasympathetic nerve fibers to cerebral vessels in rat. J Cereb Blood Flow Metab 10:399–408

    Article  CAS  PubMed  Google Scholar 

  17. Kano M, Moskowitz MA, Yokota M (1991) Parasympathetic denervation of rat pial vessels significantly increases infarction volume following middle cerebral artery occlusion. J Cereb Blood Flow Metab 11:628–637

    Article  CAS  PubMed  Google Scholar 

  18. Hamner JW, Tan CO, Tzeng Y-CC, Taylor JA (2012) Cholinergic control of the cerebral vasculature in humans. J Physiol 590:6343–6352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Dampney RAL, Horiuchi J, Tagawa T, Fontes MAP, Potts PD, Polson JW (2003) Medullary and supramedullary mechanisms regulating sympathetic vasomotor tone. Acta Physiol Scand 177:209–218

    Article  CAS  PubMed  Google Scholar 

  20. Krassioukov AV, Weaver LC (2009) Reflex and morphological changes in spinal preganglionic neurons after cord injury in rats. Clin Exp Hypertens 17:361–373

    Article  Google Scholar 

  21. Ogoh S, Volianitis S, Nissen P, Wray DW, Secher NH, Raven PB (2003) Carotid baroreflex responsiveness to head-up tilt-induced central hypovolaemia: effect of aerobic fitness. J Physiol 551:601–608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ogoh S, Yoshiga CC, Secher NH, Raven PB (2006) Carotid-cardiac baroreflex function does not influence blood pressure regulation during head-up tilt in humans. J Physiol Sci 56:227–233

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. Lebedev VP, Krasyukov AV, Nikitin SA (1986) Electrophysiological study of sympathoexcitatory structures of the bulbar ventrolateral surface as related to vasomotor regulation. Neuroscience 17:189–203

    Article  CAS  PubMed  Google Scholar 

  25. Furlan JC, Fehlings MG, Shannon P, Norenberg MD, Krassioukov AV (2003) Descending vasomotor pathways in humans: correlation between axonal preservation and cardiovascular dysfunction after spinal cord injury. J Neurotrauma 20:1351–1363

    Article  PubMed  Google Scholar 

  26. La Rovere MT, Pinna GD, Raczak G (2008) Baroreflex sensitivity: measurement and clinical implications. Ann Noninvasive Electrocardiol 13:191–207

    Article  PubMed  Google Scholar 

  27. Heusser K, Tank J, Luft FC, Jordan J (2005) Baroreflex failure. Hypertension 45:834–839

    Article  CAS  PubMed  Google Scholar 

  28. Taylor JA, Halliwill JR, Brown TE, Hayano J, Eckberg DL (1995) “Non-hypotensive” hypovolaemia reduces ascending aortic dimensions in humans. J Physiol 483(Pt 1):289–298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Fu Q, Shibata S, Hastings JL, Prasad A, Palmer MD, Levine BD (2009) Evidence for unloading arterial baroreceptors during low levels of lower body negative pressure in humans. Am J Physiol Heart Circ Physiol 296:H480–H488

    Article  CAS  PubMed  Google Scholar 

  30. Abboud FM, Thames MD (1983) Interaction of cardiovascular reflexes in circulatory control. In: Handbook of physiology. The cardiovascular system. Peripheral circulation and organ blood flow. American Physiological Society, Bethesda, pp 675–753

    Google Scholar 

  31. Fadel PJ, Ogoh S, Keller DM, Raven PB (2003) Recent insights into carotid baroreflex function in humans using the variable pressure neck chamber. Exp Physiol 88:671–680

    Article  PubMed  Google Scholar 

  32. Sjostrand T (1953) Volume and distribution of blood and their significance in regulating the circulation. Physiol Rev 33:202–228

    CAS  PubMed  Google Scholar 

  33. Krassioukov AV, Bunge RP, Pucket WR, Bygrave MA (1999) The changes in human spinal sympathetic preganglionic neurons after spinal cord injury. Spinal Cord 37:6–13

    Article  CAS  PubMed  Google Scholar 

  34. Krassioukov AV, Johns DG, Schramm LP (2002) Sensitivity of sympathetically correlated spinal interneurons, renal sympathetic nerve activity, and arterial pressure to somatic and visceral stimuli after chronic spinal injury. J Neurotrauma 19:1521–1529

    Article  PubMed  Google Scholar 

  35. Ramer LM, van Stolk aP, Inskip J, Ramer MS, Krassioukov AV (2012) Plasticity of TRPV1-expressing sensory neurons mediating autonomic dysreflexia following spinal cord injury. Front Physiol 3:257

    Article  PubMed  PubMed Central  Google Scholar 

  36. West CR, Bellantoni A, Krassioukov AV (2013) Cardiovascular function in individuals with incomplete spinal cord injury: a systematic review. Top Spinal Cord Inj Rehabil 19:267–278

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  39. 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 

  40. Arnold JMO, Feng Q-P, Delaney GA, Teasell RW (1995) Autonomic dysreflexia in tetraplegic patients: evidence for α-adrenoceptor hyper-responsiveness. Clin Auton Res 5:267–270

    Article  CAS  PubMed  Google Scholar 

  41. Mathias CJ, Bannister R (2002) Autonomic disturbances in spinal cord lesions. In: Autonomic failure: a textbook of clinical disorders of the autonomic nervous system, 4th edn. Oxford University Press, New York

    Google Scholar 

  42. Krassioukov A (2004) Autonomic dysreflexia in acute spinal cord injury: incidence, mechanisms, and management. SCI Nurs 21:215–216

    PubMed  Google Scholar 

  43. Murray M (1993) Plasticity in the spinal cord: the dorsal root connection. Restor Neurol Neurosci 5:37–45

    CAS  PubMed  Google Scholar 

  44. Ackery AD, Norenberg MD, Krassioukov A (2007) Calcitonin gene-related peptide immunoreactivity in chronic human spinal cord injury. Spinal Cord 45:678–686

    Article  CAS  PubMed  Google Scholar 

  45. Krenz N, Weaver L (1998) Sprouting of primary afferent fibers after spinal cord transection in the rat. Neuroscience 85:443–458

    Article  CAS  PubMed  Google Scholar 

  46. Krassioukov AV, Weaver LC (1995) Episodic hypertension due to autonomic dysreflexia in acute and chronic spinal cord-injured rats. Am J Physiol 268:H2077–H2083

    CAS  PubMed  Google Scholar 

  47. Maiorov DN, Krenz NR, Krassioukov AV, Weaver LC (1997) Role of spinal NMDA and AMPA receptors in episodic hypertension in conscious spinal rats. Am J Physiol Heart Circ Physiol 273:H1266–H1274

    CAS  Google Scholar 

  48. Cameron AA, Smith GM, Randall DC, Brown DR, Rabchevsky AG (2006) Genetic manipulation of intraspinal plasticity after spinal cord injury alters the severity of autonomic dysreflexia. J Neurosci 26:2923–2932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 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 10:1108–1117

    Article  PubMed  Google Scholar 

  50. 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:H398–H405

    Article  CAS  PubMed  Google Scholar 

  51. Groothuis J, Thijssen D (2010) Angiotensin II contributes to the increased baseline leg vascular resistance in spinal cord-injured individuals. J Hypertens 28:2094–2101

    Article  CAS  PubMed  Google Scholar 

  52. Wecht JM, Radulovic M, Weir JP, Lessey J, Spungen AM, Bauman WA (2005) Partial angiotensin-converting enzyme inhibition during acute orthostatic stress in persons with tetraplegia. J Spinal Cord Med 28:103–108

    Article  PubMed  Google Scholar 

  53. Mathias CJ, Frankel HL, Christensen NJ, Spalding JM (1976) Enhanced pressor response to noradrenaline in patients with cervical spinal cord transection. Brain 99:757–770

    Article  CAS  PubMed  Google Scholar 

  54. De Groat WC, Yoshimura N (2006) Mechanisms underlying the recovery of lower urinary tract function following spinal cord injury. Prog Brain Res 152:59–84

    Article  PubMed  CAS  Google Scholar 

  55. West CR, Mills P, Krassioukov AV (2012) Influence of the neurological level of spinal cord injury on cardiovascular outcomes in humans: a meta-analysis. Spinal Cord 50:484–492

    Article  CAS  PubMed  Google Scholar 

  56. Hadley M; Guidelines (2002) Blood pressure management after acute spinal cord injury. Neurosurgery 50:S58–S62

    Google Scholar 

  57. Nacimiento W, Noth J (1999) What, if anything, is spinal shock? Arch Neurol 56:1033–1035

    Article  CAS  PubMed  Google Scholar 

  58. Vale FL, Burns J, Jackson AB, Hadley MN (1997) Combined medical and surgical treatment after acute spinal cord injury: results of a prospective pilot study to assess the merits of aggressive medical resuscitation and blood pressure management. J Neurosurg 87:239–246

    Article  CAS  PubMed  Google Scholar 

  59. Hebert LE, Scherr PA, Bennett DA, Bienias JL, Wilson RS, Morris MC, Evans DA (2004) Blood pressure and late-life cognitive function change: a biracial longitudinal population study. Neurology 62:2021–2024

    Article  CAS  PubMed  Google Scholar 

  60. Duschek S, Hadjamu M, Schandry R (2007) Enhancement of cerebral blood flow and cognitive performance following pharmacological blood pressure elevation in chronic hypotension. Psychophysiology 44:145–153

    Article  PubMed  Google Scholar 

  61. Duschek S, Schandry R (2004) Cognitive performance and cerebral blood flow in essential hypotension. Psychophysiology 41:905–913

    Article  PubMed  Google Scholar 

  62. Phillips AA, Warburton DE, Ainslie PN, Krassioukov AV (2014) Regional neurovascular coupling and cognitive performance in those with low blood pressure secondary to high-level spinal cord injury: improved by alpha-1 agonist midodrine hydrochloride. J Cereb Blood Flow Metab 34:794–801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Claydon VE, Steeves JD, Krassioukov A (2006) Orthostatic hypotension following spinal cord injury: understanding clinical pathophysiology. Spinal Cord 44:341–351

    Article  CAS  PubMed  Google Scholar 

  64. Wecht JM, Bauman WA (2013) Decentralized cardiovascular autonomic control and cognitive deficits in persons with spinal cord injury. J Spinal Cord Med 36:74–81

    Article  PubMed  PubMed Central  Google Scholar 

  65. Phillips AA, Krassioukov AV, Ainslie PN, Warburton DER (2014) Perturbed and spontaneous regional cerebral blood flow responses to changes in blood pressure after high level spinal cord injury: the effect of midodrine. J Appl Physiol 116:645–653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Cariga P, Ahmed S, Mathias CJ, Gardner BP (2002) The prevalence and association of neck (coat-hanger) pain and orthostatic (postural) hypotension in human spinal cord injury. Spinal Cord 40:77–82

    Article  CAS  PubMed  Google Scholar 

  67. Illman A, Stiller K, Williams M (2000) The prevalence of orthostatic hypotension during physiotherapy treatment in patients with an acute spinal cord injury. Spinal Cord 38:741

    Article  CAS  PubMed  Google Scholar 

  68. Krassioukov A, Warburton DE, Teasell R, Eng JJ (2009) A systematic review of the management of autonomic dysreflexia after spinal cord injury. Arch Phys Med Rehabil 90:682–695

    Article  PubMed  PubMed Central  Google Scholar 

  69. Ekland MB, Krassioukov AV, McBride KE, Elliott SL (2008) Incidence of autonomic dysreflexia and silent autonomic dysreflexia in men with spinal cord injury undergoing sperm retrieval: implications for clinical practice. J Spinal Cord Med 31:33–39

    Article  PubMed  PubMed Central  Google Scholar 

  70. Hubli M, Gee CM, Krassioukov AV (2014) Refined assessment of blood pressure instability after spinal cord injury. Am J Hypertens. doi:10.1093/ajh/hpu122

    PubMed  Google Scholar 

  71. 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 29:207–216

    Article  PubMed  PubMed Central  Google Scholar 

  72. Chancellor MB, Rivas DA, Erhard MJ, Hirsch IH, Bagley DH (1993) Flexible cystoscopy during urodynamic evaluation of spinal cord-injured patients. J Endourol 7:531–535

    Article  CAS  PubMed  Google Scholar 

  73. Charney KJ (1975) General surgery problems in patients with spinal cord injuries. Arch Surg 110:1083

    Article  CAS  PubMed  Google Scholar 

  74. Wineinger MA, Basford JR (1985) Autonomic dysreflexia due to medication: misadventure in the use of an isometheptene combination to treat migraine. Arch Phys Med Rehabil 66:645–646

    CAS  PubMed  Google Scholar 

  75. Kim JH, Rivas DA, Shenot PJ, Green B, Kennelly M, Erickson JR, O’Leary M, Yoshimura N, Chancellor MB (2003) Intravesical resiniferatoxin for refractory detrusor hyperreflexia: a multicenter, blinded, randomized, placebo-controlled trial. J Spinal Cord Med 26:358–363

    Article  PubMed  Google Scholar 

  76. Lindan R, Joiner E, Freehafer AA, Hazel C (1980) Incidence and clinical features of autonomic dysreflexia in patients with spinal cord injury. Paraplegia 18:285–292

    Article  CAS  PubMed  Google Scholar 

  77. McGregor JA, Meeuwsen J (1985) Autonomic hyperreflexia: A mortal danger for spinal cord-damaged women in labor. Am J Obstet Gynecol 151:330–333

    Article  CAS  PubMed  Google Scholar 

  78. Barton CH, Khonsari F, Vaziri ND, Byrne C, Gordon S, Friis R (1986) The effect of modified transurethral sphincterotomy on autonomic dysreflexia. J Urol 135:83–85

    CAS  PubMed  Google Scholar 

  79. Hohenfellner M, Pannek J, Bötel U, Dahms S, Pfitzenmaier J, Fichtner J, Hutschenreiter G, Thüroff JW (2001) Sacral bladder denervation for treatment of detrusor hyperreflexia and autonomic dysreflexia. Urology 58:28–32

    Article  CAS  PubMed  Google Scholar 

  80. Perkash I (1997) Autonomic dysreflexia and detrusor-sphincter dyssynergia in spinal cord injury patients. J Spinal Cord Med 20:365–370

    CAS  PubMed  Google Scholar 

  81. Vaidyanathan S, Krishnan KR, Soni BM (1996) Endoscopic management of urethral trauma in male spinal cord injury patients. Spinal Cord 34:651–656

    Article  CAS  PubMed  Google Scholar 

  82. Brown BT, Carrion HM, Politano VA (1979) Guanethidine sulfate in the prevention of autonomic hyperreflexia. J Urol 122:55–57

    Article  CAS  PubMed  Google Scholar 

  83. Dykstra DD, Sidi AA, Anderson LC (1987) The effect of nifedipine on cystoscopy-induced autonomic hyperreflexia in patients with high spinal cord injuries. J Urol 138:1155–1157

    CAS  PubMed  Google Scholar 

  84. Snow JC, Sideropoulos HP, Kripke BJ, Freed MM, Shah NK, Schlesinger RM (1978) Autonomic hyperreflexia during cystoscopy in patients with high spinal cord injuries. Paraplegia 15:327–332

    Article  CAS  PubMed  Google Scholar 

  85. Sizemore GW, Winternitz WW (1970) Autonomic hyper-reflexia--suppression with alpha-adrenergic blocking agents. N Engl J Med 282:795

    Article  CAS  PubMed  Google Scholar 

  86. Widerström-Noga E, Cruz-Almeida Y, Krassioukov A (2004) Is there a relationship between chronic pain and autonomic dysreflexia in persons with cervical spinal cord injury? J Neurotrauma 21:195–204

    Article  PubMed  Google Scholar 

  87. Paola FA, Sales D, Garcia-Zozaya I (2003) Phenazopyridine in the management of autonomic dysreflexia associated with urinary tract infection. J Spinal Cord Med 26:409–411

    Article  PubMed  Google Scholar 

  88. Kursh ED, Freehafer A, Persky L (1977) Complications of autonomic dysreflexia. J Urol 118:70–72

    CAS  PubMed  Google Scholar 

  89. Chang CP, Chen MT, Chang LS (1991) Autonomic hyperreflexia in spinal cord injury patient during percutaneous nephrolithotomy for renal stone: a case report. J Urol 146:1601–1602

    CAS  PubMed  Google Scholar 

  90. Kabalin JN, Lennon S, Gill HS, Wolfe V, Perkash I (1993) Incidence and management of autonomic dysreflexia and other intraoperative problems encountered in spinal cord injury patients undergoing extracorporeal shock wave lithotripsy without anesthesia on a second generation lithotriptor. J Urol 149:1064–1067

    CAS  PubMed  Google Scholar 

  91. Frankel HL, Mathias CJ (1980) Severe hypertension in patients with high spinal cord lesions undergoing electro-ejaculation--management with prostaglandin E2. Paraplegia 18:293–299

    Article  CAS  PubMed  Google Scholar 

  92. Ohl DA, Sonksen J, Menge AC, McCabe M, Keller LM (1997) Electroejaculation versus vibratory stimulation in spinal cord injured men: sperm quality and patient preference. J Urol 157:2147–2149

    Article  CAS  PubMed  Google Scholar 

  93. Steinberger RE, Ohl DA, Bennett CJ, McCabe M, Wang SC (1990) Nifedipine pretreatment for autonomic dysreflexia during electroejaculation. Urology 36:228–231

    Article  CAS  PubMed  Google Scholar 

  94. Elliott S, Krassioukov A (2006) Malignant autonomic dysreflexia in spinal cord injured men. Spinal Cord 44:386–392

    Article  CAS  PubMed  Google Scholar 

  95. Scott MB, Morrow JW (1978) Phenoxybenzamine in neurogenic bladder dysfunction after spinal cord injury. II. Autonomic dysreflexia. J Urol 119:483–484

    CAS  PubMed  Google Scholar 

  96. Sheel AW, Krassioukov AV, Inglis JT, Elliott SL (2005) Autonomic dysreflexia during sperm retrieval in spinal cord injury: influence of lesion level and sildenafil citrate. J Appl Physiol 99:53–58

    Article  PubMed  Google Scholar 

  97. Erickson RP (1980) Autonomic hyperreflexia: pathophysiology and medical management. Arch Phys Med Rehabil 61:431–440

    CAS  PubMed  Google Scholar 

  98. Brackett NL, Ferrell SM, Aballa TC, Amador MJ, Padron OF, Sonksen J, Lynne CM (1998) An analysis of 653 trials of penile vibratory stimulation in men with spinal cord injury. J Urol 159:1931–1934

    Article  CAS  PubMed  Google Scholar 

  99. Mathias C, Frankel H (1999) Autonomic Failure: A Textbook of Clinical Disorders of the Autonomic Nervous System (5 ed.)Edited by Christopher J. Mathias and Sir Roger Bannister Sign up to an individual subscription to Autonomic Failure. Oxford University Press. doi:10.1093/med/9780198566342.001.000

  100. Maehama T, Izena H, Kanazawa K (2000) Management of autonomic hyperreflexia with magnesium sulfate during labor in a woman with spinal cord injury. Am J Obstet Gynecol 183:492–493

    Article  CAS  PubMed  Google Scholar 

  101. Osgood S, Kuczkowski K (2006) Autonomic dysreflexia in a parturient with spinal cord injury. Acta Anaesthesiol Belg 57:161–162

    CAS  PubMed  Google Scholar 

  102. Katz VL, Thorp JM, Cefalo RC (1990) Epidural analgesia and autonomic hyperreflexia: a case report. Am J Obstet Gynecol 162:471–472

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  104. Cross LL, Meythaler JM, Tuel SM, Cross AL (1992) Pregnancy, labor and delivery post spinal cord injury. Paraplegia 30:890–902

    Article  CAS  PubMed  Google Scholar 

  105. Tabsh KM, Brinkman CR, Reff RA (1982) Autonomic dysreflexia in pregnancy. Obstet Gynecol 60:119–122

    CAS  PubMed  Google Scholar 

  106. Hickey KJ, Vogel LC, Willis KM, Anderson CJ (2004) Prevalence and etiology of autonomic dysreflexia in children with spinal cord injuries. J Spinal Cord Med 27(Suppl 1):S54–S60

    Article  PubMed  Google Scholar 

  107. Kewalramani LS (1980) Autonomic dysreflexia in traumatic myelopathy. Am J Phys Med 59:1–21

    CAS  PubMed  Google Scholar 

  108. Cosman BC, Vu TT (2005) Lidocaine anal block limits autonomic dysreflexia during anorectal procedures in spinal cord injury: a randomized, double-blind, placebo-controlled trial. Dis Colon Rectum 48:1556–1561

    Article  PubMed  Google Scholar 

  109. Hawkins RL, Bailey RH, Donnovan WH (1994) Autonomic dysreflexia resulting from prolapsed hemorrhoids. Dis Colon Rectum 37:492–493

    Article  PubMed  Google Scholar 

  110. Donald IP, Gear MW, Wilkinson SP (1987) A life-threatening respiratory complication of gastro-oesophageal reflux in a patient with tetraplegia. Postgrad Med J 63:397–399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Head H, Riddoch G (1917) The automatic bladder, excessive sweating and some other reflex conditions, in gross injuries of the spinal cord. Brain 40:188–263

    Article  Google Scholar 

  112. Bar-On Z, Ohry A (1995) The acute abdomen in spinal cord injury individuals. Paraplegia 33:704–706

    Article  CAS  PubMed  Google Scholar 

  113. Jane MJ, Freehafer AA, Hazel C, Lindan R, Joiner E (1982) Autonomic dysreflexia. A cause of morbidity and mortality in orthopedic patients with spinal cord injury. Clin Orthop Relat Res 169:151–154

    Google Scholar 

  114. Matthews JM, Wheeler GD, Burnham RS, Malone LA, Steadwarde RD (1997) The effects of surface anaesthesia on the autonomic dysreflexia response during functional electrical stimulation. Spinal Cord 35:647–651

    Article  CAS  PubMed  Google Scholar 

  115. Finocchiaro DN, Herzfeld ST (1990) Understanding autonomic dysreflexia. Am J Nurs 90:56–59

    CAS  PubMed  Google Scholar 

  116. Hall PA, Young JV (1983) Autonomic hyperreflexia in spinal cord injured patients: trigger mechanism--dressing changes of pressure sores. J Trauma 23:1074–1075

    Article  CAS  PubMed  Google Scholar 

  117. Salzberg CA, Byrne DW, Cayten CG, van Niewerburgh P, Murphy JG, Viehbeck M (1996) A new pressure ulcer risk assessment scale for individuals with spinal cord injury. Am J Phys Med Rehabil 75:96–104

    Article  CAS  PubMed  Google Scholar 

  118. 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

    Article  CAS  PubMed  Google Scholar 

  119. Simpson DM (1997) Clinical trials of botulinum toxin in the treatment of spasticity. Muscle Nerve 20:169–175

    Article  Google Scholar 

  120. Beard JP, Wade WH, Barber DB (1996) Sacral insufficiency stress fracture as etiology of positional autonomic dysreflexia: Case report. Paraplegia 34:173–175

    Article  CAS  PubMed  Google Scholar 

  121. Mohit AA, Mirza S, James J, Goodkin R (2005) Charcot arthropathy in relation to autonomic dysreflexia in spinal cord injury: case report and review of the literature. J Neurosurg Spine 2:476–480

    Article  PubMed  Google Scholar 

  122. Selçuk B, Inanir M, Kurtaran A, Sulubulut N, Akyüz M (2004) Autonomic dysreflexia after intramuscular injection in traumatic tetraplegia: a case report. Am J Phys Med Rehabil 83(1):61–64

    Article  PubMed  Google Scholar 

  123. Graham GP, Dent CM, Evans PD, McKibbin B (1992) Recurrent dislocation of the hip in adult paraplegics. Paraplegia 30:587–591

    Article  CAS  PubMed  Google Scholar 

  124. Han M, Kim H (2003) Chronic hip instability as a cause of autonomic dysreflexia: successful management by resection arthroplasty. JBJS Case Connect 85:126–128

    Google Scholar 

  125. 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

    Article  CAS  PubMed  Google Scholar 

  126. Kolodin EL, Vitale TD, Goldberg KL, Giannakaros JD, Kirshblum S, Voorman SJ, Linsenmeyer TA (2001) Autonomic dysreflexia and foot and ankle surgery. J Foot Ankle Surg 40:172–177

    Article  CAS  PubMed  Google Scholar 

  127. Lambert DH, Deane RS, Mazuzan JE (1982) Anesthesia and the control of blood pressure in patients with spinal cord injury. Anesth Analg 61:344–348

    Article  CAS  PubMed  Google Scholar 

  128. Schonwald G, Fish KJ, Perkash I (1981) Cardiovascular complications during anesthesia in chronic spinal cord injured patients. Anesthesiology 55:550–558

    Article  CAS  PubMed  Google Scholar 

  129. Stowe DF, Bernstein JS, Madsen KE, McDonald DJ, Ebert TJ (1989) Autonomic hyperreflexia in spinal cord injured patients during extracorporeal shock wave lithotripsy. Anesth Analg 68:788–791

    Article  CAS  PubMed  Google Scholar 

  130. Nieder RM (1970) Autonomic hyperreflexia in urologic surgery. J Am Med Assoc 213:867

    Article  CAS  Google Scholar 

  131. Scher AT (1978) Autonomic hyperreflexia. A serious complication of radiological procedures in patients with cervical or upper thoracic spinal cord lesions. S Afr Med J 53:208–210

    CAS  PubMed  Google Scholar 

  132. Wu K, Lai P, Lee L, Hsu C (2005) Autonomic dysreflexia triggered by an unstable lumbar spine in a quadriplegic patient. Chang Gung Med J 28:508–511

    PubMed  Google Scholar 

  133. Thumbikat P, Ravichandran G, McClelland MR (2001) Neuropathic lumbar spondylolisthesis--a rare trigger for posture induced autonomic dysreflexia. Spinal Cord 39:564–567

    Article  CAS  PubMed  Google Scholar 

  134. Colachis SC (1991) Autonomic hyperreflexia in spinal cord injury associated with pulmonary embolism. Arch Phys Med Rehabil 72:1014–1016

    PubMed  Google Scholar 

  135. McGarry J, Woolsey RM, Thompson CW (1982) Autonomic hyperreflexia following passive stretching to the hip joint. Phys Ther 62:30–31

    Article  CAS  PubMed  Google Scholar 

  136. Khurana RK (1987) Orthostatic hypotension-induced autonomic dysreflexia. Neurology 37:1221–1224

    Article  CAS  PubMed  Google Scholar 

  137. Abouleish EI, Hanley ES, Palmer SM (1989) Can epidural fentanyl control autonomic hyperreflexia in a quadriplegic parturient? Anesth Analg 68:523–526

    Article  CAS  PubMed  Google Scholar 

  138. Kurnick NB (1956) Autonomic hyperreflexia and its control in patients with spinal cord lesions. Ann Intern Med 44:678

    Article  CAS  PubMed  Google Scholar 

  139. Averill A, Cotter AC, Nayak S, Matheis RJ, Shiflett SC (2000) Blood pressure response to acupuncture in a population at risk for autonomic dysreflexia. Arch Phys Med Rehabil 81:1494–1497

    Article  CAS  PubMed  Google Scholar 

  140. Harris P (1994) Self-induced autonomic dysreflexia (‘boosting’) practised by some tetraplegic athletes to enhance their athletic performance. Paraplegia 32:289–291

    Article  CAS  PubMed  Google Scholar 

  141. Bhambhani Y (2002) Physiology of wheelchair racing in athletes with spinal cord injury. Sport Med 32:23–51

    Article  Google Scholar 

  142. Wheeler G, Cumming D, Burnham R, Maclean I, Sloley BD, Bhambhani Y, Steadward RD (1994) Testosterone, cortisol and catecholamine responses to exercise stress and autonomic dysreflexia in elite quadriplegic athletes. Paraplegia 32:292–299

    Article  CAS  PubMed  Google Scholar 

  143. Yarkony GM, Katz RT, Wu YC (1986) Seizures secondary to autonomic dysreflexia. Arch Phys Med Rehabil 67:834–835

    CAS  PubMed  Google Scholar 

  144. Pan S-LL, Wang Y-HH, Lin H-LL, Chang C-WW, Wu T-YY, Hsieh E-TT (2005) Intracerebral hemorrhage secondary to autonomic dysreflexia in a young person with incomplete C8 tetraplegia: A case report. Arch Phys Med Rehabil 86:591–593

    Article  PubMed  Google Scholar 

  145. Vallès M, Benito J, Portell E, Vidal J (2005) Cerebral hemorrhage due to autonomic dysreflexia in a spinal cord injury patient. Spinal Cord 43:738–740

    Article  PubMed  Google Scholar 

  146. Hanowell L, Wilmot C (1988) Spinal cord injury leading to intracranial hemorrhage. Crit Care Med 16:911–912

    Article  CAS  PubMed  Google Scholar 

  147. Colachis SC, Fugate LP (2002) Autonomic dysreflexia associated with transient aphasia. Spinal Cord 40:142–144

    Article  CAS  PubMed  Google Scholar 

  148. Kiker JD, Woodside JR, Jelinek GE (1982) Neurogenic pulmonary edema associated with autonomic dysreflexia. J Urol 128:1038–1039

    CAS  PubMed  Google Scholar 

  149. Scheutzow MH, Bockenek WL (2000) An unusual complication during electroejaculation in an individual with tetraplegia. J Spinal Cord Med 23:28–30

    Article  CAS  PubMed  Google Scholar 

  150. Colachis SC, Clinchot DM (1997) Autonomic hyperreflexia associated with recurrent cardiac arrest: case report. Spinal Cord 35:256–257

    Article  PubMed  Google Scholar 

  151. Clinical orthopaedics and related research. [cited 3 Oct 2014]. Available from: http://journals.lww.com/corr/Citation/1982/09000/Autonomic_Dysreflexia__A_Cause_of_Morbidity_and.21.aspx

  152. Wan D, Krassioukov AV (2014) Life-threatening outcomes associated with autonomic dysreflexia: a clinical review. J Spinal Cord Med 37:2–10

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  154. Zhang Y, Guan Z, Reader B, Shawler T, Mandrekar-Colucci S, Huang K, Weil Z, Bratasz A, Wells J, Powell ND, Sheridan JF, Whitacre CC, Rabchevsky AG, Nash MS, Popovich PG (2013) Autonomic dysreflexia causes chronic immune suppression after spinal cord injury. J Neurosci 33:12970–12981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Giannantoni A, Di Stasi SM, Scivoletto G, Mollo A, Silecchia A, Fuoco U, Vespasiani G, Stasi SD (1998) Autonomic dysreflexia during urodynamics. Spinal Cord 36:756–760

    Article  CAS  PubMed  Google Scholar 

  156. Kirshblum SC, House JG, O’Connor KC (2002) Silent autonomic dysreflexia during a routine bowel program in persons with traumatic spinal cord injury: a preliminary study. Arch Phys Med Rehabil 83:1774–1776

    Article  PubMed  Google Scholar 

  157. Curt A, Nitsche B, Rodic B, Schurch B, Dietz V (1997) Assessment of autonomic dysreflexia in patients with spinal cord injury. J Neurol Neurosurg Psychiatry 62:473–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Claydon VE, Hol AT, Eng JJ, Krassioukov AV (2006) Cardiovascular responses and postexercise hypotension after arm cycling exercise in subjects with spinal cord injury. Arch Phys Med Rehabil 87:1106–1114

    Article  PubMed  Google Scholar 

  159. Blackmer J (2003) Rehabilitation medicine: 1. Autonomic dysreflexia. Can Med Assoc J 169:931–935

    Google Scholar 

  160. Mathias CJ (1995) Orthostatic hypotension: causes, mechanisms, and influencing factors. Neurology 45:S6–S11

    Article  CAS  PubMed  Google Scholar 

  161. Kaufmann H (1996) Consensus statement on the definition of orthostatic hypotension, pure autonomic failure and multiple system atrophy. Clin Auton Res 6:125–126

    Article  CAS  PubMed  Google Scholar 

  162. Cleophas TJM, Kauw FHW, Bijl C, Meijers J, Stapper G (1986) Effects of beta adrenergic receptor agonists and antagonists in diabetics with symptoms of postural hypotension: a double-blind, placebo-controlled study. Angiology 37:855–862

    Article  CAS  PubMed  Google Scholar 

  163. Frisbie JH, Steele DJ (1997) Postural hypotension and abnormalities of salt and water metabolism in myelopathy patients. Spinal Cord 35:303–307

    Article  CAS  PubMed  Google Scholar 

  164. Sclater A, Alagiakrishnan K (2004) Orthostatic hypotension. A primary care primer for assessment and treatment. Geriatrics 59:22–27

    PubMed  Google Scholar 

  165. Horowitz D, Kaufmann H (2001) Autoregulatory cerebral vasodilation occurs during orthostatic hypotension in patients with primary autonomic failure. Clin Auton Res 11:363–367

    Article  CAS  PubMed  Google Scholar 

  166. Phillips AA, Ainslie PN, Krassioukov AV, Warburton DER (2013) Regulation of cerebral blood flow after spinal cord injury. J Neurotrauma 30:1551–1563

    Article  CAS  PubMed  Google Scholar 

  167. Eigenbrodt ML, Rose KM, Couper DJ, Arnett DK, Smith R, Jones D (2000) Orthostatic hypotension as a risk factor for stroke: the atherosclerosis risk in communities (ARIC) study, 1987–1996. Stroke 31:2307–2313

    Article  CAS  PubMed  Google Scholar 

  168. Wu JC, Chen YC, Liu L, Chen TJ, Huang WC, Cheng H, Tung-Ping S (2012) Increased risk of stroke after spinal cord injury: a nationwide 4-year follow-up cohort study. Neurology 78:1051–1057

    Article  PubMed  Google Scholar 

  169. Vaziri ND (2003) Nitric oxide in microgravity-induced orthostatic intolerance: relevance to spinal cord injury. J Spinal Cord Med 26:5–11

    Article  CAS  PubMed  Google Scholar 

  170. West CR, Krassioukov DAV (2012) Passive hind-limb cycling ameliorates autonomic dysreflexia after T3 spinal cord trascection. In: American Spinal Injury Association annual meeting, Chicago

    Google Scholar 

  171. Shibata S, Perhonen M, Levine BD (2010) Supine cycling plus volume loading prevent cardiovascular deconditioning during bed rest. J Appl Physiol 108:1177–1186

    Article  PubMed  PubMed Central  Google Scholar 

  172. Krassioukov AV, Karlsson A-K, Wecht JM, Wuermser L-A, Mathias CJ, Marino RJ (2007) Assessment of autonomic dysfunction following spinal cord injury: rationale for additions to International Standards for Neurological Assessment. J Rehabil Res Dev 44:103–112

    Article  PubMed  Google Scholar 

  173. Glenn M, Bergman S (1997) Cardiovascular changes following spinal cord injury. Top Spinal Cord Inj Rehabil 2:47–53

    Google Scholar 

  174. Piepmeier JM, Lehmann KB, LANE JG (1985) Cardiovascular instability following acute cervical spinal cord trauma. Cent Nerv Syst Trauma 2:153–160

    Article  CAS  PubMed  Google Scholar 

  175. Winslow EB, Lesch M, Talano JV, Meyer PR (1986) Spinal cord injuries associated with cardiopulmonary complications. Spine 11:809–812

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  178. Tuli S, Tuli J, Coleman WP, Geisler FH, Krassioukov A (2007) Hemodynamic parameters and timing of surgical decompression in acute cervical spinal cord injury. J Spinal Cord Med 30:482–490

    Article  PubMed  PubMed Central  Google Scholar 

  179. Ditunno JF, Little JW, Tessler A, Burns AS (2004) Spinal shock revisited: a four-phase model. Spinal Cord 42:383–395

    Article  CAS  PubMed  Google Scholar 

  180. Devivo MJ (2012) Epidemiology of traumatic spinal cord injury: trends and future implications. Spinal Cord 50:365–372

    Article  CAS  PubMed  Google Scholar 

  181. Washburm RA (1998) Physical activity and chronic cardiovascular disease prevention in spinal cord injury: a comprehensive literature review. Top Spinal Cord Inj Rehabil 3(3):16–32

    Google Scholar 

  182. Hetz SP, Latimer AE, Buchholz AC, Martin Ginis KA (2009) Increased participation in activities of daily living is associated with lower cholesterol levels in people with spinal cord injury. Arch Phys Med Rehabil 90:1755–1759

    Article  PubMed  Google Scholar 

  183. Elder CP, Apple DF, Bickel CS, Meyer RA, Dudley GA (2004) Intramuscular fat and glucose tolerance after spinal cord injury--a cross-sectional study. Spinal Cord 42:711–716

    Article  CAS  PubMed  Google Scholar 

  184. Myers J, Lee M, Kiratli J (2007) Cardiovascular disease in spinal cord injury: an overview of prevalence, risk, evaluation, and management. Am J Phys Med Rehabil 86:142–152

    Article  PubMed  Google Scholar 

  185. Bauman WA, Spungen AM (1994) Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging. Metabolism 43:749–756

    Article  CAS  PubMed  Google Scholar 

  186. Cragg JJ, Noonan VK, Dvorak M, Krassioukov A, Mancini GBJ, Borisoff JF (2013) Spinal cord injury and type 2 diabetes: results from a population health survey. Neurology 81:1864–1868

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  188. Lieberman JA, Hammond FM, Barringer TA, Goff DC, Norton HJ, Bockenek WL, Scelza WM (2011) Adherence with the National Cholesterol Education Program guidelines in men with chronic spinal cord injury. J Spinal Cord Med 34:28–34

    Article  PubMed  PubMed Central  Google Scholar 

  189. Warburton DE, Nicol CW, Bredin SS (2006) Health benefits of physical activity: the evidence. Can Med Assoc J 174:801–809

    Article  Google Scholar 

  190. Stapleton JN, Martin Ginis KA (2014) Sex differences in theory-based predictors of leisure time physical activity in a population-based sample of adults with spinal cord injury. Arch Phys Med Rehabil 95:1787–1790

    Article  PubMed  Google Scholar 

  191. Vlachopoulos C, Aznaouridis K, Stefanadis C (2010) Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J Am Coll Cardiol 55:1318–1327

    Article  PubMed  Google Scholar 

  192. Ginis KAM, Hicks AL, Latimer AE, Warburton DER, Bourne C, Ditor DS, Goodwin DL, Hayes KC, McCartney N, McIlraith A, Pomerleau P, Smith K, Stone JA, Wolfe DL (2011) The development of evidence-informed physical activity guidelines for adults with spinal cord injury. Spinal Cord 49:1088–1096

    Article  PubMed  Google Scholar 

  193. Medicine, A.C. of S (2013) ACSM’s guidelines for exercise testing and prescription. Lippincott Williams & Wilkins. Baltimore, MD

    Google Scholar 

  194. Jeon JY, Weiss CB, Steadward RD, Ryan E, Burnham RS, Bell G, Chilibeck P, Wheeler GD (2002) Improved glucose tolerance and insulin sensitivity after electrical stimulation-assisted cycling in people with spinal cord injury. Spinal Cord 40:110–117

    Article  CAS  PubMed  Google Scholar 

  195. Chilibeck PD, Bell G, Jeon J, Weiss CB, Murdoch G, MacLean I, Ryan E, Burnham R (1999) Functional electrical stimulation exercise increases GLUT-1 and GLUT-4 in paralyzed skeletal muscle. Metabolism 48:1409–1413

    Article  CAS  PubMed  Google Scholar 

  196. Hjeltnes N, Wallberg-Henriksson H (1998) Improved work capacity but unchanged peak oxygen uptake during primary rehabilitation in tetraplegic patients. Spinal Cord 36:691–698

    Article  CAS  PubMed  Google Scholar 

  197. Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH (1997) Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N Engl J Med 336:973–979

    Article  CAS  PubMed  Google Scholar 

  198. Guijarro C (2001) High-sensitivity C-reactive protein: potential adjunct for global risk assessment in the primary prevention of cardiovascular disease. Circulation 104:E127 [cited 29 Sept 2014]

    Google Scholar 

  199. Anson CA, Shepherd C (1996) Incidence of secondary complications in spinal cord injury. Int J Rehabil Res 19:55–66

    Article  CAS  PubMed  Google Scholar 

  200. Frost F, Roach MJ, Kushner I, Schreiber P (2005) Inflammatory C-reactive protein and cytokine levels in asymptomatic people with chronic spinal cord injury. Arch Phys Med Rehabil 86:312–317

    Article  PubMed  Google Scholar 

  201. Hollis ER, Lu P, Blesch A, Tuszynski MH (2009) IGF-I gene delivery promotes corticospinal neuronal survival but not regeneration after adult CNS injury. Exp Neurol 215:53–59

    Article  CAS  PubMed  Google Scholar 

  202. Heldenberg D, Rubinstein A, Levtov O, Werbin B, Tamir I (1981) Serum lipids and lipoprotein concentrations in young quadriplegic patients. Atherosclerosis 39:163–167

    Article  CAS  PubMed  Google Scholar 

  203. Brenes G, Dearwater S, Shapera R, LaPorte RE, Collins E (1986) High density lipoprotein cholesterol concentrations in physically active and sedentary spinal cord injured patients. Arch Phys Med Rehabil 67:445–450

    CAS  PubMed  Google Scholar 

  204. Baigent C, Blackwell L, Emberson J, Holland LE, Reith C, Bhala N, Peto R, Barnes EH, Keech A, Simes J, Collins R (2010) Efficacy and safety of more intensive lowering of LDL cholesterol: a meta-analysis of data from 170,000 participants in 26 randomised trials. Lancet 376:1670–1681

    Article  CAS  PubMed  Google Scholar 

  205. Genest J, McPherson R, Frohlich J, Anderson T, Campbell N, Carpentier A, Couture P, Dufour R, Fodor G, Francis GA, Grover S, Gupta M, Hegele RA, Lau DC, Leiter L, Lewis GF, Lonn E, Mancini GBJ, Ng D, Pearson GJ, Sniderman A, Stone JA, Ur E, John Mancini GB (2009) 2009 Canadian Cardiovascular Society/Canadian guidelines for the diagnosis and treatment of dyslipidemia and prevention of cardiovascular disease in the adult – 2009 recommendations. Can J Cardiol 25:567–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  206. Executive summary of the third report of The National Cholesterol Education Program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III) (2001) JAMA 285:2486–2497

    Google Scholar 

  207. El-Sayed H, Hainsworth R (1995) Relationship between plasma volume, carotid baroreceptor sensitivity and orthostatic tolerance. Clin Sci 88:463–470

    Article  CAS  PubMed  Google Scholar 

  208. Stewart AD, Millasseau SC, Kearney MT, Ritter JM, Chowienczyk PJ (2003) Effects of inhibition of basal nitric oxide synthesis on carotid-femoral pulse wave velocity and augmentation index in humans. Hypertension 42:915–918

    Article  CAS  PubMed  Google Scholar 

  209. De Groot PCE, 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

    Article  PubMed  Google Scholar 

  210. Hooker SP, Wells CL (1989) Effects of low- and moderate-intensity training in spinal cord-injured persons. Med Sci Sports Exerc 21:18–22

    Article  CAS  PubMed  Google Scholar 

  211. O’Rourke MF, Staessen JA, Vlachopoulos C, Duprez D, Plante GE (2002) Clinical applications of arterial stiffness; definitions and reference values. Am J Hypertens 15:426–444

    Article  PubMed  Google Scholar 

  212. Cecelja M, Chowienczyk P (2009) Dissociation of aortic pulse wave velocity with risk factors for cardiovascular disease other than hypertension: a systematic review. Hypertension 54:1328–1336

    Article  CAS  PubMed  Google Scholar 

  213. Green DJ, Jones H, Thijssen D, Cable NT, Atkinson G (2011) Flow-mediated dilation and cardiovascular event prediction: does nitric oxide matter? Hypertension 57:363–369

    Article  CAS  PubMed  Google Scholar 

  214. Phillips AA, Krassioukov AV, Ainslie PN, Cote AT, Warburton DER (2014) Increased central arterial stiffness explains baroreflex dysfunction in spinal cord injury. J Neurotrauma 31:1122–1128

    Article  PubMed  Google Scholar 

  215. Kooijman M, Thijssen DHJ, de Groot PCE, Bleeker MWP, van Kuppevelt HJM, Green DJ, Rongen GA, Smits P, Hopman MTE (2008) Flow-mediated dilatation in the superficial femoral artery is nitric oxide mediated in humans. J Physiol 586:1137–1145

    Article  CAS  PubMed  Google Scholar 

  216. 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

    Article  PubMed  Google Scholar 

  217. Thijssen DH, Ellenkamp R, Smits P, Hopman MT (2006) Rapid vascular adaptations to training and detraining in persons with spinal cord injury. Arch Phys Med Rehabil 87:474–481

    Article  PubMed  Google Scholar 

  218. Laurent S, Cockcroft J, Van Bortel L, Boutouyrie P, Giannattasio C, Hayoz D, Pannier B, Vlachopoulos C, Wilkinson I, Struijker-Boudier H (2006) Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 27:2588–2605

    Article  PubMed  Google Scholar 

  219. Khoshdel AR, Carney SL, Nair BR, Gillies A (2007) Better management of cardiovascular diseases by pulse wave velocity: combining clinical practice with clinical research using evidence-based medicine. Clin Med Res 5:45–52

    Article  PubMed  PubMed Central  Google Scholar 

  220. De Groot PC, Bleeker MW, van Kuppevelt DH, van der Woude LH, Hopman MT (2006) Rapid and extensive arterial adaptations after spinal cord injury. Arch Phys Med Rehabil 87:688–696

    Article  PubMed  Google Scholar 

  221. Driussi C, Ius A (2014) Structural and functional left ventricular impairment in subjects with chronic spinal cord injury and no overt cardiovascular disease. J Spinal Cord Med 37:85–92

    Article  PubMed  PubMed Central  Google Scholar 

  222. Matos-Souza JR, Pithon KR, Oliveira RT, Teo FH, Blotta MH, Cliquet A Jr, Nadruz W Jr (2011) Altered left ventricular diastolic function in subjects with spinal cord injury. Spinal Cord 49:65–69

    Article  CAS  PubMed  Google Scholar 

  223. 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

    Article  PubMed  PubMed Central  Google Scholar 

  224. West CR, Crawford M, Poormasjedi-Meibod M-S, 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 592:1771–1783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  225. Krumholz HM, Larson M, Levy D (1995) Prognosis of left ventricular geometric patterns in the Framingham Heart Study. J Am Coll Cardiol 25:879–884

    Article  CAS  PubMed  Google Scholar 

  226. Carrick-Ranson G, Hastings JL, Bhella PS, Shibata S, Levine BD (2013) The effect of exercise training on left ventricular relaxation and diastolic suction at rest and during orthostatic stress after bed rest. Exp Physiol 98:501–513

    Article  PubMed  Google Scholar 

  227. Dorfman TA, Rosen BD, Perhonen MA, Tillery T, McColl R, Peshock RM, Levine BD (2008) Diastolic suction is impaired by bed rest: MRI tagging studies of diastolic untwisting. J Appl Physiol 104:1037–1044

    Article  PubMed  Google Scholar 

  228. 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

    CAS  PubMed  Google Scholar 

  229. Davidoff G, Morris J, Roth E, Bleiberg J (1985) Cognitive dysfunction and mild closed head injury in traumatic spinal cord injury. Arch Phys Med Rehabil 66:489–491

    CAS  PubMed  Google Scholar 

  230. Davidoff G, Roth E, Thomas P, Doljanac R, Dijkers M, Berent S, Morris J, Yarkony G (1990) Depression and neuropsychological test performance in acute spinal cord injury patients: lack of correlation. Arch Clin Neuropsychol 5:77–88

    Article  CAS  PubMed  Google Scholar 

  231. Davidoff GN, Roth EJ, Haughton JS, Ardner MS (1990) Cognitive dysfunction in spinal cord injury patients: sensitivity of the Functional Independence Measure subscales vs neuropsychologic assessment. Arch Phys Med Rehabil 71:326–329

    CAS  PubMed  Google Scholar 

  232. Roth E, Davidoff G, Thomas P, Doljanac R, Dijkers M, Berent S, Morris J, Yarkony G (1989) A controlled study of neuropsychological deficits in acute spinal cord injury patients. Paraplegia 27:480–489

    Article  CAS  PubMed  Google Scholar 

  233. Wilmot CB, Cope DN, Hall KM, Acker M (1985) Occult head injury: its incidence in spinal cord injury. Arch Phys Med Rehabil 66:227–231

    Article  CAS  PubMed  Google Scholar 

  234. Dowler RN, O’Brien SA, Haaland KY, Harrington DL, Feel F, Fiedler K (1995) Neuropsychological functioning following a spinal cord injury. Appl Neuropsychol 2:124–129

    Article  CAS  PubMed  Google Scholar 

  235. Davidoff GN, Roth EJ, Richards JS (1992) Cognitive deficits in spinal cord injury: epidemiology and outcome. Arch Phys Med Rehabil 73:275–284

    Article  CAS  PubMed  Google Scholar 

  236. Davidoff G, Thomas P, Johnson M, Berent S, Dijkers M, Doljanac R (1988) Closed head injury in acute traumatic spinal cord injury: incidence and risk factors. Arch Phys Med Rehabil 69:869–872

    CAS  PubMed  Google Scholar 

  237. Dowler RN, Harrington DL, Haaland KY, Swanda RM, Fee F, Fiedler K (1997) Profiles of cognitive functioning in chronic spinal cord injury and the role of moderating variables. Int Neuropsychol Soc 3:464–472

    CAS  Google Scholar 

  238. O’Brien JT, Erkinjuntti T, Reisberg B, Roman G, Sawada T, Pantoni L, Bowler JV, Ballard C, DeCarli C, Gorelick PB, Rockwood K, Burns A, Gauthier S, DeKosky ST (2003) Vascular cognitive impairment. Lancet Neurol 2:89–98

    Article  PubMed  Google Scholar 

  239. Markus H, Cullinane M (2001) Severely impaired cerebrovascular reactivity predicts stroke and TIA risk in patients with carotid artery stenosis and occlusion. Brain 124:457–467

    Article  CAS  PubMed  Google Scholar 

  240. Phillips AA, Krassioukov AV, Zheng MMZ, Warburton DER (2013) Neurovascular coupling of the posterior cerebral artery in spinal cord injury: a pilot study. Brain Sci 3:781–789

    Article  PubMed  PubMed Central  Google Scholar 

  241. Bailey DM, Jones DW, Sinnott A, Brugniaux JV, New KJ, Hodson D, Marley CJ, Smirl JD, Ogoh S, Ainslie PN (2013) Impaired cerebral haemodynamic function associated with chronic traumatic brain injury in professional boxers. Clin Sci 124:177–189

    Article  CAS  PubMed  Google Scholar 

  242. Squair J, West CR, Krassioukov AV (2015) Neuroprotection, plasticity manipulation, and regenerative strategies to improve cardiovascular function following spinal cord injury. J Neurotrauma 32:609–621

    Article  PubMed  Google Scholar 

  243. Hou S, Tom VJ, Graham L, Lu P, Blesch A (2013) Partial restoration of cardiovascular function by embryonic neural stem cell grafts after complete spinal cord transection. J Neurosci 33:17138–17149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  244. Kalincík T, Choi EA, Féron F, Bianco J, Sutharsan R, Hayward I, Mackay-Sim A, Carrive P, Waite PME (2010) Olfactory ensheathing cells reduce duration of autonomic dysreflexia in rats with high spinal cord injury. Auton Neurosci 154:20–29

    Article  PubMed  Google Scholar 

  245. Dusart I, Schwab ME (1994) Secondary cell death and the inflammatory reaction after dorsal hemisection of the rat spinal cord. Eur J Neurosci 6:712–724

    Article  CAS  PubMed  Google Scholar 

  246. Popovich PG, Wei P, Stokes BT (1997) Cellular inflammatory response after spinal cord injury in Sprague–Dawley and Lewis rats. J Comp Neurol 377:443–464

    Article  CAS  PubMed  Google Scholar 

  247. Bartholdi D, Schwab ME (1997) Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur J Neurosci 9:1422–1438

    Article  CAS  PubMed  Google Scholar 

  248. Klusman I, Schwab ME (1997) Effects of pro-inflammatory cytokines in experimental spinal cord injury. Brain Res 762:173–184

    Article  CAS  PubMed  Google Scholar 

  249. Cuzzocrea S, Riley D, Caputi A, Salvemini D (2001) Antioxidant therapy: a new pharmacological approach in shock, inflammation, and ischemia/reperfusion injury. Pharmacol Rev 53:135–159

    CAS  PubMed  Google Scholar 

  250. Hall E (1994) Free radicals in central nervous system injury. New Compr Biochem 28:217–238

    Google Scholar 

  251. Gris D, Marsh DR, Dekaban GA, Weaver LC (2005) Comparison of effects of methylprednisolone and anti-CD11d antibody treatments on autonomic dysreflexia after spinal cord injury. Exp Neurol 194:541–549

    Article  CAS  PubMed  Google Scholar 

  252. Fleming JC, Bao F, Chen Y, Hamilton EF, Relton JK, Weaver LC (2008) Alpha4beta1 integrin blockade after spinal cord injury decreases damage and improves neurological function. Exp Neurol 214:147–159

    Article  CAS  PubMed  Google Scholar 

  253. Gris D, Marsh DR, Oatway MA, Chen Y, Hamilton EF, Dekaban GA, Weaver LC (2004) Transient blockade of the CD11d/CD18 integrin reduces secondary damage after spinal cord injury, improving sensory, autonomic, and motor function. J Neurosci 24:4043–4051

    Article  CAS  PubMed  Google Scholar 

  254. Ditor DS, Bao F, Chen Y, Dekaban GA, Weaver LC (2006) A therapeutic time window for anti-CD 11d monoclonal antibody treatment yielding reduced secondary tissue damage and enhanced behavioral recovery following severe spinal cord injury. J Neurosurg Spine 5:343–352

    Article  PubMed  Google Scholar 

  255. Marsh DR, Wong ST, Meakin SO, MacDonald JIS, Hamilton EF, Weaver LC (2002) Neutralizing intraspinal nerve growth factor with a trkA-IgG fusion protein blocks the development of autonomic dysreflexia in a clip-compression model of spinal cord injury. J Neurotrauma 19:1531–1541

    Article  PubMed  Google Scholar 

  256. Webb AA, Chan CB, Brown A, Saleh TM (2006) Estrogen reduces the severity of autonomic dysfunction in spinal cord-injured male mice. Behav Brain Res 171:338–349

    Article  CAS  PubMed  Google Scholar 

  257. Breault G, Altaweel W, Corcos J (2008) Management of autonomic dysreflexia. Curr Bladder Dysfunct Rep 3:13–16

    Article  Google Scholar 

  258. A clinical practice guideline for health-care professionals (2003) Paralyzed Veterans of America

    Google Scholar 

  259. Phillips AA, Elliott SL, Zheng MM, Krassioukov AV (2014) Selective alpha adrenergic antagonist reduces severity of transient hypertension during sexual stimulation after spinal cord injury. J Neurotrauma. doi:10.1089/neu.2014.3590

    Google Scholar 

  260. Sengoku A, Okamura K, Kimoto Y, Ogawa T, Namima T, Yamanishi T, Yokoyama T, Akino H, Maeda Y (2014) Botulinum toxin A injection for the treatment of neurogenic detrusor overactivity secondary to spinal cord injury: Multi-institutional experience in Japan. Int J Urol 22:306–309

    Article  PubMed  CAS  Google Scholar 

  261. Fougere RJ, Currie KD, Nigro MK, Stothers L, Rapoport D, Krassioukov AV (2016). Reduction in Bladder-Related Autonomic Dysreflexia after Onabotulinumtoxin A Treatment in Spinal Cord Injury. J Neurotrauma 33(18):1651–1657

    Google Scholar 

  262. Houtman S, Oeseburg B, Hughson RL, Hopman MT (2000) Sympathetic nervous system activity and cardiovascular homeostatis during head-up tilt in patients with spinal cord injuries. Clin Auton Res 10:207–212

    Article  CAS  PubMed  Google Scholar 

  263. Freeman R (2003) Treatment of orthostatic hypotension. Semin Neurol 23:435–442

    Article  PubMed  Google Scholar 

  264. Ten Harkel ADJ, Lieshout JJ, Wieling W (1992) Treatment of orthostatic hypotension with sleeping in the head-up tilt position, alone and in combination with fludrocortisone. J Intern Med 232:139–145

    Article  PubMed  Google Scholar 

  265. Chaudhuri R (2003) Autonomic failure. A textbook of clinical disorders of the autonomic nervous system, 4th edn. Edited by Mathias CJ, Bannister R (p 562, pound70.00). Published by Oxford University Press, Oxford, 2002. ISBN 0 19 262850 X. J Neurol Neurosurg Psychiatry 74:551–551

    Google Scholar 

  266. Groomes TE, Huang CT (1991) Orthostatic hypotension after spinal cord injury: treatment with fludrocortisone and ergotamine. Arch Phys Med Rehabil 72:56–58

    CAS  PubMed  Google Scholar 

  267. Mukand J, Karlin L, Barrs K, Lublin P (2001) Midodrine for the management of orthostatic hypotension in patients with spinal cord injury: A case report. Arch Phys Med Rehabil 82:694–696

    Article  CAS  PubMed  Google Scholar 

  268. Barber DB, Rogers SJ, Fredrickson MD, Able AC (2000) Midodrine hydrochloride and the treatment of orthostatic hypotension in tetraplegia: two cases and a review of the literature. Spinal Cord 38:109

    Article  CAS  PubMed  Google Scholar 

  269. Shin H-K, Yoo K-M, Chang HM, Caplan LR (1999) Bilateral intracranial vertebral artery disease in the New England medical Center Posterior Circulation Registry. Arch Neurol 56:1353–1358

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. International Collaboration on Repair Discoveries (ICORD), University of British Columbia – Vancouver, Vancouver, BC, Canada

    Aaron A. Phillips & Andrei V. Krassioukov

  2. Centre for Heart, Lung and Vascular Health, School of Health and Exercise Sciences, University of British Columbia – Okanagan, Kelowna, BC, Canada

    Aaron A. Phillips

  3. Division of Physical Medicine and Rehabilitation, Department of Medicine, University of British Columbia, Vancouver, BC, Canada

    Andrei V. Krassioukov

  4. Spinal Cord Program, GF Strong Rehabilitation Centre, Vancouver Coastal Health Authority, Vancouver, BC, Canada

    Andrei V. Krassioukov

Authors
  1. Aaron A. Phillips
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrei V. Krassioukov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrei V. Krassioukov .

Editor information

Editors and Affiliations

  1. Spinal Cord Injury Center, Heidelberg University Hospital, Heidelberg, Germany

    Norbert Weidner

  2. Spinal Cord Injury Center, Heidelberg University Hospital, Heidelberg, Germany

    Rüdiger Rupp

  3. Methodist Rehabilitation Center, University of Mississippi Medical Center, Veterans Administration Medical Center, Jackson, Mississippi, USA

    Keith E. Tansey

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Phillips, A.A., Krassioukov, A.V. (2017). Cardiovascular Dysfunction Following Spinal Cord Injury. In: Weidner, N., Rupp, R., Tansey, K. (eds) Neurological Aspects of Spinal Cord Injury. Springer, Cham. https://doi.org/10.1007/978-3-319-46293-6_14

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-46293-6_14

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-46291-2

  • Online ISBN: 978-3-319-46293-6

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation