Scand J Med Sci Sports 2014: ••: ••–•• doi: 10.1111/sms.12308
© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Cardiovascular control, autonomic function, and elite endurance performance in spinal cord injury C. R. West1, C. M. Gee1, C. Voss2, M. Hubli1, K. D. Currie1, J. Schmid3, A. V. Krassioukov1,4,5 1
International Collaboration on Repair Discoveries (ICORD), Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada, 2Centre for Hip Health and Mobility, Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada, 3Paracycling Classification, International Cycling Union, Aigle, Switzerland, 4Division of Physical Medicine and Rehabilitation, Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada, 5GF Strong Rehabilitation Centre, Vancouver Health Authority, Vancouver, British Columbia, Canada Corresponding author: Andrei Krassioukov, MD, PhD, FRCPC, ICORD-BSCC, UBC, 818 West 10th Avenue, Vancouver, BC V5Z 1M9, Canada. Tel: 1 604 675 8819, Fax: 1 604 675 8820, E-mail: [email protected] Accepted for publication 17 July 2014
We aimed to determine the relationship between level of injury, completeness of injury, resting as well as exercise hemodynamics, and endurance performance in athletes with spinal cord injury (SCI). Twenty-three elite male paracycling athletes (C3-T8) were assessed for neurological level/completeness of injury, autonomic completeness of injury, resting cardiovascular function, and time to complete a 17.3-km World Championship time-trial test. A subset were also fitted with heart rate (HR) monitors and their cycles were fitted with a global positioning systems device (n = 15). Thoracic SCI exhibited higher seated systolic blood pressure along with superior timetrial performance compared with cervical SCI (all
P < 0.01). When further stratified by autonomic completeness of injury, the four athletes with cervical autonomic incomplete SCI exhibited a faster time-trial time and a higher average speed compared with cervical autonomic complete SCI (all P < 0.042). Maximum and average HR also tended to be higher in cervical autonomic incomplete vs autonomic complete. There were no differences in time-trial time, HR, or speed between thoracic autonomic complete vs incomplete SCI. In conclusion, autonomic completeness of injury and the consequent ability of the cardiovascular system to respond to exercise appear to be a critical determinant of endurance performance in elite athletes with cervical SCI.
Individuals with spinal cord injury (SCI) exhibit secondary complications that extend far beyond paralysis. Some of the most devastating side effects of SCI relate to impaired cardiovascular function, which increases cardiovascular disease risk (Garshick et al., 2005; Cragg et al., 2013). The extent of cardiovascular dysfunction is known to be level dependent, whereby those with the most rostral injuries exhibit the most severe impairment in cardiorespiratory function and exercise capacity (Haisma et al., 2006; Taylor et al., 2010). Reduced exercise capacity in cervical SCI is attributed to impaired motor function, loss of the sub-lesional venous muscle pump, reduced blood volume, and a decentralized sympathetic nervous system, which alters vascular tone and ultimately reduces stroke volume, cardiac output and oxygen delivery (Houtman et al., 2000; Teasell et al., 2000; Theisen, 2012). Autonomic completeness of injury (i.e., integrity of descending spinal autonomic pathways) also provides independent predictive value for resting cardiovascular function in cervical SCI (West et al., 2014b). We and others have found a relatively high proportion of
individuals with cervical SCI exhibit sparing of descending autonomic fibers (Claydon & Krassioukov, 2006; Sahota et al., 2012; West et al., 2014b). It is plausible that such sparing may circumvent the “traditional” limitations that are thought to occur because of decentralized sympathetic circuits in cervical SCI. To this end, we recently reported that the group mean maximum heart rate (HR) of elite wheelchair rugby athletes with cervical SCI exceeded 150 bpm, and that the HR achieved was strongly correlated to the degree of disruption to spinal autonomic pathways (West et al., 2013b). Such exerciseinduced tachycardia would be expected to confer multiple advantages during exercise, such as an enhancement of cardiac output and endurance performance. This advantage is anticipated to be most pronounced in exercise modalities that are heavily dependent on aerobic exercise capacity, such as long-distance wheelchair racing and/or paracycling. Conversely, it has been reported that individuals with a high-thoracic SCI (i.e., T1-T3) may sustain complete injury to the descending spinal autonomic pathways, yet spare the motor/sensory pathways (Claydon & Krassioukov, 2006). Such instances are also expected to compromise vaso- and
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West et al. sudo-motor function to a similar degree that occurs in autonomic complete cervical SCI. To examine the complex relationships between lesion level, neurological completeness of injury, autonomic completeness of injury, and endurance performance, we conducted a comprehensive assessment of resting cardio-autonomic function and endurance performance in 23 male athletes with SCI during the time-trial event of the 2013 Paracycling World Championships. We hypothesized that athletes with thoracic SCI would exhibit superior resting cardiovascular function and time-trial performance compared with athletes with cervical SCI. We also hypothesized that autonomic incomplete cervical/high-thoracic SCI would outperform their lesion-level matched autonomic complete counterparts. Methods Participants All protocols were approved by the institutional ethics committee and endorsed by the International Paralympic Committee, and all athletes provided written informed consent. We conducted all assessments during the 2013 Paracycling World Championships (Baie Comeau, Canada). We tested 11 of 12 competing athletes in the male H1 class (cervical SCI), and 12 of 17 competing athletes in the male H2 class (thoracic SCI), for a total of 23 athletes. Thus, our sample represented 80% of the top SCI paracyclists in the world. None of the athletes smoked or had a history of cardiopulmonary disease. Athletes presented with a traumatic SCI between C5 and T8 (age 41 ± 8 years, time since injury 17 ± 7 years). Self-reported stature and mass were 1.79 ± 0.12 m and 66 ± 8 kg, respectively. Athletes self-reported to train for an average of 14 h/ week (range 5–32 h/week).
Methods of measurement Neurological classification and questionnaires We conducted a neurological classification in accordance with the International Standards for the Neurological Classification of SCI to determine the American Spinal Injuries Association Impairment Scale (AIS) grade (Kirshblum et al., 2011). We also administered the revised International Standards to document remaining autonomic function after SCI (Krassioukov et al., 2012). Athletes selfadministered a demographics and general autonomic function questionnaire. Among other questions, the athletes were specifically asked; “do you have any episodes of autonomic dysreflexia (AD), a condition where your blood pressure rises very fast, usually resulting in symptoms such as severe headache, sweating, excessive spasms, hot/cold flushes, and nasal congestion”.
Cardiovascular assessment We used a one lead electrocardiogram and finometer (Finometer, Finapres Medical Systems BV, Arnhem, the Netherlands) for the beat-by-beat assessment of HR and blood pressure (BP, respectively. An automated BP cuff (Dinamap, General Electric Pro 300V2; Tampa, Florida, USA) was also fitted over the brachial artery and inflated every minute to calibrate the finometer. Resting systolic and diastolic BP as well as HR were recorded for 10 min during supine rest using an analog-to-digital converter (Powerlab/ 16SP model ML795; ADInstruments, Colorado Springs, Colorado, USA) interfaced with a computer. Next, we assessed BP and HR during a 10-min sit-up test; briefly, we moved participants to
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an upright seated position with their legs hanging off the side of the bed at 90 degrees. This sit-up position mimics that experienced while seated in a wheelchair, except the lower legs and feet are unsupported. We informed participants as to the importance of this procedure being passive and instructed them to not assist in the “sit-up” procedure. We defined orthostatic hypotension (OH) as a ≥ 20 mmHg drop in systolic BP (SBP) or a ≥ 10 mmHg drop in diastolic BP (DBP) within 3 min of assuming an upright position (Consensus Committee of the American Autonomic Society and the American Academy of Neurology, 1996). We terminated the test early if the participant exhibited signs/symptoms of presyncope or on athlete request.
Sympathetic skin responses (SSRs) Following 10 min of supine rest, we assessed athletes for SSRs to median nerve stimulation at the wrist. The SSR assessment records a change in skin conductance after activation of sweat glands in response to various stimuli (Cariga et al., 2002; Vetrugno et al., 2003). The SSR tests sudomotor function, but has previously been shown to correlate well with the phase 4 overshoot during Valsalva (Previnaire et al., 2012), suggesting it acts as a proxy for assessing the integrity of descending autonomic (vasomotor) pathways. We conducted the SSR protocol as previously described in our laboratory (Claydon & Krassioukov, 2006; West et al., 2013b, 2014b). Briefly, we simultaneously recorded bilateral plantar and palmar SSRs over a 10-s period at a band pass of 3 Hz to 3 kHz, using a Dantec Keypoint® 4 system (Natus Medical Incorporated, San Carlos, California, USA). To minimize the well-known habituation of these responses, we applied the stimuli in random order and with variable time delays (minimum delay 90 s; Cariga et al., 2001). Five recordings in response to median nerve stimulation (0.2-ms duration, 10–20 mA intensity) were obtained at each site. We deemed an SSR present when there was a clear positive deflection from baseline (Kucera et al., 2004). For analyses, we only assessed the number of present palmar SSRs, since these responses are controlled by sympathetic pre- and post-ganglionic fibres that exit the spinal cord at a similar level to those that innervate the heart (i.e., T1-T5). We excluded any potential that coincided with muscle spasm, limb movement, or cough. Left and right palmar responses were summed and divided by two such that an average number of responses were calculated. Based on our previous findings that even minimal sparing of descending sympathetic fibers confers cardiovascular benefits (West et al., 2014b), we defined individuals as autonomic complete if they had 0 or 1 SSRs, and autonomic incomplete if they had between 2 and 5 SSRs.
Exercise responses We assessed time to complete the 17.3-km time-trial event (two laps of the same course) during the 2013 Paracycling World Championships. Athletes raced in their respective paracycling class as determined during a separate classification that was conducted by the Union Cycliste Internationale. Class H1 raced in the early afternoon and class H2 raced in the late afternoon. Within their respective classes, athletes started the course in 1-min intervals. We obtained the athletes’ official time-trial times, measured to the nearest millisecond, for analyses. Additionally, 1 h prior to the race, we fitted HR monitors to a subset (n = 15) of the athletes (Polar team System 2.0, Polar Electro Oy, Kempele, Finland) and instrumented the racing cycle of a subset of athletes (n = 15) with a Global Positioning System (GPS) device (QStarz Q100XT, Qstarz International Co., Ltd., Taipei, Taiwan). The GPS device was configured to log the following variables second by second: date and time, geographic coordinates (latitude and longitude), speed (km/h), distance (m), and elevation (m). Physiologic and
Endurance performance in SCI performance characteristics (speed) throughout the race were mapped and analyzed using Geographic Information Systems Software (ArcGIS v.10.1; Esri, Redlands, California, USA). Peak HR (HRpeak) and peak speed was defined as the highest value averaged over a rolling 30-s epoch.
Data analyses We carried out two levels of analyses to examine the effect of injury level and autonomic completeness of injury on resting cardiovascular function and exercise performance. First, we compared cervical SCI (n = 11), high-thoracic SCI (T1-T5; n = 6) and low-thoracic SCI (T6-T8; n = 6). However, we found no differences in baseline cardiovascular function or time-trial performance between high- and low-thoracic SCI; hence, we grouped all thoracic SCI together. Next, we stratified the cervical and thoracic SCI groups into autonomic complete (cervical SCI n = 7, thoracic SCI n = 3) and autonomic incomplete based on the palmar SSR response to median nerve stimulation.
Statistics Between-group differences were assessed using a two-way analysis of variance with one factor for lesion-level and one factor for autonomic completeness of injury. Tukey corrected post-hoc comparisons were conducted as appropriate. Between-group differences for categorical dependent variables (i.e., AIS grade/selfreport AD) were assessed using a Pearson’s chi-squared analyses. If our stratification resulted in a group with less than three athletes, then no statistical analyses were conducted. Associations between continuous outcome measures were assessed using Pearson product-moment correlation coefficient. All analyses were conducted using Stata v10 (StataCorp, College Station, Texas, USA). Alpha was set at P < 0.05.
Results Effect of level of injury on baseline demographics and cardiovascular function Age, stature, and body mass were similar between cervical and thoracic SCI. Self-report AD was more frequent in cervical vs thoracic SCI (n = 8 vs n = 4, P = 0.027). Upper limb motor score was significantly lower in cervical vs thoracic SCI (P = 0.045). There was no difference in the prevalence of neurologically complete/incomplete injury between groups. There were no significant differences in supine SBP or DBP between groups (Table 1). Seated SBP, however, was lower in cervical SCI (P = 0.0093). Raw SSR score was not different between groups. Only three individuals had clinically defined OH, of which all had a cervical SCI.
different in cervical vs thoracic (P = 0.082: Fig. 1(c)), but average HR was lower in cervical SCI (P = 0.0073: Fig. 1(e)). Effect of level and autonomic completeness of injury on baseline cardiovascular function When athletes with cervical or thoracic SCI were further stratified into autonomic complete and incomplete, there were still no between-group differences in age, mass or stature. Prevalence of self-reported AD was higher in autonomic complete cervical SCI (P = 0.038), while seated SBP was lower in autonomic complete cervical SCI vs all other groups (P = 0.031). Effect of level and autonomic completeness of injury on exercise performance For cervical SCI, the four athletes who had an autonomic incomplete SCI finished in the top four positions during the H1 time-trial event; Thus, there was a significant interaction effect for level and autonomic completeness of injury (P = 0.049), whereby time-trial time was significantly faster in autonomic incomplete vs complete cervical SCI (P = 0.029), but was not different between autonomic complete and incomplete thoracic SCI (Figs 2 and 3). Similarly, there was a significant interaction effect between level and autonomic completeness of injury for average speed (P = 0.041), whereby average speed was significantly faster in cervical autonomic incomplete vs cervical autonomic complete athletes (P = 0.040), but not different between autonomic incomplete and complete thoracic SCI athletes. Although we had an insufficient number of athletes with cervical SCI who were also assessed for HR data to statistically assess between-group differences (n = 2 cervical incomplete, n = 5 cervical complete), we did anecdotally observe that cervical autonomic incomplete athletes exhibited higher maximal (190 ± 3 vs 167 ± 8 bpm) and average HRs (174 ± 2 vs 146 ± 7 bpm) than cervical autonomic complete athletes. For cervical SCI, there were positive associations between maximum HR and time-trial time (r2 = 0.66, P = 0.051, n = 7). One athlete with an autonomic complete cervical SCI exhibited an unexpectedly high maximum HR (186 bpm), but a considerably lower average HR (147 bpm). For thoracic SCI, there were no significant differences in HR or speed indices between those with autonomic complete and incomplete injuries. Discussion
Effect of level of injury on exercise performance Time-trial time was faster in thoracic vs cervical SCI (P = 0.0002; Fig. 1(a)). In the athletes assessed for race profiles via GPS and HR, we found that mean and minimum speed were faster in thoracic vs cervical SCI (P < 0.001; Fig. 1(d & f)). Maximum HR was not
This is the first study to demonstrate that endurance performance in SCI is critically dependent on not only the level of injury, but also on the extent of disruption to descending autonomic pathways. Within the H1 class (i.e., cervical SCI), athletes with an autonomic incomplete cervical SCI exhibit a faster time-trial performance,
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4 122 ± 9 65 ± 7 60 ± 10 122 ± 11* 64 ± 6 69 ± 10 0±7 −1 ± 5 9±6 2.5 ± 1.7 3/12 0/12
1.5 ± 1.9 7/11 3/11
12 0
40.7 ± 7.5 1.80 ± 0.07 67 ± 5 49 ± 6*
114 ± 11 64 ± 7 57 ± 6 107 ± 15 60 ± 11 74 ± 8 −7 ± 9 −4 ± 5 17 ± 7
9 2
40.7 ± 8.1 1.77 ± 0.06 66 ± 11 39 ± 13
T1-T8 (n = 12)
0.1 ± 0.4 N/A 2/7
112 ± 10 64 ± 9 56 ± 7 107 ± 17 61 ± 12 72 ± 7 −6 ± 9 −3 ± 5 16 ± 6
6 1
43.1 ± 7.6 1.78 ± 0.06 67 ± 8 37 ± 14
C4-C7 autonomic complete (n = 7)
3.5 ± 1.3†‡ N/A 1/4
118 ± 10 64 ± 3 60 ± 5 110 ± 11 59 ± 6 79 ± 11 −9 ± 8 −5 ± 5 19 ± 8
3 1
35.7 ± 8.0 1.75 ± 0.05 63 ± 8 44 ± 5
C4-C7 autonomic incomplete (n = 4)
0.2 ± 0.5 N/A 0/3
117 ± 15 65 ± 11 50 ± 1 125 ± 14 65 ± 8 68 ± 3 7 ± 10 0±5 8±4
3 0
47.6 ± 7.3 1.81 ± 0.03 67 ± 8 49 ± 1
T1-T8 autonomic complete (n = 3)
3.6 ± 0.9†‡ N/A 0/9
124 ± 8 66 ± 5 64 ± 11 124 ± 7† 65 ± 5 72 ± 9 −1 ± 4 −1 ± 6 8±7
9 0
38.7 ± 6.2 1.80 ± 0.07 67 ± 6 50 ± 0†
T1-T8 autonomic incomplete (n = 9)
*P < 0.05 vs C4-C7. † P < 0.05 vs C4-C7 autonomic complete. ‡ P < 0.05 vs T1-T8 autonomic complete. AIS, American Spinal Injuries Association Impairment Scale; “Autonomic complete”, number of participants with an absent palmar SSR response (SSR score of 0 or 1); DBP, diastolic blood pressure; “Delta”, change in blood pressure/heart rate in response to sit-up; HR, heart rate; “Orthostatic hypotension”, number of participants who demonstrated a drop in SBP of 20 mmHg or a drop in DBP of 10 mmHg or greater in response to sit-up; SBP, systolic blood pressure; SSR, sympathetic skin response as measured by the palmar response to median nerve stimulation, scored between 0 and 5; ULMS, upper limb motor score.
Demographics Age (year) Stature (m) Mass (kg) ULMS (/50) AIS grade AIS A (n) AIS B (n) Hemodynamics Supine SBP (mmHg) Supine DBP (mmHg) Supine HR (mmHg) Seated SBP (mmHg) Seated DBP (mmHg) Seated HR (mmHg) Delta SBP (mmHg) Delta DBP (mmHg) Delta HR (mmHg) Autonomic function SSR score (/5) Autonomic complete Orthostatic hypotension
C4-C7 (n = 11)
Table 1. Participant demographics and resting cardio-autonomic function
West et al.
Endurance performance in SCI
Fig. 1. Indices of endurance performance in athletes with cervical (circles) or thoracic SCI (squares). Note that thoracic SCI exhibited the fastest time-trial time (panel a) along with the highest average and minimum speeds (panels d, f). Maximal speed (panel b) and heart rate (HR; panel c) during the time trial were similar between groups. Average heart rate was significantly lower in cervical athletes (panel e). *P < 0.05.
higher average speed, and higher maximal and average HRs during competition than their autonomic complete cervical SCI counterparts. The relationship between autonomic integrity and endurance performance, however, does not hold for those in the H2 class (i.e., thoracic SCI). These data imply that elite athletes with autonomic incomplete cervical SCI are at a distinct endurance performance advantage during competition compared with their autonomic complete competitors. Resting cardiovascular and autonomic function In line with our previous research in paralympic athletes that compete in court-based sport (West et al., 2014b), we found that elite athletes with cervical SCI exhibit a reduced seated SBP compared with thoracic SCI.
Subsequent stratification by autonomic completeness revealed that seated SBP was only lower in cervical SCI individuals with an autonomic complete SCI. This finding confirms previous findings that autonomic completeness of SCI is a potent predictor of baseline hemodynamics (reviewed in West et al., 2013a). The incidence of OH in the current sample was markedly reduced compared with previous findings in SCI patients and court-based athletes (Claydon & Krassioukov, 2006; West et al., 2014b), which leads us to speculate that chronic endurance training may confer a protective effect against OH after SCI. Specifically, we postulate that an exercise-induced increase in blood volume (Houtman et al., 2000) and/or alterations in peripheral vascular function (Thijssen et al., 2006) could explain the potential protective effect of endurance training on OH.
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Fig. 2. Indices of endurance performance in athletes with cervical (circles) or thoracic SCI (squares) stratified by autonomic completeness of injury (closed symbols = autonomic complete, open symbols = autonomic incomplete). Note that time-trial time along with average speed were significantly faster in those with autonomic complete cervical SCI vs autonomic incomplete cervical SCI (panels a, b, and d), Maximal and average heart rate also tended to be higher in those with autonomic complete cervical SCI vs autonomic incomplete cervical SCI (panels c and e). Minimum speed was similar between groups (panel f). *P < 0.05.
The incidence of autonomic complete injury was greatest in those with cervical SCI (n = 7/11) compared with thoracic SCI (n = 3/12). These incidence rates are almost identical to our previous observations in courtbased athletes with SCI (West et al., 2014b), but differ from the patient population where a higher proportion of cervical individuals are autonomic complete (Claydon & Krassioukov, 2006). Since the spinal sympathetic outflow exits at thoracic spinal segments, it appears counterintuitive that an individual with cervical SCI can exhibit preserved descending sympathetic control while an individual with thoracic SCI can exhibit a loss of descending sympathetic control. Level of injury, however, is determined via the AIS assessment, which examines only the integrity of the descending motor tracts (lateral and anterior corticospinal tract) and the ascending sensory tracts (anterior spinothalamic tract and dorsal columns; Kirshblum et al., 2011). The
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descending autonomic tracts on the other hand are primarily located in the dorsolateral funiculus; hence, the spatial organization of these intraspinal pathways is such that an SCI may damage one pathway but not the other (reviewed in West et al., 2013a). Thus, in agreement with our previous findings (West et al., 2014b), we found no relationship between autonomic completeness of injury and motor/sensory completeness of injury. Accordingly, we suggest that when an individual has a high-thoracic/ cervical SCI, an assessment of autonomic function should also be included as part of the medical/sports classification. Physiological responses during endurance exercise Using GPS technology combined with HR monitoring, we conducted the first assessment of the temporal and physiological responses to a Paracyling World
Endurance performance in SCI
Fig. 3. Example speed data collected during lap 2 of the Paracycling class 1 time-trial event for one athlete with autonomic complete SCI and one athlete with an autonomic incomplete SCI. Note that despite racing in the same class and exhibiting a similar lesion level, age, time since injury, and neurological completeness of injury, the athlete with autonomic incomplete SCI maintained a higher speed throughout the lap, specifically between the start/finish line and the third inlet, during which time the course was predominantly flat or uphill.
Championship time-trial event. Athletes with thoracic injuries were significantly faster than athletes with cervical injuries. This lesion-dependent response is most likely a reflection of the greater muscle mass used and subsequent increase in power output and aerobic exercise capacity in athletes with thoracic SCI vs athletes with cervical SCI (Wicks et al., 1983; Campbell et al., 2004). An interesting and noteworthy finding was that athletes with cervical SCI exhibit a similar maximum HR to that of thoracic SCI athletes. This is in contrast to almost all previous literature describing the HR response to exercise in the SCI population, whereby individuals with cervical injuries present with an attenuated HR response to exercise (Theisen, 2012). Since we have previously reported that maximum HR is critically dependent on the degree of sympathetic decentralization (West et al., 2013b), we believe the lack of between lesion-level difference in maximum HR is a reflection of our findings that four of the athletes with cervical SCI had an autonomic incomplete injury. The similar maximum HRs between cervical and thoracic SCI may also be a reflection of the time trial being conducted in the field rather than the lab. In this respect, we have previously shown that field-based testing evokes superior cardiovascular responses to laboratory-based testing, most likely because of elite athletes being more accustomed to field- than laboratory-based exercise and having the freedom to self-select their speed and push technique (West et al., 2013b). To establish the within lesion level, and therefore the within racing class, effect of autonomic completeness of injury on exercise responses and endurance
performance, we stratified athletes with the same level of injury by autonomic completeness. For cervical SCI, athletes with autonomic incomplete SCI outperformed their lesion-level matched autonomic complete counterparts, and exhibited superior physiological responses during exercise. We also found results indicative of a strong association between HRpeak and time-trial time in athletes with cervical SCI, confirming our previous findings in court-based athletes (West et al., 2013b). The cardiovascular response to exercise in (autonomic complete) cervical SCI is compromised by the loss of supraspinal control over the peripheral and splanchnic vasculature (Thijssen et al., 2009), a limited catecholaminergic response to exercise (Schmid et al., 1998), and reduced vasoconstrictor reserve below the injury (Groothuis et al., 2010). Together, these alterations in cardiovascular function conspire to impair venous return and stroke volume during exercise (Figoni et al., 1988). Accordingly, any exercise-induced increase in cardiac output is mediated entirely by increases in HR. In the face of such limitations, it is perhaps unsurprising that the ability to increase HR is a key determinant of endurance performance in cervical SCI athletes. Interestingly, by visualizing the GPS data, it became apparent that athletes with autonomic complete and incomplete cervical SCI were completing the downhill sections similarly (see Fig. 3 section between final inlet and finish); hence, top speeds were similar between autonomic complete and incomplete cervical SCI. When athletes were pushing on the uphill and flat sections of the course (see Fig. 3, sections between inlets 1, 2, and 3), however, the differences between autonomic complete and
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West et al. incomplete cervical SCI were much more apparent; hence, average speed was substantially faster in autonomic incomplete cervical SCI. We believe these findings reflect the greater dependence on the cardiorespiratory system during flat/uphill pushing vs downhill “cruising.” Together, these data demonstrate that athletes with autonomic incomplete cervical SCI are at a distinct advantage during endurance activities compared with their autonomic complete counterparts. The peak HR values obtained in the autonomic complete cervical SCI group were markedly higher than those typically reported in the literature. Interestingly, the group mean value of 169 bpm is remarkably similar to that reported by Schmid et al. (2001) during exercise in a dysreflexic state. AD, a condition defined by uncontrolled hypertension, can occur during exercise in SCI either intentionally (i.e., boosting) or non-intentionally due to some form of afferent stimuli, such as a full bladder (Krassioukov, 2012). This latter cause of AD may be particularly problematic in endurance events (such as the time trial) because of excessive fluid intake without micturition. Although a dysreflexic state has been shown to improve time-trial performance by 10% (Burnham et al., 1994), the associated uncontrolled hypertensive episodes can also lead to deleterious side effects such as dizziness, blurred vision and impaired cognition, and left untreated can lead to life threatening consequences, including, intracranial hemorrhage, retinal detachments, seizures, cardiac arrhythmias, and even death (Eltorai et al., 1992; Ho & Krassioukov, 2010). In the current study, we were unable to control for AD during the time trial; however, we did ask athletes to self-report if they boosted during the event. One autonomic complete cervical SCI athlete self-reported that he boosted during the competition; hence, this may go some way to explaining the high HRs in this group. An alternative explanation for the high peak HR in autonomic complete cervical SCI may relate to an increased activation of cardiac β-receptors secondary to an exerciseinduced increase in systemic norepinephrine. In this regard, it has been reported that tetraplegics exhibit an exercise-induced increase in norepinephrine during exercise (Schmid et al., 1998), presumably a result of spill over into the systemic circulation from tonically active post-ganglionic sympathetic nerve endings. Although we made no measures of catecholamines during exercise in the current study, we think it unlikely that the high HRs obtained in our autonomic complete cervical SCI athletes were reflective of hormonal activation since the athletes all reached high HRs rapidly (i.e., within 30–60 s of the onset of exercise). In contrast to cervical SCI, we found no differences in endurance performance between autonomic complete and incomplete thoracic SCI, suggesting that the cardiovascular system may not limit performance to the same extent as in cervical SCI. This is in agreement with previous studies that have reported compression of the
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peripheral/splanchnic vasculature via an anti-gravity suit or an abdominal binder enhances exercise capacity/ endurance performance in cervical SCI (Pitetti et al., 1994; West et al., 2014a) but not in thoracic SCI (Hopman et al., 1993; Kerk et al., 1995). Improved exercise capacity of tetraplegics in response to a mechanically stimulated central translocation of peripheral blood volume implies that the limitation to exercise performance is likely more “central,” whereas the lack of improvement in paraplegics implies the limitation to exercise is not “central.” Thus, factors other than the degree of remaining autonomic cardiovascular control are likely to moderate endurance performance in athletes with a thoracic SCI. In conclusion, this is the first study to demonstrate that endurance performance in cervical SCI is critically dependent on not only the level of injury, but also on the extent of disruption to descending autonomic pathways. Athletes with autonomic incomplete cervical SCI exhibit a greater degree of exercise-induced cardiac chronotropy and enhanced endurance performance compared with autonomic complete cervical SCI. This finding has implications for sport classification since the current system accounts only for differences in level of injury rather than for differences in autonomic integrity. Together, these findings further demonstrate that autonomic function should be included into the classification of athletes with cervical SCI, especially in sports that involve a large cardiovascular demand. Perspectives While several studies have investigated the relationship between autonomic completeness of injury and cardiovascular function at rest and during exercise in athletes with SCI (West et al., 2013b, 2014b), no study has specifically examined the relationship between autonomic completeness of injury and endurance performance in the SCI population. We assessed 23 elite paracyclists with SCI at the 2013 Paracycling World Championships for resting cardio-autonomic function and time to complete a 17.3-km time-trial event. We found that athletes with cervical SCI who were autonomic incomplete exhibited superior time-trial performance and enhanced cardiovascular responses during exercise compared with their autonomic complete cervical SCI counterparts. The novel data collected here emphasize that the presence of descending sympathetic control is critical to elicit the appropriate hemodynamic responses to exercise in cervical SCI, and by extension to match oxygen delivery to demand. When descending sympathetic control is absent, impaired vaso- and sudo-motor function along with reduced cardiac chronotropy and inotropy conspire to curtail endurance performance. The relationship between autonomic integrity and endurance performance, however, does not hold for those with thoracic SCI suggesting that other as yet unidentified
Endurance performance in SCI mechanisms are more important for endurance performance in this sub-population. These data imply that elite athletes with autonomic incomplete cervical SCI are at a distinct endurance performance advantage during competition compared with their autonomic complete competitors. We propose, therefore, that autonomic testing should be incorporated into the classification of athletes with cervical SCI, particularly in sports with a large endurance component. Key words: Tetraplegia, paracycling, blood pressure.
paraplegia,
exercise,
Acknowledgements Data for this study was collected during the 2013 Paracycling World Championship. The authors would like to thank all paracyclists who took part in this study and the Union Cycliste Internationale for allowing the study to take place during the 2013 Paracycling World Championship. GPS devices were provided by the Centre for Hip Health and Mobility, University of British Columbia. Dr. C West is funded by a Craig Neilsen and Michael Smith Foundation for Health Research Postdoctoral Fellowship. Research in the laboratory of Dr. Krassioukov is funded by the Canadian Institute for Health research and the Craig Neilsen Foundation.
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during exercise at the same VO2. Adapt Phys Act Q 1988: 5: 130–139. Garshick E, Kelley A, Cohen SA, Garrison A, Tun CG, Gagnon D, Brown R. A prospective assessment of mortality in chronic spinal cord injury. Spinal Cord 2005: 43: 408–416. Groothuis JT, Rongen GA, Geurts AC, Smits P, Hopman MT. Effect of different sympathetic stimuli-autonomic dysreflexia and head-up tilt-on leg vascular resistance in spinal cord injury. Arch Phys Med Rehabil 2010: 91: 1930–1935. Haisma JA, van der Woude LH, Stam HJ, Bergen MP, Sluis TA, Bussmann JB. Physical capacity in wheelchairdependent persons with a spinal cord injury: a critical review of the literature. Spinal Cord 2006: 44: 642–652. Ho CP, Krassioukov AV. Autonomic dysreflexia and myocardial ischemia. Spinal Cord 2010: 48: 714–715. Hopman MT, Kamerbeek IC, Pistorius M, Binkhorst RA. The effect of an anti-G suit on the maximal performance of individuals with paraplegia. Int J Sports Med 1993: 14: 357–361. Houtman S, Oeseburg B, Hopman MT. Blood volume and hemoglobin after spinal cord injury. Am J Phys Med Rehabil 2000: 79: 260–265. Kerk JK, Clifford PS, Snyder AC, Prieto TE, O’Hagan KP, Schot PK, Myklebust JB, Myklebust BM. Effect of an abdominal binder during wheelchair exercise. Med Sci Sports Exerc 1995: 27: 913–919. Kirshblum SC, Burns SP, Biering-Sorensen F, Donovan W, Graves DE, Jha A, Johansen M, Jones L, Krassioukov A, Mulcahey MJ, Schmidt-Read M, Waring W. International standards for neurological classification of spinal cord injury (revised 2011). J Spinal Cord Med 2011: 34: 535–546. Krassioukov A. Autonomic dysreflexia: current evidence related to unstable
arterial blood pressure control among athletes with spinal cord injury. Clin J Sport Med 2012: 22: 39–45. Krassioukov A, Biering-Sorensen F, Donovan W, Kennelly M, Kirshblum S, Krogh K, Alexander MS, Vogel L, Wecht J. International standards to document remaining autonomic function after spinal cord injury. J Spinal Cord Med 2012: 35: 201–210. Kucera P, Goldenberg Z, Kurca E. Sympathetic skin response: review of the method and its clinical use. Bratisl Lek Listy 2004: 105: 108–116. Pitetti KH, Barrett PJ, Campbell KD, Malzahn DE. The effect of lower body positive pressure on the exercise capacity of individuals with spinal cord injury. Med Sci Sports Exerc 1994: 26: 463–468. Previnaire JG, Soler JM, Leclercq V, Denys P. Severity of autonomic dysfunction in patients with complete spinal cord injury. Clin Auton Res 2012: 22: 9–15. Sahota IS, Ravensbergen HR, McGrath MS, Claydon VE. Cerebrovascular responses to orthostatic stress after spinal cord injury. J Neurotrauma 2012: 29: 2446–2456. Schmid A, Huonker M, Barturen JM, Stahl F, Schmidt-Trucksass A, Konig D, Grathwohl D, Lehmann M, Keul J. Catecholamines, heart rate, and oxygen uptake during exercise in persons with spinal cord injury. J Appl Physiol 1998: 85: 635–641. Schmid A, Schmidt-Trucksass A, Huonker M, Konig D, Eisenbarth I, Sauerwein H, Brunner C, Storch MJ, Lehmann M, Keul J. Catecholamines response of high performance wheelchair athletes at rest and during exercise with autonomic dysreflexia. Int J Sports Med 2001: 22: 2–7. Taylor BJ, West CR, Romer LM. No effect of arm-crank exercise on diaphragmatic fatigue or ventilatory
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Thijssen DH, Steendijk S, Hopman MT. Blood redistribution during exercise in subjects with spinal cord injury and controls. Med Sci Sports Exerc 2009: 41: 1249–1254. Vetrugno R, Liguori R, Cortelli P, Montagna P. Sympathetic skin response: basic mechanisms and clinical applications. Clin Auton Res 2003: 13: 256–270. West CR, Bellantoni A, Krassioukov AV. Cardiovascular function in individuals with incomplete spinal cord injury: a systematic review. Top Spinal Cord Inj Rehabil 2013a: 19: 267–278. West CR, Romer LM, Krassioukov A. Autonomic function and exercise performance in elite athletes with cervical spinal cord injury.
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© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Cardiovascular control, autonomic function, and elite endurance performance in spinal cord injury C. R. West1, C. M. Gee1, C. Voss2, M. Hubli1, K. D. Currie1, J. Schmid3, A. V. Krassioukov1,4,5 1
International Collaboration on Repair Discoveries (ICORD), Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada, 2Centre for Hip Health and Mobility, Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada, 3Paracycling Classification, International Cycling Union, Aigle, Switzerland, 4Division of Physical Medicine and Rehabilitation, Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada, 5GF Strong Rehabilitation Centre, Vancouver Health Authority, Vancouver, British Columbia, Canada Corresponding author: Andrei Krassioukov, MD, PhD, FRCPC, ICORD-BSCC, UBC, 818 West 10th Avenue, Vancouver, BC V5Z 1M9, Canada. Tel: 1 604 675 8819, Fax: 1 604 675 8820, E-mail: [email protected] Accepted for publication 17 July 2014
We aimed to determine the relationship between level of injury, completeness of injury, resting as well as exercise hemodynamics, and endurance performance in athletes with spinal cord injury (SCI). Twenty-three elite male paracycling athletes (C3-T8) were assessed for neurological level/completeness of injury, autonomic completeness of injury, resting cardiovascular function, and time to complete a 17.3-km World Championship time-trial test. A subset were also fitted with heart rate (HR) monitors and their cycles were fitted with a global positioning systems device (n = 15). Thoracic SCI exhibited higher seated systolic blood pressure along with superior timetrial performance compared with cervical SCI (all
P < 0.01). When further stratified by autonomic completeness of injury, the four athletes with cervical autonomic incomplete SCI exhibited a faster time-trial time and a higher average speed compared with cervical autonomic complete SCI (all P < 0.042). Maximum and average HR also tended to be higher in cervical autonomic incomplete vs autonomic complete. There were no differences in time-trial time, HR, or speed between thoracic autonomic complete vs incomplete SCI. In conclusion, autonomic completeness of injury and the consequent ability of the cardiovascular system to respond to exercise appear to be a critical determinant of endurance performance in elite athletes with cervical SCI.
Individuals with spinal cord injury (SCI) exhibit secondary complications that extend far beyond paralysis. Some of the most devastating side effects of SCI relate to impaired cardiovascular function, which increases cardiovascular disease risk (Garshick et al., 2005; Cragg et al., 2013). The extent of cardiovascular dysfunction is known to be level dependent, whereby those with the most rostral injuries exhibit the most severe impairment in cardiorespiratory function and exercise capacity (Haisma et al., 2006; Taylor et al., 2010). Reduced exercise capacity in cervical SCI is attributed to impaired motor function, loss of the sub-lesional venous muscle pump, reduced blood volume, and a decentralized sympathetic nervous system, which alters vascular tone and ultimately reduces stroke volume, cardiac output and oxygen delivery (Houtman et al., 2000; Teasell et al., 2000; Theisen, 2012). Autonomic completeness of injury (i.e., integrity of descending spinal autonomic pathways) also provides independent predictive value for resting cardiovascular function in cervical SCI (West et al., 2014b). We and others have found a relatively high proportion of
individuals with cervical SCI exhibit sparing of descending autonomic fibers (Claydon & Krassioukov, 2006; Sahota et al., 2012; West et al., 2014b). It is plausible that such sparing may circumvent the “traditional” limitations that are thought to occur because of decentralized sympathetic circuits in cervical SCI. To this end, we recently reported that the group mean maximum heart rate (HR) of elite wheelchair rugby athletes with cervical SCI exceeded 150 bpm, and that the HR achieved was strongly correlated to the degree of disruption to spinal autonomic pathways (West et al., 2013b). Such exerciseinduced tachycardia would be expected to confer multiple advantages during exercise, such as an enhancement of cardiac output and endurance performance. This advantage is anticipated to be most pronounced in exercise modalities that are heavily dependent on aerobic exercise capacity, such as long-distance wheelchair racing and/or paracycling. Conversely, it has been reported that individuals with a high-thoracic SCI (i.e., T1-T3) may sustain complete injury to the descending spinal autonomic pathways, yet spare the motor/sensory pathways (Claydon & Krassioukov, 2006). Such instances are also expected to compromise vaso- and
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West et al. sudo-motor function to a similar degree that occurs in autonomic complete cervical SCI. To examine the complex relationships between lesion level, neurological completeness of injury, autonomic completeness of injury, and endurance performance, we conducted a comprehensive assessment of resting cardio-autonomic function and endurance performance in 23 male athletes with SCI during the time-trial event of the 2013 Paracycling World Championships. We hypothesized that athletes with thoracic SCI would exhibit superior resting cardiovascular function and time-trial performance compared with athletes with cervical SCI. We also hypothesized that autonomic incomplete cervical/high-thoracic SCI would outperform their lesion-level matched autonomic complete counterparts. Methods Participants All protocols were approved by the institutional ethics committee and endorsed by the International Paralympic Committee, and all athletes provided written informed consent. We conducted all assessments during the 2013 Paracycling World Championships (Baie Comeau, Canada). We tested 11 of 12 competing athletes in the male H1 class (cervical SCI), and 12 of 17 competing athletes in the male H2 class (thoracic SCI), for a total of 23 athletes. Thus, our sample represented 80% of the top SCI paracyclists in the world. None of the athletes smoked or had a history of cardiopulmonary disease. Athletes presented with a traumatic SCI between C5 and T8 (age 41 ± 8 years, time since injury 17 ± 7 years). Self-reported stature and mass were 1.79 ± 0.12 m and 66 ± 8 kg, respectively. Athletes self-reported to train for an average of 14 h/ week (range 5–32 h/week).
Methods of measurement Neurological classification and questionnaires We conducted a neurological classification in accordance with the International Standards for the Neurological Classification of SCI to determine the American Spinal Injuries Association Impairment Scale (AIS) grade (Kirshblum et al., 2011). We also administered the revised International Standards to document remaining autonomic function after SCI (Krassioukov et al., 2012). Athletes selfadministered a demographics and general autonomic function questionnaire. Among other questions, the athletes were specifically asked; “do you have any episodes of autonomic dysreflexia (AD), a condition where your blood pressure rises very fast, usually resulting in symptoms such as severe headache, sweating, excessive spasms, hot/cold flushes, and nasal congestion”.
Cardiovascular assessment We used a one lead electrocardiogram and finometer (Finometer, Finapres Medical Systems BV, Arnhem, the Netherlands) for the beat-by-beat assessment of HR and blood pressure (BP, respectively. An automated BP cuff (Dinamap, General Electric Pro 300V2; Tampa, Florida, USA) was also fitted over the brachial artery and inflated every minute to calibrate the finometer. Resting systolic and diastolic BP as well as HR were recorded for 10 min during supine rest using an analog-to-digital converter (Powerlab/ 16SP model ML795; ADInstruments, Colorado Springs, Colorado, USA) interfaced with a computer. Next, we assessed BP and HR during a 10-min sit-up test; briefly, we moved participants to
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an upright seated position with their legs hanging off the side of the bed at 90 degrees. This sit-up position mimics that experienced while seated in a wheelchair, except the lower legs and feet are unsupported. We informed participants as to the importance of this procedure being passive and instructed them to not assist in the “sit-up” procedure. We defined orthostatic hypotension (OH) as a ≥ 20 mmHg drop in systolic BP (SBP) or a ≥ 10 mmHg drop in diastolic BP (DBP) within 3 min of assuming an upright position (Consensus Committee of the American Autonomic Society and the American Academy of Neurology, 1996). We terminated the test early if the participant exhibited signs/symptoms of presyncope or on athlete request.
Sympathetic skin responses (SSRs) Following 10 min of supine rest, we assessed athletes for SSRs to median nerve stimulation at the wrist. The SSR assessment records a change in skin conductance after activation of sweat glands in response to various stimuli (Cariga et al., 2002; Vetrugno et al., 2003). The SSR tests sudomotor function, but has previously been shown to correlate well with the phase 4 overshoot during Valsalva (Previnaire et al., 2012), suggesting it acts as a proxy for assessing the integrity of descending autonomic (vasomotor) pathways. We conducted the SSR protocol as previously described in our laboratory (Claydon & Krassioukov, 2006; West et al., 2013b, 2014b). Briefly, we simultaneously recorded bilateral plantar and palmar SSRs over a 10-s period at a band pass of 3 Hz to 3 kHz, using a Dantec Keypoint® 4 system (Natus Medical Incorporated, San Carlos, California, USA). To minimize the well-known habituation of these responses, we applied the stimuli in random order and with variable time delays (minimum delay 90 s; Cariga et al., 2001). Five recordings in response to median nerve stimulation (0.2-ms duration, 10–20 mA intensity) were obtained at each site. We deemed an SSR present when there was a clear positive deflection from baseline (Kucera et al., 2004). For analyses, we only assessed the number of present palmar SSRs, since these responses are controlled by sympathetic pre- and post-ganglionic fibres that exit the spinal cord at a similar level to those that innervate the heart (i.e., T1-T5). We excluded any potential that coincided with muscle spasm, limb movement, or cough. Left and right palmar responses were summed and divided by two such that an average number of responses were calculated. Based on our previous findings that even minimal sparing of descending sympathetic fibers confers cardiovascular benefits (West et al., 2014b), we defined individuals as autonomic complete if they had 0 or 1 SSRs, and autonomic incomplete if they had between 2 and 5 SSRs.
Exercise responses We assessed time to complete the 17.3-km time-trial event (two laps of the same course) during the 2013 Paracycling World Championships. Athletes raced in their respective paracycling class as determined during a separate classification that was conducted by the Union Cycliste Internationale. Class H1 raced in the early afternoon and class H2 raced in the late afternoon. Within their respective classes, athletes started the course in 1-min intervals. We obtained the athletes’ official time-trial times, measured to the nearest millisecond, for analyses. Additionally, 1 h prior to the race, we fitted HR monitors to a subset (n = 15) of the athletes (Polar team System 2.0, Polar Electro Oy, Kempele, Finland) and instrumented the racing cycle of a subset of athletes (n = 15) with a Global Positioning System (GPS) device (QStarz Q100XT, Qstarz International Co., Ltd., Taipei, Taiwan). The GPS device was configured to log the following variables second by second: date and time, geographic coordinates (latitude and longitude), speed (km/h), distance (m), and elevation (m). Physiologic and
Endurance performance in SCI performance characteristics (speed) throughout the race were mapped and analyzed using Geographic Information Systems Software (ArcGIS v.10.1; Esri, Redlands, California, USA). Peak HR (HRpeak) and peak speed was defined as the highest value averaged over a rolling 30-s epoch.
Data analyses We carried out two levels of analyses to examine the effect of injury level and autonomic completeness of injury on resting cardiovascular function and exercise performance. First, we compared cervical SCI (n = 11), high-thoracic SCI (T1-T5; n = 6) and low-thoracic SCI (T6-T8; n = 6). However, we found no differences in baseline cardiovascular function or time-trial performance between high- and low-thoracic SCI; hence, we grouped all thoracic SCI together. Next, we stratified the cervical and thoracic SCI groups into autonomic complete (cervical SCI n = 7, thoracic SCI n = 3) and autonomic incomplete based on the palmar SSR response to median nerve stimulation.
Statistics Between-group differences were assessed using a two-way analysis of variance with one factor for lesion-level and one factor for autonomic completeness of injury. Tukey corrected post-hoc comparisons were conducted as appropriate. Between-group differences for categorical dependent variables (i.e., AIS grade/selfreport AD) were assessed using a Pearson’s chi-squared analyses. If our stratification resulted in a group with less than three athletes, then no statistical analyses were conducted. Associations between continuous outcome measures were assessed using Pearson product-moment correlation coefficient. All analyses were conducted using Stata v10 (StataCorp, College Station, Texas, USA). Alpha was set at P < 0.05.
Results Effect of level of injury on baseline demographics and cardiovascular function Age, stature, and body mass were similar between cervical and thoracic SCI. Self-report AD was more frequent in cervical vs thoracic SCI (n = 8 vs n = 4, P = 0.027). Upper limb motor score was significantly lower in cervical vs thoracic SCI (P = 0.045). There was no difference in the prevalence of neurologically complete/incomplete injury between groups. There were no significant differences in supine SBP or DBP between groups (Table 1). Seated SBP, however, was lower in cervical SCI (P = 0.0093). Raw SSR score was not different between groups. Only three individuals had clinically defined OH, of which all had a cervical SCI.
different in cervical vs thoracic (P = 0.082: Fig. 1(c)), but average HR was lower in cervical SCI (P = 0.0073: Fig. 1(e)). Effect of level and autonomic completeness of injury on baseline cardiovascular function When athletes with cervical or thoracic SCI were further stratified into autonomic complete and incomplete, there were still no between-group differences in age, mass or stature. Prevalence of self-reported AD was higher in autonomic complete cervical SCI (P = 0.038), while seated SBP was lower in autonomic complete cervical SCI vs all other groups (P = 0.031). Effect of level and autonomic completeness of injury on exercise performance For cervical SCI, the four athletes who had an autonomic incomplete SCI finished in the top four positions during the H1 time-trial event; Thus, there was a significant interaction effect for level and autonomic completeness of injury (P = 0.049), whereby time-trial time was significantly faster in autonomic incomplete vs complete cervical SCI (P = 0.029), but was not different between autonomic complete and incomplete thoracic SCI (Figs 2 and 3). Similarly, there was a significant interaction effect between level and autonomic completeness of injury for average speed (P = 0.041), whereby average speed was significantly faster in cervical autonomic incomplete vs cervical autonomic complete athletes (P = 0.040), but not different between autonomic incomplete and complete thoracic SCI athletes. Although we had an insufficient number of athletes with cervical SCI who were also assessed for HR data to statistically assess between-group differences (n = 2 cervical incomplete, n = 5 cervical complete), we did anecdotally observe that cervical autonomic incomplete athletes exhibited higher maximal (190 ± 3 vs 167 ± 8 bpm) and average HRs (174 ± 2 vs 146 ± 7 bpm) than cervical autonomic complete athletes. For cervical SCI, there were positive associations between maximum HR and time-trial time (r2 = 0.66, P = 0.051, n = 7). One athlete with an autonomic complete cervical SCI exhibited an unexpectedly high maximum HR (186 bpm), but a considerably lower average HR (147 bpm). For thoracic SCI, there were no significant differences in HR or speed indices between those with autonomic complete and incomplete injuries. Discussion
Effect of level of injury on exercise performance Time-trial time was faster in thoracic vs cervical SCI (P = 0.0002; Fig. 1(a)). In the athletes assessed for race profiles via GPS and HR, we found that mean and minimum speed were faster in thoracic vs cervical SCI (P < 0.001; Fig. 1(d & f)). Maximum HR was not
This is the first study to demonstrate that endurance performance in SCI is critically dependent on not only the level of injury, but also on the extent of disruption to descending autonomic pathways. Within the H1 class (i.e., cervical SCI), athletes with an autonomic incomplete cervical SCI exhibit a faster time-trial performance,
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4 122 ± 9 65 ± 7 60 ± 10 122 ± 11* 64 ± 6 69 ± 10 0±7 −1 ± 5 9±6 2.5 ± 1.7 3/12 0/12
1.5 ± 1.9 7/11 3/11
12 0
40.7 ± 7.5 1.80 ± 0.07 67 ± 5 49 ± 6*
114 ± 11 64 ± 7 57 ± 6 107 ± 15 60 ± 11 74 ± 8 −7 ± 9 −4 ± 5 17 ± 7
9 2
40.7 ± 8.1 1.77 ± 0.06 66 ± 11 39 ± 13
T1-T8 (n = 12)
0.1 ± 0.4 N/A 2/7
112 ± 10 64 ± 9 56 ± 7 107 ± 17 61 ± 12 72 ± 7 −6 ± 9 −3 ± 5 16 ± 6
6 1
43.1 ± 7.6 1.78 ± 0.06 67 ± 8 37 ± 14
C4-C7 autonomic complete (n = 7)
3.5 ± 1.3†‡ N/A 1/4
118 ± 10 64 ± 3 60 ± 5 110 ± 11 59 ± 6 79 ± 11 −9 ± 8 −5 ± 5 19 ± 8
3 1
35.7 ± 8.0 1.75 ± 0.05 63 ± 8 44 ± 5
C4-C7 autonomic incomplete (n = 4)
0.2 ± 0.5 N/A 0/3
117 ± 15 65 ± 11 50 ± 1 125 ± 14 65 ± 8 68 ± 3 7 ± 10 0±5 8±4
3 0
47.6 ± 7.3 1.81 ± 0.03 67 ± 8 49 ± 1
T1-T8 autonomic complete (n = 3)
3.6 ± 0.9†‡ N/A 0/9
124 ± 8 66 ± 5 64 ± 11 124 ± 7† 65 ± 5 72 ± 9 −1 ± 4 −1 ± 6 8±7
9 0
38.7 ± 6.2 1.80 ± 0.07 67 ± 6 50 ± 0†
T1-T8 autonomic incomplete (n = 9)
*P < 0.05 vs C4-C7. † P < 0.05 vs C4-C7 autonomic complete. ‡ P < 0.05 vs T1-T8 autonomic complete. AIS, American Spinal Injuries Association Impairment Scale; “Autonomic complete”, number of participants with an absent palmar SSR response (SSR score of 0 or 1); DBP, diastolic blood pressure; “Delta”, change in blood pressure/heart rate in response to sit-up; HR, heart rate; “Orthostatic hypotension”, number of participants who demonstrated a drop in SBP of 20 mmHg or a drop in DBP of 10 mmHg or greater in response to sit-up; SBP, systolic blood pressure; SSR, sympathetic skin response as measured by the palmar response to median nerve stimulation, scored between 0 and 5; ULMS, upper limb motor score.
Demographics Age (year) Stature (m) Mass (kg) ULMS (/50) AIS grade AIS A (n) AIS B (n) Hemodynamics Supine SBP (mmHg) Supine DBP (mmHg) Supine HR (mmHg) Seated SBP (mmHg) Seated DBP (mmHg) Seated HR (mmHg) Delta SBP (mmHg) Delta DBP (mmHg) Delta HR (mmHg) Autonomic function SSR score (/5) Autonomic complete Orthostatic hypotension
C4-C7 (n = 11)
Table 1. Participant demographics and resting cardio-autonomic function
West et al.
Endurance performance in SCI
Fig. 1. Indices of endurance performance in athletes with cervical (circles) or thoracic SCI (squares). Note that thoracic SCI exhibited the fastest time-trial time (panel a) along with the highest average and minimum speeds (panels d, f). Maximal speed (panel b) and heart rate (HR; panel c) during the time trial were similar between groups. Average heart rate was significantly lower in cervical athletes (panel e). *P < 0.05.
higher average speed, and higher maximal and average HRs during competition than their autonomic complete cervical SCI counterparts. The relationship between autonomic integrity and endurance performance, however, does not hold for those in the H2 class (i.e., thoracic SCI). These data imply that elite athletes with autonomic incomplete cervical SCI are at a distinct endurance performance advantage during competition compared with their autonomic complete competitors. Resting cardiovascular and autonomic function In line with our previous research in paralympic athletes that compete in court-based sport (West et al., 2014b), we found that elite athletes with cervical SCI exhibit a reduced seated SBP compared with thoracic SCI.
Subsequent stratification by autonomic completeness revealed that seated SBP was only lower in cervical SCI individuals with an autonomic complete SCI. This finding confirms previous findings that autonomic completeness of SCI is a potent predictor of baseline hemodynamics (reviewed in West et al., 2013a). The incidence of OH in the current sample was markedly reduced compared with previous findings in SCI patients and court-based athletes (Claydon & Krassioukov, 2006; West et al., 2014b), which leads us to speculate that chronic endurance training may confer a protective effect against OH after SCI. Specifically, we postulate that an exercise-induced increase in blood volume (Houtman et al., 2000) and/or alterations in peripheral vascular function (Thijssen et al., 2006) could explain the potential protective effect of endurance training on OH.
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West et al.
Fig. 2. Indices of endurance performance in athletes with cervical (circles) or thoracic SCI (squares) stratified by autonomic completeness of injury (closed symbols = autonomic complete, open symbols = autonomic incomplete). Note that time-trial time along with average speed were significantly faster in those with autonomic complete cervical SCI vs autonomic incomplete cervical SCI (panels a, b, and d), Maximal and average heart rate also tended to be higher in those with autonomic complete cervical SCI vs autonomic incomplete cervical SCI (panels c and e). Minimum speed was similar between groups (panel f). *P < 0.05.
The incidence of autonomic complete injury was greatest in those with cervical SCI (n = 7/11) compared with thoracic SCI (n = 3/12). These incidence rates are almost identical to our previous observations in courtbased athletes with SCI (West et al., 2014b), but differ from the patient population where a higher proportion of cervical individuals are autonomic complete (Claydon & Krassioukov, 2006). Since the spinal sympathetic outflow exits at thoracic spinal segments, it appears counterintuitive that an individual with cervical SCI can exhibit preserved descending sympathetic control while an individual with thoracic SCI can exhibit a loss of descending sympathetic control. Level of injury, however, is determined via the AIS assessment, which examines only the integrity of the descending motor tracts (lateral and anterior corticospinal tract) and the ascending sensory tracts (anterior spinothalamic tract and dorsal columns; Kirshblum et al., 2011). The
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descending autonomic tracts on the other hand are primarily located in the dorsolateral funiculus; hence, the spatial organization of these intraspinal pathways is such that an SCI may damage one pathway but not the other (reviewed in West et al., 2013a). Thus, in agreement with our previous findings (West et al., 2014b), we found no relationship between autonomic completeness of injury and motor/sensory completeness of injury. Accordingly, we suggest that when an individual has a high-thoracic/ cervical SCI, an assessment of autonomic function should also be included as part of the medical/sports classification. Physiological responses during endurance exercise Using GPS technology combined with HR monitoring, we conducted the first assessment of the temporal and physiological responses to a Paracyling World
Endurance performance in SCI
Fig. 3. Example speed data collected during lap 2 of the Paracycling class 1 time-trial event for one athlete with autonomic complete SCI and one athlete with an autonomic incomplete SCI. Note that despite racing in the same class and exhibiting a similar lesion level, age, time since injury, and neurological completeness of injury, the athlete with autonomic incomplete SCI maintained a higher speed throughout the lap, specifically between the start/finish line and the third inlet, during which time the course was predominantly flat or uphill.
Championship time-trial event. Athletes with thoracic injuries were significantly faster than athletes with cervical injuries. This lesion-dependent response is most likely a reflection of the greater muscle mass used and subsequent increase in power output and aerobic exercise capacity in athletes with thoracic SCI vs athletes with cervical SCI (Wicks et al., 1983; Campbell et al., 2004). An interesting and noteworthy finding was that athletes with cervical SCI exhibit a similar maximum HR to that of thoracic SCI athletes. This is in contrast to almost all previous literature describing the HR response to exercise in the SCI population, whereby individuals with cervical injuries present with an attenuated HR response to exercise (Theisen, 2012). Since we have previously reported that maximum HR is critically dependent on the degree of sympathetic decentralization (West et al., 2013b), we believe the lack of between lesion-level difference in maximum HR is a reflection of our findings that four of the athletes with cervical SCI had an autonomic incomplete injury. The similar maximum HRs between cervical and thoracic SCI may also be a reflection of the time trial being conducted in the field rather than the lab. In this respect, we have previously shown that field-based testing evokes superior cardiovascular responses to laboratory-based testing, most likely because of elite athletes being more accustomed to field- than laboratory-based exercise and having the freedom to self-select their speed and push technique (West et al., 2013b). To establish the within lesion level, and therefore the within racing class, effect of autonomic completeness of injury on exercise responses and endurance
performance, we stratified athletes with the same level of injury by autonomic completeness. For cervical SCI, athletes with autonomic incomplete SCI outperformed their lesion-level matched autonomic complete counterparts, and exhibited superior physiological responses during exercise. We also found results indicative of a strong association between HRpeak and time-trial time in athletes with cervical SCI, confirming our previous findings in court-based athletes (West et al., 2013b). The cardiovascular response to exercise in (autonomic complete) cervical SCI is compromised by the loss of supraspinal control over the peripheral and splanchnic vasculature (Thijssen et al., 2009), a limited catecholaminergic response to exercise (Schmid et al., 1998), and reduced vasoconstrictor reserve below the injury (Groothuis et al., 2010). Together, these alterations in cardiovascular function conspire to impair venous return and stroke volume during exercise (Figoni et al., 1988). Accordingly, any exercise-induced increase in cardiac output is mediated entirely by increases in HR. In the face of such limitations, it is perhaps unsurprising that the ability to increase HR is a key determinant of endurance performance in cervical SCI athletes. Interestingly, by visualizing the GPS data, it became apparent that athletes with autonomic complete and incomplete cervical SCI were completing the downhill sections similarly (see Fig. 3 section between final inlet and finish); hence, top speeds were similar between autonomic complete and incomplete cervical SCI. When athletes were pushing on the uphill and flat sections of the course (see Fig. 3, sections between inlets 1, 2, and 3), however, the differences between autonomic complete and
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West et al. incomplete cervical SCI were much more apparent; hence, average speed was substantially faster in autonomic incomplete cervical SCI. We believe these findings reflect the greater dependence on the cardiorespiratory system during flat/uphill pushing vs downhill “cruising.” Together, these data demonstrate that athletes with autonomic incomplete cervical SCI are at a distinct advantage during endurance activities compared with their autonomic complete counterparts. The peak HR values obtained in the autonomic complete cervical SCI group were markedly higher than those typically reported in the literature. Interestingly, the group mean value of 169 bpm is remarkably similar to that reported by Schmid et al. (2001) during exercise in a dysreflexic state. AD, a condition defined by uncontrolled hypertension, can occur during exercise in SCI either intentionally (i.e., boosting) or non-intentionally due to some form of afferent stimuli, such as a full bladder (Krassioukov, 2012). This latter cause of AD may be particularly problematic in endurance events (such as the time trial) because of excessive fluid intake without micturition. Although a dysreflexic state has been shown to improve time-trial performance by 10% (Burnham et al., 1994), the associated uncontrolled hypertensive episodes can also lead to deleterious side effects such as dizziness, blurred vision and impaired cognition, and left untreated can lead to life threatening consequences, including, intracranial hemorrhage, retinal detachments, seizures, cardiac arrhythmias, and even death (Eltorai et al., 1992; Ho & Krassioukov, 2010). In the current study, we were unable to control for AD during the time trial; however, we did ask athletes to self-report if they boosted during the event. One autonomic complete cervical SCI athlete self-reported that he boosted during the competition; hence, this may go some way to explaining the high HRs in this group. An alternative explanation for the high peak HR in autonomic complete cervical SCI may relate to an increased activation of cardiac β-receptors secondary to an exerciseinduced increase in systemic norepinephrine. In this regard, it has been reported that tetraplegics exhibit an exercise-induced increase in norepinephrine during exercise (Schmid et al., 1998), presumably a result of spill over into the systemic circulation from tonically active post-ganglionic sympathetic nerve endings. Although we made no measures of catecholamines during exercise in the current study, we think it unlikely that the high HRs obtained in our autonomic complete cervical SCI athletes were reflective of hormonal activation since the athletes all reached high HRs rapidly (i.e., within 30–60 s of the onset of exercise). In contrast to cervical SCI, we found no differences in endurance performance between autonomic complete and incomplete thoracic SCI, suggesting that the cardiovascular system may not limit performance to the same extent as in cervical SCI. This is in agreement with previous studies that have reported compression of the
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peripheral/splanchnic vasculature via an anti-gravity suit or an abdominal binder enhances exercise capacity/ endurance performance in cervical SCI (Pitetti et al., 1994; West et al., 2014a) but not in thoracic SCI (Hopman et al., 1993; Kerk et al., 1995). Improved exercise capacity of tetraplegics in response to a mechanically stimulated central translocation of peripheral blood volume implies that the limitation to exercise performance is likely more “central,” whereas the lack of improvement in paraplegics implies the limitation to exercise is not “central.” Thus, factors other than the degree of remaining autonomic cardiovascular control are likely to moderate endurance performance in athletes with a thoracic SCI. In conclusion, this is the first study to demonstrate that endurance performance in cervical SCI is critically dependent on not only the level of injury, but also on the extent of disruption to descending autonomic pathways. Athletes with autonomic incomplete cervical SCI exhibit a greater degree of exercise-induced cardiac chronotropy and enhanced endurance performance compared with autonomic complete cervical SCI. This finding has implications for sport classification since the current system accounts only for differences in level of injury rather than for differences in autonomic integrity. Together, these findings further demonstrate that autonomic function should be included into the classification of athletes with cervical SCI, especially in sports that involve a large cardiovascular demand. Perspectives While several studies have investigated the relationship between autonomic completeness of injury and cardiovascular function at rest and during exercise in athletes with SCI (West et al., 2013b, 2014b), no study has specifically examined the relationship between autonomic completeness of injury and endurance performance in the SCI population. We assessed 23 elite paracyclists with SCI at the 2013 Paracycling World Championships for resting cardio-autonomic function and time to complete a 17.3-km time-trial event. We found that athletes with cervical SCI who were autonomic incomplete exhibited superior time-trial performance and enhanced cardiovascular responses during exercise compared with their autonomic complete cervical SCI counterparts. The novel data collected here emphasize that the presence of descending sympathetic control is critical to elicit the appropriate hemodynamic responses to exercise in cervical SCI, and by extension to match oxygen delivery to demand. When descending sympathetic control is absent, impaired vaso- and sudo-motor function along with reduced cardiac chronotropy and inotropy conspire to curtail endurance performance. The relationship between autonomic integrity and endurance performance, however, does not hold for those with thoracic SCI suggesting that other as yet unidentified
Endurance performance in SCI mechanisms are more important for endurance performance in this sub-population. These data imply that elite athletes with autonomic incomplete cervical SCI are at a distinct endurance performance advantage during competition compared with their autonomic complete competitors. We propose, therefore, that autonomic testing should be incorporated into the classification of athletes with cervical SCI, particularly in sports with a large endurance component. Key words: Tetraplegia, paracycling, blood pressure.
paraplegia,
exercise,
Acknowledgements Data for this study was collected during the 2013 Paracycling World Championship. The authors would like to thank all paracyclists who took part in this study and the Union Cycliste Internationale for allowing the study to take place during the 2013 Paracycling World Championship. GPS devices were provided by the Centre for Hip Health and Mobility, University of British Columbia. Dr. C West is funded by a Craig Neilsen and Michael Smith Foundation for Health Research Postdoctoral Fellowship. Research in the laboratory of Dr. Krassioukov is funded by the Canadian Institute for Health research and the Craig Neilsen Foundation.
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