Spinal cord injury (SCI) can cause devastating paralysis. However, it is not uncommon for SCI to be associated with a range of autonomic dysregulation, leading to cardiovascular, bladder, bowel, temperature, and/or sexual dysfunction. Individuals with a cervical or high-thoracic SCI face lifelong abnormalities in systemic arterial pressure control.1,2 Their resting arterial pressure generally is lower than that of able-bodied individuals. Spinal cord injury also commonly is accompanied by persistent orthostatic intolerance.3 Such cord-injured individuals can experience transient episodes of hypertension, known as “autonomic dysreflexia” (AD), which often is accompanied by disturbances in heart rate (HR) and rhythm.4 The severity of SCI varies between individuals, and this impacts greatly on cardiovascular control. For example, in the acute period of SCI, hypotension secondary to neurogenic shock affects between 20% and 30% of all spinal cord–injured individuals.5,6 However, clinical observations strongly suggest that the duration and severity of acute hypotension, to the point of requiring vasopressive therapy, correlate well with the severity of the SCI, both with cervical and high-thoracic injuries, and that this acute hypotension can last up to 5 weeks after injury.1,7–10 Likewise, the severity of AD correlates with the completeness of SCI, as assessed using the American Spinal Injury Association Impairment Scale11: only 27% of incomplete quadriplegics present with signs of AD versus 91% of complete quadriplegics.12
To further complicate matters, those same athletes with SCI who are potentially at a disadvantage due to the presence of cardiovascular dysfunction that could affect their performance are also the athletes who are able to “boost.”13,14 “Boosting” is AD that is intentionally induced by an athlete during training or competition.13,15 Boosting has been shown to increase athletic performance relative to a nonboosted state.14,16,17 However, there are significant health risks associated with boosting. For example, the increase in blood pressure (BP) that can occur during AD can cause serious adverse health events, like intracerebral hemorrhaging, seizures, myocardial ischemia, and even sudden death.18–22 Therefore, the practice of boosting has been banned in the Paralympics.15,23
The purpose of this article is to present the complex issue of the impact of SCI in sport, specifically focusing on AD and the potentially debilitating effects of unstable BP control among athletes. To begin, autonomic control of cardiovascular function in able-bodied and SCI individuals will be reviewed. Then, the clinical presentation of AD, its major triggers, and its management will be described. Finally, we review the literature evidence considering how autonomic dysfunction can impact athletic performance during both boosted and nonboosted states in athletes.
During the preparation of this article, a key word electronic literature search of articles, practice guidelines, and review articles pertaining to AD was conducted using MEDLINE, SportDiscus, and EMBASE. The key words “autonomic dysreflexia” and “spinal cord injury” were combined with “blood pressure,” “heart rate,” “exercise,” “boosting,” and “sport performance.” Abstracts were reviewed to identify papers in which trained athletes with SCI are subjects.
RESULTS AND DISCUSSION
What Do We Know About Autonomic Control of the Cardiovascular System?
Both components of the autonomic nervous system (parasympathetic and sympathetic) play crucial roles in the maintenance of normal arterial BP and HR (Figure 1). Parasympathetic control is prominent during restful states and is mediated through the vagus nerve, acting to decrease HR. Vagal control of the heart originates in the medulla and usually is spared after SCI.3 The vagus nerve innervates only the heart, with no effect on blood vessel function. The sympathetic nervous system innervates both cardiac muscle and smooth muscles within peripheral blood vessels and is dominant in times of physiological stress and exercise, acting to increase HR and BP.3 Sympathetic innervation to the heart and the majority of blood vessels to the upper extremities originates within upper thoracic segments (T1-T5); the vasculature beds in the gut and lower extremities are under the control of the more caudal T6 to L2 spinal sympathetic neurons.3 Injury below T6 tends to spare cardiac and most blood vessel control, whereas SCI above T6 can interrupt supraspinal sympathetic control to the heart, after which spinal circuits become solely responsible for the generation of sympathetic activity below the level of injury.1,24 For the purposes of this article, the term “high-level SCI” will denote any injury above T6. A high-level SCI affecting the autonomic nervous system results in low resting sympathetic tone below the level of injury, with mostly unopposed parasympathetic tone to the heart. This leads to reduced BP and HR at rest and abnormal cardiovascular responses to physiological stressors, including exercise.
What Are the General Cardiovascular Consequences of Spinal Cord Injury?
The acute period after injury to the spinal cord can be associated with life-threatening cardiovascular complications, including severe hypotension, bradyarrhythmias, and cardiac arrest.5,25 This condition is known as “neurogenic shock,” can last from days to weeks, and frequently requires vasopressive therapy. Although the occurrence of this condition diminishes over the weeks after SCI, cardiovascular control does not return to normal. Cervical and high-thoracic SCIs alter cardiovascular responses to exercise,26 impair circadian oscillations in BP,12,27,28 and, of most concern, predispose the individual to AD (Figure 2). Although this possibility should always be considered in the clinical setting, it remains the case that AD typically develops over time after SCI.29,30 It is well known that, after SCI, baseline resting BP is inversely correlated with level of injury; individuals with a high-level SCI have resting systolic BPs averaging 15 to 20 mmHg lower than those in able-bodied individuals.31 A similar pattern also can be seen with HR, resulting in a stroke volume that is lower in individuals with greater severity SCI.31,32 There is also peripheral pooling of blood in the lower extremities due to decreased sympathetic tone, in addition to altered muscle pump activity of the skeletal muscles below the level of injury.33 In general, the best-known and most commonly described phenomenon in response to exercise in high-level SCI individuals is poor HR and BP response. Furthermore, individuals with SCI also are prone to developing exercise-induced hypotension that may further affect their performance.26
What Is Autonomic Dysreflexia and Its Typical Presentation?
Autonomic dysreflexia is a condition characterized by episodes of extreme hypertension (systolic BP up to 300 mmHg); however, because individuals with SCI can have low systolic BP in the 90 to 110 mmHg range, an elevation in BP by 20 to 40 mmHg above baseline can be a sign of AD in the proper clinical context. Autonomic dysreflexia occurs in individuals with SCI at or above T6, below which the main sympathetic outflow exits the spinal cord, with an incidence of 50% to 90% after cervical and high-thoracic SCIs.34–37 Autonomic dysreflexia increases with ascending level and injury severity12,38 and is 3 times more common after complete compared with incomplete injuries.12 Anxiety and sadness are also more prevalent in individuals with autonomic dysfunction,39 and a recent survey of individuals with SCI identified the elimination of AD as a high priority for both paraplegics and quadriplegics.40 We have found that AD can occur during the acute phase of SCI, as early as 4 days after severe cervical injury.41
What Are the Possible Mechanisms Responsible for the Development of Autonomic Dysreflexia?
The mechanisms underlying the development of AD remain poorly understood, although there is evidence that neuroplastic changes (“rewiring”) within the central nervous system contribute to the development of this condition.3 From animal experiments, it has been established that autonomic instability after SCI results from changes occurring within spinal (central) and peripheral autonomic circuits, both in the acute and chronic stages after injury.42–44 Loss of supraspinal inhibitory control secondary to destruction of the descending vasomotor pathways during SCI is considered to be the predominant factor underlying the unstable BP that tends to follow SCI.45 Furthermore, the results of numerous animal and human studies suggest that plastic changes within the spinal cord (specifically, spinal sympathetic neurons and primary afferents) also contribute to the abnormal cardiovascular control and development of AD after SCI.46–48 Finally, alterations in the sensitivity of peripheral α-adrenergic receptors (receptors in the sympathetic nervous system) and plastic changes within peripheral sympathetic circuits also are considered contributing mechanisms in AD development.44,49
How Will the Completeness and Level of Injury Affect the Development of Autonomic Dysreflexia?
To answer this question, we must review our knowledge on neural control of the cardiovascular system (Figure 1). Injury to the spinal cord is often limited to a small area that disrupts spinal pathways affecting both sympathetic and parasympathetic components, as well as cardiovascular homeostasis.45,50 The heart receives innervation from both the parasympathetic (via cranial nerve X, the vagus nerve) and the sympathetic (via the upper thoracic spinal segments, T1-T5) nervous systems. Blood vessels in the upper half of the body receive sympathetic innervation from T1 to T5 spinal sympathetic neurons, whereas the vasculature in the gut and lower extremities receives sympathetic innervation from caudal T6 to L2 spinal sympathetic neurons. Cervical or upper thoracic SCI disrupts sympathetic input to the heart and blood vessels below the level of injury, but parasympathetic innervation remains intact (because cranial nerve X bypasses the spinal cord). With injuries below T6, both sympathetic and parasympathetic innervations of the heart are maintained; however, sympathetic control of the critical splanchnic bed, and of lower extremity blood vessels, is lost below the injured segments (Figure 1).
What Are the Most Common Triggers of Autonomic Dysreflexia Episodes?
The sudden increases in arterial BP that are associated with AD can be provoked by a range of different noxious and nonnoxious stimuli, including bowel and bladder distension, spasms, and pressure sores.30 Routine procedures (like catheterization and manipulation of an indwelling catheter), bladder percussion, and urinary tract infections are among other well-known precipitants of AD. There also are numerous reports of iatrogenic triggering factors, like cystoscopy, cystometry, vibration (Figure 2) and electrostimulation for ejaculation, and the electrical stimulation of muscles.51–53
The clinical presentation of AD is variable and ranges from mildly uncomfortable symptoms (eg, sweating and piloerection) to life-threatening crises.18,54,55 In addition to extreme hypertension, additional signs and symptoms include pounding headache, slow HR, increased spasticity, sweating, blurred vision, nasal congestion, cutis anserina (goose bumps), piloerection, upper body flushing, and general apprehension (Table).1,34,56
How Quickly After Spinal Cord Injury Will the First Episode of Autonomic Dysreflexia Typically Occur?
Autonomic dysreflexia typically develops weeks to months after SCI29,30; however, it can occur as early as 4 days after a severe cervical injury41,57 and is likely underrecognized during the acute phase of SCI.41
What Do You Do When Autonomic Dysreflexia Is in Progress?
The best management of AD is prevention. By knowing the major triggers that could result in an episode of AD, individuals and their caregivers could be prepared to face and/or avoid life-threatening emergencies. The management of the urinary bladder and bowel is paramount for these individuals because 90% of AD cases are triggered by some process or procedure involving these organs.58
Once an episode of AD has started, one must promptly follow a well-established management protocol.59 As a first step, it is recommended that the patient is shifted into a seated position and that all potentially restrictive clothing is loosened. By elevating the patient's head, we are attempting to use the orthostatic reflex to decrease any BP elevation. If arterial BP continues to be elevated, the next step in management is to reduce any irritation to the bladder and bowel (eg, check for possible catheter blockage or perform bladder catheterization or bowel disimpaction). If these nonpharmacological measures fail and arterial BP is 150 mmHg or greater, then pharmacological management should be initiated.59 However, the Consortium for Spinal Cord Medicine59 does not identify any particular medication as best for the management of AD. Numerous pharmacological agents have been proposed to manage episodes of AD.60–62 Short-acting pharmacological oral agents (nifedipine and captopril) or topical nitrates (ie, ointment or paste) are the most commonly used agents.58
What Do We Know About Self-Induced Episodes of Autonomic Dysreflexia (Boosting) After Spinal Cord Injury?
The important components of cardiovascular control needed for exercise performance include the ability of arterial BP and HR to respond appropriately to the increased demands of the body during exercise.63,64 This requires balanced coordination of both sympathetic and parasympathetic signals in the regulation of the cardiovascular system, resulting in sufficient blood redistribution to the muscles. This is possible only with proper sympathetic control of the cardiac and regional blood vessels, in addition to skeletal muscle pump activity.3 Other systems influence exercise performance, as well, including respiratory and muscular function, and temperature and sweat regulation.3 Unfortunately, all of these systems, including the cardiovascular, are commonly affected by SCI, and, as was presented previously, the extent of dysfunction of these systems depends on the level and severity of the injury.
With respect to exercise and cardiovascular system adaptation after SCI, studies consistently show that SCI athletes with injuries above T6 have lower maximal HR (due to altered sympathetic tone and reduced catecholamine release),16 lower maximal oxygen uptake (V[Combining Dot Above]O2),65 and lower peak power (W)66 in response to submaximal and maximal exercise relative to athletes with lower levels of SCI and athletes with an intact autonomic nervous system. Furthermore, as described previously, a significant number of individuals with SCI, including elite athletes, suffer from resting and orthostatic hypotension that can further contribute to fatigue and alter their athletic performance. This altered autonomic control of the cardiovascular system that can impact exercise performance creates the potential for an uneven playing field between wheelchair athletes who practice inappropriate strategies to accommodate for their loss of (physiological) function. Boosting, or voluntarily induced AD, is a practice unique to athletes with a high-level SCI and is sometimes used by this population to improve exercise performance.13,15 There are various anecdotal reports of different methods of boosting during competition, including sitting on one's scrotum, clamping one's Foley catheter, and even breaking one's big toe.
Presently, only a few studies have specifically compared the cardiovascular responses of SCI athletes in a boosted versus nonboosted state. Wheeler et al14 and Burnham et al67 used the same SCI athletes with cervical injuries who were elite road racers. Athletes were observed under boosted and nonboosted conditions while performing a 7.5-km race and during a graded arm exercise to test maximal effort in a controlled environment. Schmid et al16 studied 6 elite athletes with a high-level SCI, all performing a graded arm exercise to test maximal effort using a wheelchair ergometer. In all 3 of these studies, boosting was achieved either by increasing fluid intake before the event to overdistend the bladder or by prolonged sitting in the wheelchair before the exercise protocol.
With the graded arm exercise, Burnham and Wheeler found that, during a boosted state, athletes experienced a significant increase in peak HR, peak BP, circulating norepinephrine levels, maximal V[Combining Dot Above]O2, and peak W relative to when nonboosted. During the 7.5-km wheelchair race, there was a significant decrease in racing time in the boosted (22.6 ± 6.6 min) versus nonboosted (25.6 ± 9 min) state, which translated to a mean performance increase of 9.2%.67 There also was a lower rating of perceived exertion by the athletes during the boosted state.
Athletes participating in Wheeler's and Burnham's studies also filled out a questionnaire on their practice of boosting, and all reported having used boosting to improve their performance during competition. They reported that boosting subjectively increased arm strength and endurance, decreased arm stiffness, improved breathing, and increased alertness and aggressiveness. Half of the subjects also reported that they could “boost too much,” and the majority felt that they could not boost predictably. Side effects frequently experienced with boosting included headaches and excessive shivering and sweating. All of the athletes believed that the practice of boosting for the purpose of performance enhancement is widespread (90%-100% prevalence) among competitive athletes with a high-level SCI.
Athletes participating in a study by Schmid et al16 denied using boosting to improve their performance during a race. However, the majority of them knew about boosting and had experienced side effects of AD during training. In these athletes, responses to exercises during the boosted state also revealed significant increases in peak HR, peak BP, circulating norepinephrine levels, maximal V[Combining Dot Above]O2, and peak W. These changes were consistent with those demonstrated in the studies by Wheeler et al14 and Burnham et al.67 Unfortunately, none of these studies had a control group with similar levels of injury and training but an intact central nervous system, so as to determine how much boosting actually compensates for the impact of autonomic dysregulation on exercise performance.
In these studies, arterial BP responses during the boosted state were significantly elevated, sometimes exceeding 200 mmHg.14,67 Although there are limited data demonstrating improved performance with boosting in high-level SCI athletes, it is very important to be aware of the potential dangers of uncontrolled AD. No adverse consequences directly linked to boosting in competition have been documented to date. However, numerous reports exist of significant consequences in clinical situations, including myocardial infarction, seizures, intracranial hemorrhages, and sudden death.18,22,68
The latest study on the use of boosting among athletes was conducted during the Beijing Summer Paralympic Games in 2008. In this study, Bhambhani et al15 examined the perception of boosting by asking Paralympians with SCI to answer a self-report questionnaire. Of the 99 participants, a majority were involved in wheelchair rugby (54.2%) and familiar with the term boosting (54%). Only 10 participants acknowledged that they used boosting to improve their performance [wheelchair rugby (55.5%), wheelchair marathon (22.2%), and long-distance racing (22.2%)]. The majority of individuals (80%) who acknowledged having used boosting during competition had an injury at T6 or above. This is not surprising because the majority of these individuals with a high injury experience significant cardiovascular dysfunction that hinders their athletic performance. The results of this study underline how boosting continues to be practiced by elite athletes with a high-level SCI, despite recognized health risks and the ban of this practice by the International Paralympic Committee (IPC).23
Due to potential health risks of boosting, the IPC and other governing bodies have long struggled with the dilemma of how to address this issue in elite athletes.23 Although boosting can be used to enhance performance, significant controversy arises as to whether boosting should be considered a form of doping, largely because of the way in which “doping” has been defined as “the administration of or use of any substance foreign to the athlete's body, or of any physiological substance taken in abnormal quantity or taken by abnormal route of entry in to the body with the sole intention of artificially increasing performance in competition.”23 According to this definition, the practice of boosting does not meet specific requirements for doping, which creates a conundrum for these governing bodies. Adding to the controversy is the difficulty proving whether episodes of high BP identified during competition are intentionally induced because spontaneous episodes of AD are a common occurrence in the daily lives of individuals with a high-level SCI.
Concern for the potential health risks of uncontrolled hypertension has led the IPC to officially ban boosting in the Paralympic Movement for health safety reasons.69 Screening for AD in athletes before competition was first instituted at the 1996 Atlantic Summer Paralympic Games and have continued since.23 To screen for AD, the IPC medical staff check athletes for signs of AD before a race or an event and take BP measurements. If the BP is significantly elevated (systolic BP >180 mmHg), the athlete is given time to rest and attempt to lower their BP, and the BP is then remeasured.69
Devastating paralysis, a range of autonomic dysfunctions, and abnormal cardiovascular control after SCI present significant challenges for these individuals remaining active and participating in competitive sports. The added complexity and variations in cardiovascular disorders that these individuals can experience on a daily basis (from resting hypotension to orthostatic hypotension to episodes of life-threatening hypertension associated with AD) make the process of training and competing even more challenging. However, despite all these challenges, many individuals with SCI continue to be active and, most importantly, to benefit from physical activities not only because of social interactions but also because of significant resultant health benefits. Medical practitioners who are involved in the care of wheelchair athletes should be aware of the unique array of cardiovascular dysfunction that can result from SCI and may occur at any time, even with seemingly innocuous triggers. Prompt recognition and appropriate management of these conditions, including episodes of AD, could be life saving. Moreover, those who care for wheelchair athletes must be aware of the potential use of boosting by some of these athletes. Clearly, further research is warranted to determine whether presently established IPC classifications of Paralympic athletes could benefit from the addition of autonomic testing.70
1. Mathias CJ, Frankel HLBannister R, Mathias CJ. Autonomic disturbances in spinal cord lesions Autonomic Failure: A Textbook of Clinical Disorders of the Autonomic Nervous System. 20024th ed Oxford, UK Oxford Medical Publications:839–881
2. Krassioukov A, Claydon VE. The clinical problems in cardiovascular control following spinal cord injury: an overview. Prog Brain Res. 2006;152:223–229
3. Krassioukov A. Autonomic function following cervical spinal cord injury. Respir Physiol Neurobiol. 2009;169:157–164
4. Krassioukov A, Eng JJ, Warburton DE, et al. A systematic review of the management of orthostatic hypotension after spinal cord injury. Arch Phys Med Rehabil. 2009;90:876–885
5. Lehmann KG, Lane JG, Piepmeier JM, et al. Cardiovascular abnormalities accompanying acute spinal cord injury in humans: incidence, time course and severity. J Am Coll Cardiol. 1987;10:46–52
6. Piepmeier JM, Lehmann KB, Lane JG. Cardiovascular instability following acute cervical spinal cord trauma. Cent Nerv Syst Trauma. 1985;2:153–160
7. Atkinson PP, Atkinson JL. Spinal shock. Mayo Clin Proc. 1996;71:384–389
8. Hadley M. Blood pressure management after acute spinal cord injury. Neurosurgery. 2002;50:S58–S62
9. Nacimiento W, Noth J. What, if anything, is spinal shock? Arch Neurol. 1999;56:1033–1035
10. Vale FL, Burns J, Jackson AB, et al. 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. 1997;87:239–246
11. Marino RJ, Barros T, Biering-Sorensen F, et al. International standards for neurological classification of spinal cord injury. J Spinal Cord Med. 2003;26(suppl 1):S50–S56
12. Curt A, Nitsche B, Rodic B, et al. Assessment of autonomic dysreflexia in patients with spinal cord injury. J Neurol Neurosurg Psychiatry. 1997;62:473–477
13. Harris P. Self-induced autonomic dysreflexia (‘boosting') practised by some tetraplegic athletes to enhance their athletic performance. Paraplegia. 1994;32:289–291
14. Wheeler G, Cumming D, Burnham R, et al. Testosterone, cortisol and catecholamine responses to exercise stress and autonomic dysreflexia in elite quadriplegic athletes. Paraplegia. 1994;32:292–299
15. Bhambhani Y, Mactavish J, Warren S, et al. Boosting in athletes with high-level spinal cord injury: knowledge, incidence and attitudes of athletes in paralympic sport. Disabil Rehabil. 2010;32:2172–2190
16. Schmid A, Schmidt-Trucksass A, Huonker M, et al. Catecholamines response of high performance wheelchair athletes at rest and during exercise with autonomic dysreflexia. Int J Sports Med. 2001;22:2–7
17. Webborn AD. “Boosting” performance in disability sport. Br J Sports Med. 1999;33:74–75
18. Eltorai I, Kim R, Vulpe M, et al. Fatal cerebral hemorrhage due to autonomic dysreflexia in a tetraplegic patient: case report and review. Paraplegia. 1992;30:355–360
19. Yarkony GM, Katz RT, Wu Y. Seizures secondary to autonomic dysreflexia. Arch Phys Med Rehabil. 1986;67:834–835
20. Pine ZM, Miller SD, Alonso JA. Atrial fibrillation associated with autonomic dysreflexia. Am J Phys Med Rehabil. 1991;70:271–273
21. Calder KB, Estores IM, Krassioukov A. Autonomic dysreflexia and associated acute neurogenic pulmonary edema in a patient with spinal cord injury: a case report and review of the literature. Spinal Cord. 2009;47:423–425
22. Ho CP, Krassioukov AV. Autonomic dysreflexia and myocardial ischemia. Spinal Cord. 2010;48:714–715
23. Position Statement on Autonomic Dysreflexia and Boosting. International Paralympic Committee Handbook. 2006 Bonn, Germany
24. Krassioukov A. Which pathways must be spared in the injured human spinal cord to retain cardiovascular control? Prog Brain Res. 2005;152:39–47
25. Bilello JF, Davis JW, Cunningham MA, et al. Cervical spinal cord injury and the need for cardiovascular intervention. Arch Surg. 2003;138:1127–1129
26. Claydon VE, Hol AT, Eng JJ, et al. Cardiovascular responses and postexercise hypotension after arm cycling exercise in subjects with spinal cord injury. Arch Phys Med Rehabil. 2006;87:1106–1114
27. Krum H, Louis WJ, Brown DJ, et al. Diurnal blood pressure variation in quadriplegic chronic spinal cord injury patients. Clin Sci (Lond). 1991;80:271–276
28. Munakata M, Kameyama J, Nonukawa T, et al. Circadian blood pressure rhythm in patients with higher and lower spinal cord injury: simultaneous evaluation of autonomic nervous activity and physical activity. J Hypertens. 1997;15:1745–1749
29. Mathias CJ, Frankel HL. Cardiovascular control in spinal man. Annu Rev Physiol. 1988;50:577–592
30. Teasell R, Arnold AP, Krassioukov AV, et al. Cardiovascular consequences of loss of supraspinal control of the sympathetic nervous system following spinal cord injuries. Arch Phys Med Rehabil. 2000;81:506–516
31. Claydon VE, Krassioukov AV. Orthostatic hypotension and autonomic pathways after spinal cord injury. J Neurotrauma. 2006;23:1713–1725
32. DiPette D, Gavras I, North W, et al. Vasopressin response to hyperosmotic stimulus: blood pressure effect in normal subjects and patients with impaired sympathetic systems. Clin Exp Hypertens. 1984;A6:851–861
33. Hopman MT, Groothuis JT, Flendrie M, et al. Increased vascular resistance in paralyzed legs after spinal cord injury is reversible by training. J Appl Physiol. 2002;93:1966–1972
34. Elliott S, Krassioukov A. Malignant autonomic dysreflexia in spinal cord injured men. Spinal Cord. 2005;44:386–392
35. Lindan R, Joiner E, Freehafer AA, et al. Incidence and clinical features of autonomic dysreflexia in patients with spinal cord injury. Paraplegia. 1980;18:285–292
36. Mathias CJ, Frankel HL. Clinical manifestations of malfunctioning sympathetic mechanisms in tetraplegia. J Auton Nerv Syst. 1983;7:303–312
37. Karlsson AK. Autonomic dysreflexia. Spinal Cord. 1999;37:383–391
38. Helkowski WM, Ditunno JF Jr, Boninger M. Autonomic dysreflexia: incidence in persons with neurologically complete and incomplete tetraplegia. J Spinal Cord Med. 2003;26:244–247
39. Widerstrom-Noga E, Cruz-Almeida Y, Krassioukov A. Is there a relationship between chronic pain and autonomic dysreflexia in persons with cervical spinal cord injury. J Neurotrauma. 2004;21:195–204
40. Anderson KD. Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma. 2004;21:1371–1383
41. Krassioukov AV, Furlan JC, Fehlings MG. Autonomic dysreflexia in acute spinal cord injury: an under-recognized clinical entity. J Neurotrauma. 2003;20:707–716
42. Krassioukov AV, Weaver LC. Reflex and morphological changes in spinal preganglionic neurons after cord injury in rats. Clin Exp Hypertens. 1995;17:361–373
43. Krassioukov AV, Weaver LC. Episodic hypertension due to autonomic dysreflexia in acute and chronic spinal cord-injured rats. Am J Physiol. 1995;268:H2077–H2083
44. Alan N, Ramer LM, Inskip JA, et al. Recurrent autonomic dysreflexia exacerbates vascular dysfunction after spinal cord injury. Spine J. 2010;10:1108–1117
45. Furlan JC, Fehlings MG, Shannon P, et al. Descending vasomotor pathways in humans: correlation between axonal preservation and cardiovascular dysfunction after spinal cord injury. J Neurotrauma. 2003;20:1351–1363
46. Krassioukov AV, Weaver LC. Morphological changes in sympathetic preganglionic neurons after cord injury in rats. Neuroscience. 1996;70:211–225
47. Ackery AD, Norenberg MD, Krassioukov A. Calcitonin gene-related peptide immunoreactivity in chronic human spinal cord injury. Spinal Cord. 2007;45:678–686
48. Krenz NR, Meakin SO, Krassioukov AV, et al. Neutralizing intraspinal nerve growth factor blocks autonomic dysreflexia caused by spinal cord injury. J Neurosci. 1999;19:7405–7414
49. Arnold JM, Feng QP, Delaney GA, et al. Autonomic dysreflexia in tetraplegic patients: evidence for alpha-adrenoceptor hyper-responsiveness. Clin Auton Res. 1995;5:267–270
50. Krassioukov AV, Bunge RP, Puckett WR, et al. The changes in human spinal cord sympathetic preganglionic neurons after spinal cord injury. Spinal Cord. 1999;37:6–13
51. Chang CP, Chen MT, Chang LS. Autonomic hyperreflexia in spinal cord injury patient during percutaneous nephrolithotomy for renal stone: a case report. J Urol. 1991;146:1601–1602
52. Giannantoni A, Di Stasi SM, Scivoletto G, et al. Autonomic dysreflexia during urodynamics. Spinal Cord. 1998;36:756–760
53. Sheel AW, Krassioukov AV, Inglis JT, et al. Autonomic dysreflexia during sperm retrieval in spinal cord injury: influence of lesion level and sildenafil citrate. J Appl Physiol. 2005;99:53–58
54. Kirshblum SC, House JG, O'connor KC. Silent autonomic dysreflexia during a routine bowel program in persons with traumatic spinal cord injury: a preliminary study. Arch Phys Med Rehabil. 2002;83:1774–1776
55. Ekland MB, Krassioukov AV, McBride KE, et al. 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. 2008;31:33–39
56. Bishop VS, Thames MD, Schmid PG. Effects of bilateral vagal cold block on vasopressin in conscious dogs. Am J Physiol. 1984;246:R566–R569
57. Silver JR. Early autonomic dysreflexia. Spinal Cord. 2000;38:229–233
58. Krassioukov A, Warburton DE, Teasell R, et al. A systematic review of the management of autonomic dysreflexia after spinal cord injury. Arch Phys Med Rehabil. 2009;90:682–695
59. . Acute management of autonomic dysreflexia: adults with spinal cord injury presenting to health-care facilities. Consortium for spinal cord. J Spinal Cord Med. 2001;20:284–308
60. Acute Management of Autonomic Dysreflexia: Adults With spinal Cord Injury Presenting to Health-Care Facilities. Clinical Practice Guidelines. 1997 Consortium for Spinal Cord Medicine. Washington, DC: Paralyzed Veterans of America:1–37
61. Naftchi NE, Richardson JS. Autonomic dysreflexia: pharmacological management of hypertensive crises in spinal cord injured patients. J Spinal Cord Med. 1997;20:355–360
62. Blackmer J. Rehabilitation medicine: 1. Autonomic dysreflexia. CMAJ. 2003;169:931–935
63. Figoni SF. Exercise responses and quadriplegia. Med Sci Sports Exerc. 1993;25:433–441
64. Phillips WT, Kiralti BJ, Sarkarati M, et al. Effect of spinal cord injury on the heart and cardiovascular fitness. Curr Probl Cardiol. 1998;23:649–717
65. Davis GM, Servedio FJ, Glaser RM, et al. Cardiovascular responses to arm cranking and FNS-induced leg exercise in paraplegics. J Appl Physiol. 1990;69:671–677
66. Hopman MT, Oeseburg B, Binkhorst RA. Cardiovascular responses in persons with paraplegia to prolonged arm exercise and thermal stress. Med Sci Sports Exerc. 1993;25:577–583
67. Burnham R, Wheeler G, Bhambhani Y, et al. Intentional induction of autonomic dysreflexia among quadriplegic athletes for performance enhancement: efficacy, safety, and mechanism of action. Clin J Sport Med. 1994;4:1–10
68. Pan SL, Wang YH, Lin HL, et al. Intracerebral hemorrhage secondary to autonomic dysreflexia in a young person with incomplete C8 tetraplegia: a case report. Arch Phys Med Rehabil. 2005;86:591–593
69. Legg D, Mason DS. Autonomic dysreflexia in wheelchair sport: a new game in the legal arena? Marq Sports L Rev. 1998;8:225–262
70. Mills PB, Krassioukov A. Autonomic function as a missing piece of the classification of Paralympic athletes with spinal cord injury. Spinal Cord. 2011;49:768–776