Authors: Phoebe Runciman, BA (Hons) Wayne Derman, MBChB, PhD Suzanne Ferreira, PhD Yumna Albertus-Kajee, PhD Ross Tucker, PhD
Affiliations:
Cerebral Palsy
ORIGINAL RESEARCH ARTICLE
From the UCT/MRC Research Unit for Exercise Science and Sports Medicine, University of Cape Town (PR, WD, YA-K, RT); International Olympic Committee Research Centre, Cape Town (WD); and Department of Sport Science, Stellenbosch University, South Africa (SF).
Correspondence: All correspondence and requests for reprints should be addressed to Phoebe Runciman, BA (Hons), UCT/MRC Research Unit for Exercise Science and Sports Medicine, University of Cape Town, Boundary Road, Newlands, 7700 Cape Town, South Africa.
Disclosures: Funded by the University of Cape Town, National Research Foundation (NRF) and the German Academic Exchange Service (DAAD). Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.
0894-9115/15/9401-0028 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 by Lippincott Williams & Wilkins DOI: 10.1097/PHM.0000000000000136
A Descriptive Comparison of Sprint Cycling Performance and Neuromuscular Characteristics in Able-Bodied Athletes and Paralympic Athletes with Cerebral Palsy ABSTRACT Runciman P, Derman W, Ferreira S, Albertus-Kajee Y, Tucker R: A descriptive comparison of sprint cycling performance and neuromuscular characteristics in able-bodied athletes and Paralympic athletes with cerebral palsy. Am J Phys Med Rehabil 2015;94:28Y37.
Objective: This study investigated the sprint cycling performance and neuromuscular characteristics of Paralympic athletes with cerebral palsy (CP) during a fatiguing maximal cycling trial compared with those of able-bodied (AB) athletes. Design: Five elite athletes with CP and 16 AB age- and performance-matched controls performed a 30-sec Wingate cycle test. Power output (W/kg) and fatigue index (%) were calculated. Electromyography was measured in five bilateral muscles and expressed in mean amplitude (mV) and median frequency (Hz).
Results: Power output was significantly higher in the AB group (10.4 [0.5] W/kg) than in the CP group (9.8 [0.5] W/kg) (P G 0.05). Fatigue index was statistically similar between the AB (27% [0.1%]) and CP (25% [0.1%]) groups. Electromyographic mean amplitude and frequency changed similarly in all muscle groups tested, in both affected and nonaffected sides, in the CP and AB groups (P G 0.05). Neuromuscular irregularities were identified in the CP group.
Conclusions: The similarity in fatigue between the CP and AB groups indicates that elite athletes with CP may have a different exercise response to others with CP. The authors propose that this may result from high-level training over many years. This has rehabilitative implications, as it indicates near-maximal adaptation of the CP body toward normal levels. Key Words: Activation
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Wingate, Elite, Disability, Electromyography, Fatigue, Spasticity, Muscle
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C
erebral palsy (CP), with an incidence of 2.5 per 1000 live births, is one of the most common conditions affecting the neuromuscular system.1 Damage before, during, or directly after birth to one of three areas of the brain controlling movement and coordination leads to various movement impairments, including spasticity, dyskinesia, and ataxia.2,3 It has been proposed that exercise performance is impaired in individuals with CP, purportedly because of the central inhibition of motor unit activation4,5 caused by these brain lesions. This hypothesis has, however, been tested in sedentary children, with little research existing on the effect of CP on exercise performance and neuromuscular control in welltrained, adult individuals. Several studies using pediatric participants have described marked impairments in exercise performance. Isometric strength5 and sprint running speed6 have been found to be 39% to 56% lower in individuals with CP than in able-bodied (AB) controls. Deficits ranging between two and four standard deviations have been found in Wingate anaerobic performance of children with CP when compared with age- and activity-matched children without CP.7,8 Furthermore, Verschuren et al.9 found that aerobic endurance performance (V˙O2peak) using a progressive maximal treadmill test was 15% lower in individuals with CP. There is, however, evidence that regular physical training has functional benefits in children with CP. Intervention studies using sedentary, pediatric samples have found dramatic improvements in strength, aerobic capacity, and anaerobic capacity in both diplegic and hemiplegic groups, with as little as 6 wks of training.10Y12 Elite athletes, with and without disabilities, train at very high volumes for many years to compete at Olympic level. As no research exists on this caliber of athletes with CP, it is intriguing to consider whether elite levels of training in individuals with CP alter factors that contribute to performance, compared with AB individuals. These factors include fatigue profiles, peak power output capacity, and neuromuscular characteristics. A comparison between performancematched athletes would improve understanding of the persistence of the effects of CP, despite elite level training. The aim of this descriptive study was to investigate the sprint cycle performance and neuromuscular characteristics of elite Paralympic athletes with CP during a fatiguing maximal cycling trial compared with those of well-trained, sprint performance-matched AB athletes. The athletes www.ajpmr.com
with CP (CP group) were internationally competitive track and field athletes who have trained for between 6 and 15 hrs/wk over many years. Power output, muscle activation, and fatigue characteristics, as well as the presence of neuromuscular irregularities, were investigated between the groups. It was hypothesized that the CP group would perform the Wingate cycle test at a significantly lower power output than the AB group would and would show a flatter fatigue profile in power output over the course of the test. It was further hypothesized that the lower power output would be associated with a significantly lower level of muscle activation, as measured by electromyography (EMG). This would be in keeping with the published literature in untrained and pediatric individuals with CP.
METHODS Participants Five male elite athletes with spastic hemiplegic CP and 16 male well-trained AB controls were recruited for the study. The participants in the CP group were all track sprinters with hemiplegic CP, as diagnosed by a physician. They all competed at international Paralympic level. Three of the participants were classified as T38 and two as T37 athletes, in accordance with the criteria established by the Cerebral Palsy International Sports and Recreation Association and the International Paralympic Committee for Paralympic competition. T37 athletes are classified as having true ambulant spastic hemiplegia and present with distinctive hemiplegic limitations, with a fully functional nonaffected side. T38 athletes are distinguished by limitations in running activities in any limb distribution as a result of hypertonia, ataxia, or athetosis. Both T38 and T37 athletes present with grade 1 to 2 spasticity on the Modified Ashworth Scale, which indicates a mild to moderate level of resting spasticity in the affected limbs.13 Both T38 and T37 athletes fall into levels 1 to 3 on the Gross Motor Function Classification System.14 AB participants were selected from rugby, cricket, and hockey and were additionally selected only if they played in positions where sprint ability was an important attribute for performance. They competed from club to international level. All participants were unaccustomed to leg cycling exercise, as their main form of exercise was running-based sprint exercise. Cycling was used as a modality as the Wingate test is a validated method for assessing sprint performance and allows the capture of data at a high sampling rate. The use of Exercise Performance Comparison Between Athletes
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the Wingate cycle test minimized the effect of experience of cycling on performance in either group. The groups were matched for age (21.6 [4.2] yrs and 23.4 [3.0] yrs for the CP and AB groups, respectively) and current 100-m running sprint performance (12.2 [0.9] and 12.3 [1.1] for the for CP and AB groups, respectively). However, the AB participants were significantly heavier than the CP group (body mass index of 25.9 [2.4] kg/m2 vs. 21.1 [1.4] kg/m2). Each participant provided written informed consent before the study. The study was approved by the university’s Research and Human Ethics Committee (Ref: 156/2011).
General Overview of Testing Participants reported to the laboratory on one occasion. Their height and body mass were measured on calibrated equipment (Seca, Model 708, Hamburg, Germany). Participants performed a 10sec sprint test, adapted from the standard 30-sec Wingate anaerobic sprint test (WIN30). After this, participants rested for 15 mins and then performed a traditional WIN30. The 10-sec sprint was used to ensure a maximal effort in WIN30 through a comparison of the first 10 secs power output of both tests. It was also used for normalization of the EMG signal recorded during WIN30. Bilateral EMG activity of five muscles was measured during both tests. The specific details of these measurements are described subsequently.
Wingate Anaerobic Test The WIN30 was performed using an electromagnetically braked cycle ergometer (Velotron Dynafit Pro; Racermate Inc, Seattle, WA). This test has been validated in many populations, including CP, and has an interclass correlation coefficient of 0.95 in trained and nontrained individuals with CP.15,16 A standardized warm-up comprised cycling at a constant workload of 1.5 W/kg at a self-selected cadence for 5 mins, followed by a 2-min rest period before commencement of the 10-sec sprint. Upon completion of the sprint a break of 15 mins, WIN30 was performed. For standardization in both the sprint and WIN30, the participants were given 20 secs to reach 100 rpm and then were instructed to maintain 100 rpm for 10 secs, after which time a load of 0.075 kg/kg body mass was applied, commencing the test. Participants were instructed to pedal as hard and as fast as they could against the resistance for the set period (10 or 30 secs). They were instructed to remain in a seated position
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throughout the test. Power output was expressed relative to body mass (W/kg).
Fatigue Index The fatigue index (FI) was calculated as the highest power output (W/kg) achieved during the test minus the power output (W/kg) achieved in the final second of the test. This was divided by the peak power. The FI is expressed as a percentage.
Electromyography Amplitude The EMG activity of five muscles, namely, erector spinae (ES), gluteus medius, biceps femoris (BF), gastrocnemius, and vastus lateralis (VLO), was recorded in both legs using a telemetric EMG system (GT2400 G2; Noraxon, USA Inc, Scottsdale, AZ), to allow comparison of affected and nonaffected sides in the participants with CP. Affected and nonaffected sides corresponded to their nondominant and dominant sides. In the AB group, the nondominant and dominant legs were similarly compared. Before the placement of the electrodes, the area was shaved and cleaned with ethanol. Two electrodes (Blue Sensor; Medicotest, Klstykke, Denmark) were placed over the muscle belly while a reference electrode was placed on the anterior superior iliac spine of the right leg. Placement was in accordance with Surface Electromyography for the Non-Invasive Assessment of Muscle recommendations.17 As with previous research using EMG during cycling, each test was divided into 5-sec periods for processing and analysis.18Y20 For analysis of the EMG signal, the raw EMG signals were band pass filtered between 20 and 500 Hz. All signals were rectified and smoothed using root mean square analysis for a 50-msec time window. The EMG in WIN30 was normalized to the highest mean amplitude 5-sec period of the 10-sec sprint. The use of a 10-sec sprint for EMG normalization establishes a constant baseline of EMG activity to which all subsequent activity is compared and expressed as a percentage. This has been shown to be a valid method of normalization for dynamic exercise.21 To ensure reliable EMG data reporting, EMG was measured in a rested state as well as during manual isolation of every muscle. This ensured that the signals recorded were not artefacts of incorrect placement, movement, or noise generated by external variables. Mean normalized amplitude of the 5-sec periods as well as individual root-meansquared EMG signals to identify irregularities were analyzed for the present study.
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Frequency
RESULTS
Median frequency spectral analysis of the first and last 5-sec periods of WIN30 was performed using a Fast Fourier Transform algorithm. EMG frequency is the rate at which action potentials are sent to the working muscles from the central nervous system. Higher median frequencies are a mechanism of muscular force summation (higher force), whereas a change in frequency indicates a change in the type of muscle fibers activated and, ultimately, fatigue.22,23 The analysis was therefore performed to compare frequency between nonfatigued states (in the first 5 secs of the test) and fatigued states (in the last 5 secs of the test). The frequency analyses were between 5 and 500 Hz, as EMG signal outside this range contains mostly noise and unusable signal.24 As the authors were interested in fatigue, the change from prefatigue and postfatigue is reported.
Wingate Anaerobic Test
Statistical Analysis Power output and EMG were averaged over 1and 5-sec periods, respectively. All data were analyzed using statistical software (Statistica 10; Statsoft Inc, Tulsa, OK). Significance was accepted at a P value G 0.05. Intragroup comparisons between affected and nonaffected sides, as well as change over time between the groups, were performed using repeated-measures analysis of variance (time side group interaction). Descriptive data of the two groups were compared using independent t tests.
Peak power output during WIN30 was 10.4 (0.5) and 9.8 (0.5) W/kg for the AB and CP groups, respectively (P G 0.05), and occurred at 10 secs in both groups (Fig. 1). Power output was significantly higher in AB participants (P G 0.05). Power output declined similarly between groups, with the FI of the AB and CP groups calculated as 27% (6.9%) and 25% (7.3%), respectively.
Electromyography Amplitude Figure 2AYE shows normalized EMG activity on the affected and nonaffected sides of the five measured muscles in the CP group (left panels) and AB group (right panels). There were no differences in mean muscle activity over time between the affected and nonaffected sides, nor between the AB and CP groups. In four muscle groups (ES, Fig. 2A; gluteus medius, Fig. 2B; BF, Fig. 2C; gastrocnemius, Fig. 2D), EMG amplitude decreased significantly over the trial in both limbs and in both the CP and AB groups (P G 0.001). In both the CP and AB groups, VLO activity remained unchanged over time in both the CP and AB groups (Fig. 2E).
Frequency Median frequency decreased significantly but similarly between the AB and CP groups and on both the affected and nonaffected sides (Table 1, P G 0.05). Median frequency decreased significantly
FIGURE 1 Power output of 30-sec Wingate test for the able-bodied group (solid triangle) and cerebral palsy group (open square), with peak in both groups at 10 secs. *P G 0.05, time and group effect. www.ajpmr.com
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FIGURE 2 Normalized electromyographic activation over a 30-sec Wingate test for affected and nonaffected sides of the cerebral palsy (CP) group (left panel) and correlating nondominant and dominant sides of theable-bodied (AB) group (right panel) for erector spinae (A), gluteus medius (B), biceps femoris (C), gastrocnemius (D), and vastus lateralis (E). *P G 0.05, time effect.
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TABLE 1 Percentage (%) decrease in median frequency from prefatigued to postfatigued states for affected (A) and nonaffected (NA) sides in the cerebral palsy group (left column) and correlating nondominant (ND) and dominant (D) sides in the able-bodied group (right column) Cerebral Palsy Muscle Erector spinae Gluteus medius Biceps femoris Gastrocnemius Vastus lateralis a b
Able-Bodied
A
NA
ND
D
17.16%a 15.10%a 20.24%a 6.91%a 13.35%b
10.08%a 11.42%a 15.68%a 10.48%a 12.68%a
20.99%a 3.08%a 8.54%a 14.67%a 8.48%a
7.03%a 5.17%a 7.41%a 7.45%a 13.10%a
P G 0.05, time effect. P G 0.05, side and time and group effect.
more in VLO in the affected side of the CP group compared with the AB group (P G 0.05).
Individual EMG Trace Patterns Figure 3A shows bilateral coactivation of the stabilizing ES muscles on each pedal stroke in an AB participant during WIN30. The pedal stroke is identified by VLO activation in the bottom trace of the panel, with the top trace depicting ES activation. Figure 3B depicts an atypical firing pattern of the ES observed in a participant with CP. ES activity occurs during the pedal stroke on the nonaffected pedal stroke only, with no activity during the affected side’s pedal stroke. Figure 4A shows a typical firing pattern of two power producing muscles (BF and VLO) in an AB participant, which reciprocally activate per pedal
stroke. Figure 4B shows a trace of a participant with CP. BF activation on both sides increases when the affected side pedal stroke occurs. On the nonaffected side, there is significantly less BF activation. Figure 4C displays continuous activation of BF muscles of both the affected and nonaffected legs, with typical firing patterns of the VLO muscle.
DISCUSSION The present study compared elite athletes with CP with age- and sprint timeYmatched AB athletes, in a fatiguing maximal cycling task. It was initially hypothesized, based on previous literature, that individuals with CP would present with significantly lower power outputs and muscle activation levels as well as display less attenuation of these parameters with fatigue during a maximal sprint trial. It was
FIGURE 3 Electromyographic irregularities in stabilizing muscles in cerebral palsy. Typical firing pattern of the ES in an able-bodied athlete (A) with a lack of required coactivation of the ES is observed in a participant with cerebral palsy (B). VLO, vastus lateralis; ES, erector spinae. www.ajpmr.com
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FIGURE 4 Electromyographic irregularities in power-producing muscles in cerebral palsy. Typical firing pattern of vastus lateralis (VLO) and biceps femoris (BF) in an able-bodied athlete (A) in the first 5-sec epoch of the 30-sec Wingate test (nonfatigued state) is shown. Coactivation of the BF and VLO (B) and atypical motor drive of the BF (C) is observed in two participants with cerebral palsy.
found that the AB athletes produce higher power output throughout WIN30 (Fig. 1) but that all other aspects of performance, including FI and muscle activation levels, were similar between groups, providing evidence that athletes with CP can overcome previously documented deficits in performance and neuromuscular activation.
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FI was similar between groups, indicative of a similar decline in power output from peak value, measured at similar time points in CP and AB participants (Fig. 1). Associated mean EMG changed similarly over the trial in all measured musclegroups (Fig. 2). Furthermore, changes in EMG over the trial were similar between the affected
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and nonaffected sides in the CP group and corresponding nondominant and dominant sides in the AB group. The existing literature suggests that individuals with similar forms of CP to the current sample exhibit lower levels of neuromuscular fatigue as a result of suboptimal central drive and the consequent inability to produce enough isokinetic torque to create fatigue.5,25,26 This has been attributed to multiple factors including spasticity, coactivation, type I muscle fiber predominance, and weakness.27Y30 This study’s data suggest that despite weakness, demonstrated by lower power outputs in the Wingate test (10.4 [0.5] W/kg and 9.8 [0.5] W/kg for the AB and CP groups, respectively; P G 0.05), the associated lower neuromuscular fatigue shown by literature was not present in this elite athletic sample. This was demonstrated by the similarity in FI and progressive decrease in EMG activity over the trial between the AB and CP groups in all five muscles tested (P G 0.05). It is interesting to speculate whether these results may be the effect of long-term, high-level athletic training. Research to date that shows deficits in performance and flattened fatigue profiles in CP has been performed on sedentary children.31 However, marked changes in muscular adaptation have been observed with exercise training in these samples, making it clear that there is capacity to significantly improve exercise performance and functional capacity.10Y12 The current sample of elite-level athletes may represent a group of individuals with CP who have reached near-maximal muscular adaptation, including the possible movement away from type I muscle fiber predominance muscular weakness. This may explain the similar fatigue profiles seen between groups (FI of 27% [6.9%] and 25% [7.3%] for the AB and CP groups, respectively; Fig. 1) and a greater peak power output achieved in the CP group compared with previously published power values for soccer and cycling nonelite athletes with CP (9.8 vs. 8.3 W/kg).16 Frequency analysis of the EMG signal further supports that the CP and AB groups fatigued similarly, as frequency shifts were similar between the groups. The observed changes, a shift from higher to lower frequencies, are typical of a shift from type II muscle fiber activation to type I fiber activation because of fatigue of the fast-twitch power-producing fibers.32 The similarity in frequency decline in both the CP and AB groups may further support the hypotheses of (1) a higher proportion of and (2) a higher use of type II muscle fibers in this sample of elite athletes with CP.32,33 A significantly greater reduction in www.ajpmr.com
frequency occurred in the CP group’s affected side VLO (the primary power producing muscle), further suggesting the utilization of type II muscle fibers. It may be argued that the similarities in physiology observed between the groups may be the result of a sample of athletes in classes T37 and T38, representing a group of individuals with milder forms of CP. The authors believe that this is not the primary origin of the results of the present study, as they only refer to previous studies conducted using individuals in Gross Motor Function Classification System levels 1 to 3, which are comparable with the level of impairment in the current sample of athletes with CP. The possibility of this contributing factor, however, cannot be disregarded. The second important finding was the presence of neuromuscular irregularities identified in the athletes with CP that are associated with CP, in both stabilizing (ES muscles, Fig. 3) and power (VLO and BF muscles, Fig. 4) muscles, despite the similar response to fatigue to AB athletes. Figure 3 shows coactivation of both ES muscles on the nonaffected side’s pedal stroke and complete lack of activation on the affected side’s pedal stroke of an athlete with CP (Fig. 3B). The existing theory on the role of the stabilizing ES muscles during locomotion is that the ES muscles bilaterally coactivate with heel strike/pedal stroke to counteract unwanted trunk movement.34,35 They also, in conjunction with other lower back muscles, balance external loads to decrease forces on the spine, which, when disrupted, leads to injury.36,37 Thus, the lack of firing on the CP’s affected side may impair the stability required for that side’s pedal stroke and predispose this athlete to injury. Furthermore, neuromuscular irregularities in power muscles (Fig. 4) may have an impact on injury incidence, as well as overall performance.38,39 Figure 4A demonstrates typical BF and VLO activity in an AB participant. VLO and BF are active in a reciprocal manner, ensuring that the application of downward force to the pedal is timed appropriately during the upstroke. Figure 4B demonstrates coactivation of the agonist (VLO) and antagonist (BF) muscles on the affected side, with a lack of activation on the nonaffected side, where it is also required for correct pedal power production. van Ingen Schenau et al.40 concluded that biarticular muscles, including the BF, were involved in the control of the direction of force application on the pedal during cycling; therefore, coactivation may produce counteracting torques on each pedal stroke. That is, the BF may fire on the downward portion of the pedal stroke, essentially exerting opposite forces Exercise Performance Comparison Between Athletes
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to the VLO, which would result in both forces being exerted on the pedal simultaneously with a consequent loss of economy. The observed coactivation of this antagonist pair, however, may also be an activation strategy required for increased joint stability on the affected side, by equalizing articular movement and pressure during force application.41Y43 Furthermore Figure 4C displays continuous activation of BF muscles of both the affected and nonaffected legs despite typical firing patterns of the VLO muscle, indicating an atypical motor drive.4 The complete lack of coherent firing patterns may lead to a lack of coordinated power production for both the affected and nonaffected sides, which would result in a reduction in power output. There may also be an increased risk of injury owing to compensation by the antagonist muscle groups, which has been shown to be a major risk factor for muscle injuries in runners.44,45 This descriptive study has identified interesting findings in an unstudied sample, but with certain limitations. This study was unable to obtain strokeby-stroke bilateral power output on the cycle ergometer, a measurement that would have proved very useful in identifying neuromuscular differences between sides. The use of M-wave stimulation would have also allowed for absolute amplitude EMG activation comparisons between sides and is advised for future studies in this area. Finally, it would have been ideal to be able to conduct fiber typing via biopsy in the athletes, which would support this study’s hypothesis, but the expensive and invasive nature of the test needs to be taken into consideration. Future studies in this area may elucidate mechanisms for the findings of the current study. Future studies are also required during running exercise, applicable to the athletes involved. The present study described performance and neuromuscular characteristics of elite athletes with CP during maximal sprint cycling. The similarity in power output FI as well as neuromuscular fatigue between the CP and AB groups indicates that the current sample of elite athletes with CP may have a different physiology from the previously studied untrained individuals with CP. The authors propose that this movement toward AB levels may be a result of high-level training over many years. This may have both empirical and clinical application, as it may indicate the uppermost ability of the cerebral-palsied body to adapt toward normal levels. If so, these findings have large implications for CP rehabilitation and athletic participation as a form of rehabilitation. Further research, however, is required to either support or refute findings of the current study.
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ACKNOWLEDGMENTS
We thank the athletes for their time and the Sport Physiology Laboratory, Department of Sport Science, Stellenbosch University, for their assistance. REFERENCES 1. Bialik GM, Givon U: Cerebral palsy: Classification and etiology. Acta Orthop Traumatol Turc 2009;43:77Y80 2. Johnston MV, Hoon AH Jr: Cerebral palsy. Neuromolecular Med 2006;8:435Y50 3. Reddihough DS, Collins KJ: The epidemiology and causes of cerebral palsy. Aust J Physiother 2003; 49:7Y12 4. Rose J, McGill KC: Neuromuscular activation and motor-unit firing characteristics in cerebral palsy. Dev Med Child Neurol 2005;47:329Y36 5. Stackhouse SK, Binder-Macleod SA, Lee SC: Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve 2005;31:594Y601 6. Verschuren O, Bloemen M, Kruitwagen C, et al: Reference values for anaerobic performance and agility in ambulatory children and adolescents with cerebral palsy. Dev Med Child Neurol 2010;52:e222Y8 7. Bar-Or O: The Wingate anaerobic test. An update on methodology, reliability and validity. Sports Med 1987;4:381Y94 8. Parker DF, Carriere L, Hebestreit H, et al: Anaerobic endurance and peak muscle power in children with spastic cerebral palsy. Am J Dis Child 1992;146: 1069Y73 9. Verschuren O, Takken T: Aerobic capacity in children and adolescents with cerebral palsy. Res Dev Disabil 2010;31:1352Y7 10. Reid S, Hamer P, Alderson J, et al: Neuromuscular adaptations to eccentric strength training in children and adolescents with cerebral palsy. Dev Med Child Neurol 2010;52:358Y63 11. MacPhail HE, Kramer JF: Effect of isokinetic strengthtraining on functional ability and walking efficiency in adolescents with cerebral palsy. Dev Med Child Neurol 1995;37:763Y75 12. Verschuren O, Ketelaar M, Gorter JW, et al: Exercise training program in children and adolescents with cerebral palsy: A randomized controlled trial. Arch Pediatr Adolesc Med 2007;161:1075Y81 13. Tweedy SM: International Paralympic Committee Athletics Classification Project for Physical Impairments: Final Report-Stage 1. July;1.2(2010/07/16). Available at: http://www.paralympic.org/Athletics/RulesandRegulations/ Classification. Accessed November 15, 2012. 14. Morris C: Development of the gross motor function classification system (1997). Dev Med Child Neurol 2008;50:5 15. Astorino TA, Cottrell T: Reliability and validity of the Velotron Racermate Cycle Ergometer to measure anaerobic power. Int J Sports Med 2012;33:205Y10
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23. Merletti R, Lo Conte LR: Advances in processing of surface myoelectric signals: Part 1. Med Biol Eng Comput 1995;33(3 spec no):362Y72 24. Hunter AM, St Clair GA, Lambert MI, et al: Effects of supramaximal exercise on the electromyographic signal. Br J Sports Med 2003;37:296Y9 25. Brunton LK, Rice CL: Fatigue in cerebral palsy: A critical review. Dev Neurorehabil 2012;15:54Y62 26. Moreau NG, Li L, Geaghan JP, et al: Fatigue resistance during a voluntary performance task is associated with lower levels of mobility in cerebral palsy. Arch Phys Med Rehabil 2008;89:2011Y6 27. Wiley ME, Damiano DL: Lower-extremity strength profiles in spastic cerebral palsy. Dev Med Child Neurol 1998;40:100Y7 28. Allman BL, Rice CL: Neuromuscular fatigue and aging: Central and peripheral factors. Muscle Nerve 2002;25:785Y96 29. Hunter SK, Enoka RM: Sex differences in the fatigability of arm muscles depends on absolute force during isometric contractions. J Appl Physiol 2001;91: 2686Y94 30. Ratel S, Lazaar N, Williams CA, et al: Age differences in human skeletal muscle fatigue during highintensity intermittent exercise. Acta Paediatr 2003;92: 1248Y54
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38. Damiano DL, Martellotta TL, Sullivan DJ, et al: Muscle force production and functional performance in spastic cerebral palsy: Relationship of cocontraction. Arch Phys Med Rehabil 2000;81:895Y900 39. Myklebust BM, Gottlieb GL, Penn RD, et al: Reciprocal excitation of antagonistic muscles as a differentiating feature in spasticity. Ann Neurol 1982;12:367Y74 40. van Ingen Schenau GJ, Boots PJ, de Groot G, et al: The constrained control of force and position in multi-joint movements. Neuroscience 1992;46:197Y207 41. Hug F, Dorel S: Electromyographic analysis of pedaling: A review. J Electromyogr Kinesiol 2009;19:182Y98 42. Hirokawa S: Three-dimensional mathematical model analysis of the patellofemoral joint. J Biomech 1991;24:659Y71 43. Solomonow M, Baratta R, Zhou BH, et al: Electromyogram coactivation patterns of the elbow antagonist muscles during slow isokinetic movement. Exp Neurol 1988;100:470Y7 44. Yeung SS, Suen AM, Yeung EW: A prospective cohort study of hamstring injuries in competitive sprinters: Preseason muscle imbalance as a possible risk factor. Br J Sports Med 2009;43:589Y94 45. Renstrom AF: Mechanism, diagnosis, and treatment of running injuries. Instr Course Lect 1993;42:225Y34
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Affiliations:
Cerebral Palsy
ORIGINAL RESEARCH ARTICLE
From the UCT/MRC Research Unit for Exercise Science and Sports Medicine, University of Cape Town (PR, WD, YA-K, RT); International Olympic Committee Research Centre, Cape Town (WD); and Department of Sport Science, Stellenbosch University, South Africa (SF).
Correspondence: All correspondence and requests for reprints should be addressed to Phoebe Runciman, BA (Hons), UCT/MRC Research Unit for Exercise Science and Sports Medicine, University of Cape Town, Boundary Road, Newlands, 7700 Cape Town, South Africa.
Disclosures: Funded by the University of Cape Town, National Research Foundation (NRF) and the German Academic Exchange Service (DAAD). Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.
0894-9115/15/9401-0028 American Journal of Physical Medicine & Rehabilitation Copyright * 2014 by Lippincott Williams & Wilkins DOI: 10.1097/PHM.0000000000000136
A Descriptive Comparison of Sprint Cycling Performance and Neuromuscular Characteristics in Able-Bodied Athletes and Paralympic Athletes with Cerebral Palsy ABSTRACT Runciman P, Derman W, Ferreira S, Albertus-Kajee Y, Tucker R: A descriptive comparison of sprint cycling performance and neuromuscular characteristics in able-bodied athletes and Paralympic athletes with cerebral palsy. Am J Phys Med Rehabil 2015;94:28Y37.
Objective: This study investigated the sprint cycling performance and neuromuscular characteristics of Paralympic athletes with cerebral palsy (CP) during a fatiguing maximal cycling trial compared with those of able-bodied (AB) athletes. Design: Five elite athletes with CP and 16 AB age- and performance-matched controls performed a 30-sec Wingate cycle test. Power output (W/kg) and fatigue index (%) were calculated. Electromyography was measured in five bilateral muscles and expressed in mean amplitude (mV) and median frequency (Hz).
Results: Power output was significantly higher in the AB group (10.4 [0.5] W/kg) than in the CP group (9.8 [0.5] W/kg) (P G 0.05). Fatigue index was statistically similar between the AB (27% [0.1%]) and CP (25% [0.1%]) groups. Electromyographic mean amplitude and frequency changed similarly in all muscle groups tested, in both affected and nonaffected sides, in the CP and AB groups (P G 0.05). Neuromuscular irregularities were identified in the CP group.
Conclusions: The similarity in fatigue between the CP and AB groups indicates that elite athletes with CP may have a different exercise response to others with CP. The authors propose that this may result from high-level training over many years. This has rehabilitative implications, as it indicates near-maximal adaptation of the CP body toward normal levels. Key Words: Activation
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Wingate, Elite, Disability, Electromyography, Fatigue, Spasticity, Muscle
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C
erebral palsy (CP), with an incidence of 2.5 per 1000 live births, is one of the most common conditions affecting the neuromuscular system.1 Damage before, during, or directly after birth to one of three areas of the brain controlling movement and coordination leads to various movement impairments, including spasticity, dyskinesia, and ataxia.2,3 It has been proposed that exercise performance is impaired in individuals with CP, purportedly because of the central inhibition of motor unit activation4,5 caused by these brain lesions. This hypothesis has, however, been tested in sedentary children, with little research existing on the effect of CP on exercise performance and neuromuscular control in welltrained, adult individuals. Several studies using pediatric participants have described marked impairments in exercise performance. Isometric strength5 and sprint running speed6 have been found to be 39% to 56% lower in individuals with CP than in able-bodied (AB) controls. Deficits ranging between two and four standard deviations have been found in Wingate anaerobic performance of children with CP when compared with age- and activity-matched children without CP.7,8 Furthermore, Verschuren et al.9 found that aerobic endurance performance (V˙O2peak) using a progressive maximal treadmill test was 15% lower in individuals with CP. There is, however, evidence that regular physical training has functional benefits in children with CP. Intervention studies using sedentary, pediatric samples have found dramatic improvements in strength, aerobic capacity, and anaerobic capacity in both diplegic and hemiplegic groups, with as little as 6 wks of training.10Y12 Elite athletes, with and without disabilities, train at very high volumes for many years to compete at Olympic level. As no research exists on this caliber of athletes with CP, it is intriguing to consider whether elite levels of training in individuals with CP alter factors that contribute to performance, compared with AB individuals. These factors include fatigue profiles, peak power output capacity, and neuromuscular characteristics. A comparison between performancematched athletes would improve understanding of the persistence of the effects of CP, despite elite level training. The aim of this descriptive study was to investigate the sprint cycle performance and neuromuscular characteristics of elite Paralympic athletes with CP during a fatiguing maximal cycling trial compared with those of well-trained, sprint performance-matched AB athletes. The athletes www.ajpmr.com
with CP (CP group) were internationally competitive track and field athletes who have trained for between 6 and 15 hrs/wk over many years. Power output, muscle activation, and fatigue characteristics, as well as the presence of neuromuscular irregularities, were investigated between the groups. It was hypothesized that the CP group would perform the Wingate cycle test at a significantly lower power output than the AB group would and would show a flatter fatigue profile in power output over the course of the test. It was further hypothesized that the lower power output would be associated with a significantly lower level of muscle activation, as measured by electromyography (EMG). This would be in keeping with the published literature in untrained and pediatric individuals with CP.
METHODS Participants Five male elite athletes with spastic hemiplegic CP and 16 male well-trained AB controls were recruited for the study. The participants in the CP group were all track sprinters with hemiplegic CP, as diagnosed by a physician. They all competed at international Paralympic level. Three of the participants were classified as T38 and two as T37 athletes, in accordance with the criteria established by the Cerebral Palsy International Sports and Recreation Association and the International Paralympic Committee for Paralympic competition. T37 athletes are classified as having true ambulant spastic hemiplegia and present with distinctive hemiplegic limitations, with a fully functional nonaffected side. T38 athletes are distinguished by limitations in running activities in any limb distribution as a result of hypertonia, ataxia, or athetosis. Both T38 and T37 athletes present with grade 1 to 2 spasticity on the Modified Ashworth Scale, which indicates a mild to moderate level of resting spasticity in the affected limbs.13 Both T38 and T37 athletes fall into levels 1 to 3 on the Gross Motor Function Classification System.14 AB participants were selected from rugby, cricket, and hockey and were additionally selected only if they played in positions where sprint ability was an important attribute for performance. They competed from club to international level. All participants were unaccustomed to leg cycling exercise, as their main form of exercise was running-based sprint exercise. Cycling was used as a modality as the Wingate test is a validated method for assessing sprint performance and allows the capture of data at a high sampling rate. The use of Exercise Performance Comparison Between Athletes
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the Wingate cycle test minimized the effect of experience of cycling on performance in either group. The groups were matched for age (21.6 [4.2] yrs and 23.4 [3.0] yrs for the CP and AB groups, respectively) and current 100-m running sprint performance (12.2 [0.9] and 12.3 [1.1] for the for CP and AB groups, respectively). However, the AB participants were significantly heavier than the CP group (body mass index of 25.9 [2.4] kg/m2 vs. 21.1 [1.4] kg/m2). Each participant provided written informed consent before the study. The study was approved by the university’s Research and Human Ethics Committee (Ref: 156/2011).
General Overview of Testing Participants reported to the laboratory on one occasion. Their height and body mass were measured on calibrated equipment (Seca, Model 708, Hamburg, Germany). Participants performed a 10sec sprint test, adapted from the standard 30-sec Wingate anaerobic sprint test (WIN30). After this, participants rested for 15 mins and then performed a traditional WIN30. The 10-sec sprint was used to ensure a maximal effort in WIN30 through a comparison of the first 10 secs power output of both tests. It was also used for normalization of the EMG signal recorded during WIN30. Bilateral EMG activity of five muscles was measured during both tests. The specific details of these measurements are described subsequently.
Wingate Anaerobic Test The WIN30 was performed using an electromagnetically braked cycle ergometer (Velotron Dynafit Pro; Racermate Inc, Seattle, WA). This test has been validated in many populations, including CP, and has an interclass correlation coefficient of 0.95 in trained and nontrained individuals with CP.15,16 A standardized warm-up comprised cycling at a constant workload of 1.5 W/kg at a self-selected cadence for 5 mins, followed by a 2-min rest period before commencement of the 10-sec sprint. Upon completion of the sprint a break of 15 mins, WIN30 was performed. For standardization in both the sprint and WIN30, the participants were given 20 secs to reach 100 rpm and then were instructed to maintain 100 rpm for 10 secs, after which time a load of 0.075 kg/kg body mass was applied, commencing the test. Participants were instructed to pedal as hard and as fast as they could against the resistance for the set period (10 or 30 secs). They were instructed to remain in a seated position
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throughout the test. Power output was expressed relative to body mass (W/kg).
Fatigue Index The fatigue index (FI) was calculated as the highest power output (W/kg) achieved during the test minus the power output (W/kg) achieved in the final second of the test. This was divided by the peak power. The FI is expressed as a percentage.
Electromyography Amplitude The EMG activity of five muscles, namely, erector spinae (ES), gluteus medius, biceps femoris (BF), gastrocnemius, and vastus lateralis (VLO), was recorded in both legs using a telemetric EMG system (GT2400 G2; Noraxon, USA Inc, Scottsdale, AZ), to allow comparison of affected and nonaffected sides in the participants with CP. Affected and nonaffected sides corresponded to their nondominant and dominant sides. In the AB group, the nondominant and dominant legs were similarly compared. Before the placement of the electrodes, the area was shaved and cleaned with ethanol. Two electrodes (Blue Sensor; Medicotest, Klstykke, Denmark) were placed over the muscle belly while a reference electrode was placed on the anterior superior iliac spine of the right leg. Placement was in accordance with Surface Electromyography for the Non-Invasive Assessment of Muscle recommendations.17 As with previous research using EMG during cycling, each test was divided into 5-sec periods for processing and analysis.18Y20 For analysis of the EMG signal, the raw EMG signals were band pass filtered between 20 and 500 Hz. All signals were rectified and smoothed using root mean square analysis for a 50-msec time window. The EMG in WIN30 was normalized to the highest mean amplitude 5-sec period of the 10-sec sprint. The use of a 10-sec sprint for EMG normalization establishes a constant baseline of EMG activity to which all subsequent activity is compared and expressed as a percentage. This has been shown to be a valid method of normalization for dynamic exercise.21 To ensure reliable EMG data reporting, EMG was measured in a rested state as well as during manual isolation of every muscle. This ensured that the signals recorded were not artefacts of incorrect placement, movement, or noise generated by external variables. Mean normalized amplitude of the 5-sec periods as well as individual root-meansquared EMG signals to identify irregularities were analyzed for the present study.
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Frequency
RESULTS
Median frequency spectral analysis of the first and last 5-sec periods of WIN30 was performed using a Fast Fourier Transform algorithm. EMG frequency is the rate at which action potentials are sent to the working muscles from the central nervous system. Higher median frequencies are a mechanism of muscular force summation (higher force), whereas a change in frequency indicates a change in the type of muscle fibers activated and, ultimately, fatigue.22,23 The analysis was therefore performed to compare frequency between nonfatigued states (in the first 5 secs of the test) and fatigued states (in the last 5 secs of the test). The frequency analyses were between 5 and 500 Hz, as EMG signal outside this range contains mostly noise and unusable signal.24 As the authors were interested in fatigue, the change from prefatigue and postfatigue is reported.
Wingate Anaerobic Test
Statistical Analysis Power output and EMG were averaged over 1and 5-sec periods, respectively. All data were analyzed using statistical software (Statistica 10; Statsoft Inc, Tulsa, OK). Significance was accepted at a P value G 0.05. Intragroup comparisons between affected and nonaffected sides, as well as change over time between the groups, were performed using repeated-measures analysis of variance (time side group interaction). Descriptive data of the two groups were compared using independent t tests.
Peak power output during WIN30 was 10.4 (0.5) and 9.8 (0.5) W/kg for the AB and CP groups, respectively (P G 0.05), and occurred at 10 secs in both groups (Fig. 1). Power output was significantly higher in AB participants (P G 0.05). Power output declined similarly between groups, with the FI of the AB and CP groups calculated as 27% (6.9%) and 25% (7.3%), respectively.
Electromyography Amplitude Figure 2AYE shows normalized EMG activity on the affected and nonaffected sides of the five measured muscles in the CP group (left panels) and AB group (right panels). There were no differences in mean muscle activity over time between the affected and nonaffected sides, nor between the AB and CP groups. In four muscle groups (ES, Fig. 2A; gluteus medius, Fig. 2B; BF, Fig. 2C; gastrocnemius, Fig. 2D), EMG amplitude decreased significantly over the trial in both limbs and in both the CP and AB groups (P G 0.001). In both the CP and AB groups, VLO activity remained unchanged over time in both the CP and AB groups (Fig. 2E).
Frequency Median frequency decreased significantly but similarly between the AB and CP groups and on both the affected and nonaffected sides (Table 1, P G 0.05). Median frequency decreased significantly
FIGURE 1 Power output of 30-sec Wingate test for the able-bodied group (solid triangle) and cerebral palsy group (open square), with peak in both groups at 10 secs. *P G 0.05, time and group effect. www.ajpmr.com
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FIGURE 2 Normalized electromyographic activation over a 30-sec Wingate test for affected and nonaffected sides of the cerebral palsy (CP) group (left panel) and correlating nondominant and dominant sides of theable-bodied (AB) group (right panel) for erector spinae (A), gluteus medius (B), biceps femoris (C), gastrocnemius (D), and vastus lateralis (E). *P G 0.05, time effect.
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TABLE 1 Percentage (%) decrease in median frequency from prefatigued to postfatigued states for affected (A) and nonaffected (NA) sides in the cerebral palsy group (left column) and correlating nondominant (ND) and dominant (D) sides in the able-bodied group (right column) Cerebral Palsy Muscle Erector spinae Gluteus medius Biceps femoris Gastrocnemius Vastus lateralis a b
Able-Bodied
A
NA
ND
D
17.16%a 15.10%a 20.24%a 6.91%a 13.35%b
10.08%a 11.42%a 15.68%a 10.48%a 12.68%a
20.99%a 3.08%a 8.54%a 14.67%a 8.48%a
7.03%a 5.17%a 7.41%a 7.45%a 13.10%a
P G 0.05, time effect. P G 0.05, side and time and group effect.
more in VLO in the affected side of the CP group compared with the AB group (P G 0.05).
Individual EMG Trace Patterns Figure 3A shows bilateral coactivation of the stabilizing ES muscles on each pedal stroke in an AB participant during WIN30. The pedal stroke is identified by VLO activation in the bottom trace of the panel, with the top trace depicting ES activation. Figure 3B depicts an atypical firing pattern of the ES observed in a participant with CP. ES activity occurs during the pedal stroke on the nonaffected pedal stroke only, with no activity during the affected side’s pedal stroke. Figure 4A shows a typical firing pattern of two power producing muscles (BF and VLO) in an AB participant, which reciprocally activate per pedal
stroke. Figure 4B shows a trace of a participant with CP. BF activation on both sides increases when the affected side pedal stroke occurs. On the nonaffected side, there is significantly less BF activation. Figure 4C displays continuous activation of BF muscles of both the affected and nonaffected legs, with typical firing patterns of the VLO muscle.
DISCUSSION The present study compared elite athletes with CP with age- and sprint timeYmatched AB athletes, in a fatiguing maximal cycling task. It was initially hypothesized, based on previous literature, that individuals with CP would present with significantly lower power outputs and muscle activation levels as well as display less attenuation of these parameters with fatigue during a maximal sprint trial. It was
FIGURE 3 Electromyographic irregularities in stabilizing muscles in cerebral palsy. Typical firing pattern of the ES in an able-bodied athlete (A) with a lack of required coactivation of the ES is observed in a participant with cerebral palsy (B). VLO, vastus lateralis; ES, erector spinae. www.ajpmr.com
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FIGURE 4 Electromyographic irregularities in power-producing muscles in cerebral palsy. Typical firing pattern of vastus lateralis (VLO) and biceps femoris (BF) in an able-bodied athlete (A) in the first 5-sec epoch of the 30-sec Wingate test (nonfatigued state) is shown. Coactivation of the BF and VLO (B) and atypical motor drive of the BF (C) is observed in two participants with cerebral palsy.
found that the AB athletes produce higher power output throughout WIN30 (Fig. 1) but that all other aspects of performance, including FI and muscle activation levels, were similar between groups, providing evidence that athletes with CP can overcome previously documented deficits in performance and neuromuscular activation.
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FI was similar between groups, indicative of a similar decline in power output from peak value, measured at similar time points in CP and AB participants (Fig. 1). Associated mean EMG changed similarly over the trial in all measured musclegroups (Fig. 2). Furthermore, changes in EMG over the trial were similar between the affected
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and nonaffected sides in the CP group and corresponding nondominant and dominant sides in the AB group. The existing literature suggests that individuals with similar forms of CP to the current sample exhibit lower levels of neuromuscular fatigue as a result of suboptimal central drive and the consequent inability to produce enough isokinetic torque to create fatigue.5,25,26 This has been attributed to multiple factors including spasticity, coactivation, type I muscle fiber predominance, and weakness.27Y30 This study’s data suggest that despite weakness, demonstrated by lower power outputs in the Wingate test (10.4 [0.5] W/kg and 9.8 [0.5] W/kg for the AB and CP groups, respectively; P G 0.05), the associated lower neuromuscular fatigue shown by literature was not present in this elite athletic sample. This was demonstrated by the similarity in FI and progressive decrease in EMG activity over the trial between the AB and CP groups in all five muscles tested (P G 0.05). It is interesting to speculate whether these results may be the effect of long-term, high-level athletic training. Research to date that shows deficits in performance and flattened fatigue profiles in CP has been performed on sedentary children.31 However, marked changes in muscular adaptation have been observed with exercise training in these samples, making it clear that there is capacity to significantly improve exercise performance and functional capacity.10Y12 The current sample of elite-level athletes may represent a group of individuals with CP who have reached near-maximal muscular adaptation, including the possible movement away from type I muscle fiber predominance muscular weakness. This may explain the similar fatigue profiles seen between groups (FI of 27% [6.9%] and 25% [7.3%] for the AB and CP groups, respectively; Fig. 1) and a greater peak power output achieved in the CP group compared with previously published power values for soccer and cycling nonelite athletes with CP (9.8 vs. 8.3 W/kg).16 Frequency analysis of the EMG signal further supports that the CP and AB groups fatigued similarly, as frequency shifts were similar between the groups. The observed changes, a shift from higher to lower frequencies, are typical of a shift from type II muscle fiber activation to type I fiber activation because of fatigue of the fast-twitch power-producing fibers.32 The similarity in frequency decline in both the CP and AB groups may further support the hypotheses of (1) a higher proportion of and (2) a higher use of type II muscle fibers in this sample of elite athletes with CP.32,33 A significantly greater reduction in www.ajpmr.com
frequency occurred in the CP group’s affected side VLO (the primary power producing muscle), further suggesting the utilization of type II muscle fibers. It may be argued that the similarities in physiology observed between the groups may be the result of a sample of athletes in classes T37 and T38, representing a group of individuals with milder forms of CP. The authors believe that this is not the primary origin of the results of the present study, as they only refer to previous studies conducted using individuals in Gross Motor Function Classification System levels 1 to 3, which are comparable with the level of impairment in the current sample of athletes with CP. The possibility of this contributing factor, however, cannot be disregarded. The second important finding was the presence of neuromuscular irregularities identified in the athletes with CP that are associated with CP, in both stabilizing (ES muscles, Fig. 3) and power (VLO and BF muscles, Fig. 4) muscles, despite the similar response to fatigue to AB athletes. Figure 3 shows coactivation of both ES muscles on the nonaffected side’s pedal stroke and complete lack of activation on the affected side’s pedal stroke of an athlete with CP (Fig. 3B). The existing theory on the role of the stabilizing ES muscles during locomotion is that the ES muscles bilaterally coactivate with heel strike/pedal stroke to counteract unwanted trunk movement.34,35 They also, in conjunction with other lower back muscles, balance external loads to decrease forces on the spine, which, when disrupted, leads to injury.36,37 Thus, the lack of firing on the CP’s affected side may impair the stability required for that side’s pedal stroke and predispose this athlete to injury. Furthermore, neuromuscular irregularities in power muscles (Fig. 4) may have an impact on injury incidence, as well as overall performance.38,39 Figure 4A demonstrates typical BF and VLO activity in an AB participant. VLO and BF are active in a reciprocal manner, ensuring that the application of downward force to the pedal is timed appropriately during the upstroke. Figure 4B demonstrates coactivation of the agonist (VLO) and antagonist (BF) muscles on the affected side, with a lack of activation on the nonaffected side, where it is also required for correct pedal power production. van Ingen Schenau et al.40 concluded that biarticular muscles, including the BF, were involved in the control of the direction of force application on the pedal during cycling; therefore, coactivation may produce counteracting torques on each pedal stroke. That is, the BF may fire on the downward portion of the pedal stroke, essentially exerting opposite forces Exercise Performance Comparison Between Athletes
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to the VLO, which would result in both forces being exerted on the pedal simultaneously with a consequent loss of economy. The observed coactivation of this antagonist pair, however, may also be an activation strategy required for increased joint stability on the affected side, by equalizing articular movement and pressure during force application.41Y43 Furthermore Figure 4C displays continuous activation of BF muscles of both the affected and nonaffected legs despite typical firing patterns of the VLO muscle, indicating an atypical motor drive.4 The complete lack of coherent firing patterns may lead to a lack of coordinated power production for both the affected and nonaffected sides, which would result in a reduction in power output. There may also be an increased risk of injury owing to compensation by the antagonist muscle groups, which has been shown to be a major risk factor for muscle injuries in runners.44,45 This descriptive study has identified interesting findings in an unstudied sample, but with certain limitations. This study was unable to obtain strokeby-stroke bilateral power output on the cycle ergometer, a measurement that would have proved very useful in identifying neuromuscular differences between sides. The use of M-wave stimulation would have also allowed for absolute amplitude EMG activation comparisons between sides and is advised for future studies in this area. Finally, it would have been ideal to be able to conduct fiber typing via biopsy in the athletes, which would support this study’s hypothesis, but the expensive and invasive nature of the test needs to be taken into consideration. Future studies in this area may elucidate mechanisms for the findings of the current study. Future studies are also required during running exercise, applicable to the athletes involved. The present study described performance and neuromuscular characteristics of elite athletes with CP during maximal sprint cycling. The similarity in power output FI as well as neuromuscular fatigue between the CP and AB groups indicates that the current sample of elite athletes with CP may have a different physiology from the previously studied untrained individuals with CP. The authors propose that this movement toward AB levels may be a result of high-level training over many years. This may have both empirical and clinical application, as it may indicate the uppermost ability of the cerebral-palsied body to adapt toward normal levels. If so, these findings have large implications for CP rehabilitation and athletic participation as a form of rehabilitation. Further research, however, is required to either support or refute findings of the current study.
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ACKNOWLEDGMENTS
We thank the athletes for their time and the Sport Physiology Laboratory, Department of Sport Science, Stellenbosch University, for their assistance. REFERENCES 1. Bialik GM, Givon U: Cerebral palsy: Classification and etiology. Acta Orthop Traumatol Turc 2009;43:77Y80 2. Johnston MV, Hoon AH Jr: Cerebral palsy. Neuromolecular Med 2006;8:435Y50 3. Reddihough DS, Collins KJ: The epidemiology and causes of cerebral palsy. Aust J Physiother 2003; 49:7Y12 4. Rose J, McGill KC: Neuromuscular activation and motor-unit firing characteristics in cerebral palsy. Dev Med Child Neurol 2005;47:329Y36 5. Stackhouse SK, Binder-Macleod SA, Lee SC: Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve 2005;31:594Y601 6. Verschuren O, Bloemen M, Kruitwagen C, et al: Reference values for anaerobic performance and agility in ambulatory children and adolescents with cerebral palsy. Dev Med Child Neurol 2010;52:e222Y8 7. Bar-Or O: The Wingate anaerobic test. An update on methodology, reliability and validity. Sports Med 1987;4:381Y94 8. Parker DF, Carriere L, Hebestreit H, et al: Anaerobic endurance and peak muscle power in children with spastic cerebral palsy. Am J Dis Child 1992;146: 1069Y73 9. Verschuren O, Takken T: Aerobic capacity in children and adolescents with cerebral palsy. Res Dev Disabil 2010;31:1352Y7 10. Reid S, Hamer P, Alderson J, et al: Neuromuscular adaptations to eccentric strength training in children and adolescents with cerebral palsy. Dev Med Child Neurol 2010;52:358Y63 11. MacPhail HE, Kramer JF: Effect of isokinetic strengthtraining on functional ability and walking efficiency in adolescents with cerebral palsy. Dev Med Child Neurol 1995;37:763Y75 12. Verschuren O, Ketelaar M, Gorter JW, et al: Exercise training program in children and adolescents with cerebral palsy: A randomized controlled trial. Arch Pediatr Adolesc Med 2007;161:1075Y81 13. Tweedy SM: International Paralympic Committee Athletics Classification Project for Physical Impairments: Final Report-Stage 1. July;1.2(2010/07/16). Available at: http://www.paralympic.org/Athletics/RulesandRegulations/ Classification. Accessed November 15, 2012. 14. Morris C: Development of the gross motor function classification system (1997). Dev Med Child Neurol 2008;50:5 15. Astorino TA, Cottrell T: Reliability and validity of the Velotron Racermate Cycle Ergometer to measure anaerobic power. Int J Sports Med 2012;33:205Y10
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