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Muchaxo, R., De Groot, S., Kouwijzer, I., Van Der Woude, L., Janssen, T. et al. (2021) A Role for Trunk Function in Elite Recumbent Handcycling Performance? Journal of Sports Sciences https://doi.org/10.1080/02640414.2021.1930684

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A Role for Trunk Function in Elite Recumbent Handcycling Performance?

Rafael Muchaxo, Sonja De Groot, Ingrid Kouwijzer, Lucas Van Der Woude, Thomas Janssen & Carla F.J. Nooijen

To cite this article: Rafael Muchaxo, Sonja De Groot, Ingrid Kouwijzer, Lucas Van Der Woude, Thomas Janssen & Carla F.J. Nooijen (2021): A Role for Trunk Function in Elite Recumbent Handcycling Performance?, Journal of Sports Sciences, DOI: 10.1080/02640414.2021.1930684 To link to this article: https://doi.org/10.1080/02640414.2021.1930684

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Published online: 03 Jun 2021.

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Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=rjsp20 JOURNAL OF SPORTS SCIENCES https://doi.org/10.1080/02640414.2021.1930684

SPORTS PERFORMANCE A Role for Trunk Function in Elite Recumbent Handcycling Performance? Rafael Muchaxo a,b, Sonja De Groot a,b,c, Ingrid Kouwijzer b,d,e, Lucas Van Der Woude e,f,g, Thomas Janssen a,b,c and Carla F.J. Nooijen h aFaculty of Behavioural and Human Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands; bAmsterdam Rehabilitation Research Center, Amsterdam, The Netherlands; cCenter for Adapted Sports Amsterdam, Amsterdam Institute of Sport Science, Amsterdam, The Netherlands; dResearch and Development, Heliomare Rehabilitation Center, Wijk Aan Zee, The Netherlands; eUniversity of Groningen, University Medical Center Groningen, Center for Human Movement Sciences, Groningen, The Netherlands; fUniversity of Groningen, University Medical Center Groningen, Center for Rehabilitation, Groningen, The Netherlands; gLoughborough University, School of Sports, Exercise & Health, Peter Harrison Centre of Disability Sport; hSwedish School of Sport and Health Science (GIH), Stockholm, Sweden

ABSTRACT ARTICLE HISTORY Handcycling classification considers trunk function, but there is limited scientific evidence of trunk Accepted 12 May 2021 involvement in recumbent performance. This study investigated the association between trunk function KEYWORDS and recumbent handcycling performance of athletes without upper-limb impairments (H3- sport Para-cycling; paralympic classes). The study was divided into two parts. First, 528 time-trial results from 81 handcyclists with spinal classification; trunk strength; cord injury (SCI) were obtained between 2014 and 2020. Average time-trial velocity was used as average velocity; time trial; performance measure and SCI level as trunk function determinant. Multilevel regression analysis was sprint test performed to analyse differences in performance among SCI groups while correcting for lesion comple­ teness, sex, and age. Second, in 26 handcyclists, standardised trunk flexion strength was measured with a handheld dynamometer. Peak and mean power-output from a sprint test and time-trial average velocity were used as performance measures. Spearman correlations were conducted to investigate the association between trunk strength and performance. Results showed that the different SCI groups did not exhibit significant differences in performance. Furthermore, trunk flexion strength and perfor­ mance exhibited non-significant weak to moderate correlations (for time-trial speed: rs = 0.36; p = 0.07). Results of both analyses suggest that trunk flexion strength does not seem to significantly impact recumbent handcycling performance in athletes without upper-limb impairments.

Introduction Handcycling is governed by the Union Cycliste Handcycling use varies from rehabilitation programmes, to Internationale (UCI) and its classification is based on a mode of transportation, recreational sport and elite competi­ a hierarchical system of five sport classes (-) since 2014. tion (Hettinga et al., 2010). Handcycling has been a Paralympic The H1-H4 classes compete in an arm-powered handbike in sport since 2004 with more than 680 international athletes a recumbent position, with athletes in class H1 representing the worldwide (Union Cycliste Internationale, 2020a). Handcyclists athletes with the greatest impairments, e.g., athletes with compete in two outdoor racing events, namely road races and lower-limb, trunk, and upper-limb impairments (Union time-trials. Road race events range from 37 km to 70 km for Cycliste Internationale, 2020b). In contrast to the H1–H4 classes, women, and from 45 km to 80 km for men. Time-trial events the H5 class competes in an arm-trunk powered handbike in range from 10 km to 30 km for women, and from 12 km to a kneeling position and represents athletes with the least 35 km for men (Union Cycliste Internationale, 2020b). As impairments. These sports class profiles are described in a Paralympic sport, handcycling must comply with the a classification manual (Union Cycliste Internationale, 2020b), International Paralympic Committee (IPC) Athlete historically centred on people with spinal cord injury (SCI) as Classification Code, where it is stated that all Paralympic sports a reference of the functional limitation for comparison with must be centred on evidence-based classification systems other impairments. By comparing these class profiles, it is designed to minimise the impact of impairment on the perfor­ possible to identify the main physical determinants that char­ ; mance (International Paralympic Committee, 2015 Tweedy & acterise each one of them. In summary, the main characteristic Vanlandewijck, 2011). By minimising the impact of impairment, that divides H1 and is arm strength, H2 and H3 is hand differences in performance between athletes from the same strength and trunk function (no vs. minimal to limited), and H3 class are likely to be a result of genetic predisposition, talent and H4 is trunk strength. H5 differs from H4 on full trunk and and training intervention. From this classification perspective, hip-leg function plus the ability to compete in an arm-trunk athletes who augment their performance will not be disadvan­ powered handbike (Union Cycliste Internationale, 2020b). taged by being moved towards a less impaired class or vice- The involvement of the trunk in sports performance has versa (Tweedy & Vanlandewijck, 2011). received general interest from a diverse range of Paralympic

CONTACT Rafael Muchaxo [email protected];[email protected] Faculty of Behavioural and Human Movement Sciences, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands © 2021 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way. 2 R. MUCHAXO ET AL. sports over the last two decades. A higher level of SCI has been function (based on SCI level) is related to performance, using associated with decreased trunk active range of motion, slower a retrospective design. The second analysis aimed to investi­ postural reactions and lower acceleration in para-sports such as gate the association between trunk flexion strength and hand­ sit-skiing, wheelchair athletics and wheelchair rugby, with dif­ cycling performance, based on a cross-sectional cohort design. ferences being smaller when comparing individuals with partial It was hypothesised that 1) different levels of trunk function do to full trunk function (Altmann et al., 2016, 2017; Connick et al., not present significant differences in recumbent handcycling 2017; Rosso et al., 2019; Vanlandewijck, Verellen, Beckman et al., performance, and 2) that trunk flexion strength is only weakly 2011; Vanlandewijck, Verellen, Tweedy et al., 2011). These to moderately associated with recumbent handcycling sports suggest a direct trunk influence on performance given performance. the upright position, e.g., balance in sit skiing and wheelchair manoeuverability in wheelchair rugby. In the case of a recumbent aerodynamic position as H1–H4 handcycling posi­ Materials and methods tion (Mannion et al., 2018), research on the influence of trunk Design impairment is scarce. Recumbent positions with an upright backrest may evoke a higher contribution of the trunk muscles Two complementary analyses were conducted to investigate (Faupin et al., 2008; Van Der Woude et al., 2000) including a low the association between trunk function and recumbent hand­ activation of the upper abdominal (Quittmann et al., 2019) cycling performance. In the first analysis, 528 time-trial results when compared with more aerodynamic positions. However, of 81 athletes were grouped according to SCI level and multi­ these recumbent positions seem to evoke small trunk move­ level regression analyses were performed to investigate the ment in the sagittal, frontal and transverse planes (Faupin et al., influenceof lesion level on performance. In the second analysis, 2006; Quittmann et al., 2018; Stone, Mason, Warner, Goosey- correlation coefficients were calculated between trunk flexion Tolfrey et al., 2019; Stone, Mason, Warner, Tolfrey et al., 2019; strength and measures of handcycling performance (time-trial Verellen et al., 2012a) as it was observed in able-bodied, H3 and average velocity and isokinetic sprint test) from a sample of 29 H4 athletes. The small trunk movement was maintained athletes. throughout different intensities, and inter-individual variations decreased with increasing intensity among elite handcycling SCI level & handcycling performance athletes (Stone, Mason, Warner, Goosey-Tolfrey et al., 2019; Stone, Mason, Warner, Tolfrey et al., 2019). Participants The significance of trunk involvement in recumbent hand­ Eighty-one elite handcycling athletes from H3 and H4 sport cycling appears questionable, especially considering highly classes (64 males, 17 females) with SCI were included in this trained athletes. To the best of our knowledge, the only study study after providing written informed consent to share their investigating the direct association between SCI level and para-cycling classification data. All athletes were competing at handcycling focused on force generation patterns and effec­ world cups and world championships. The research was tiveness, and did not find significant differences among groups approved by the Scientific and Ethical Review Board of the of athletes with different SCI levels (Verellen et al., 2012b). Faculty of Behavioural and Movement Sciences, Vrije However, according to the current para-cycling classification Universiteit Amsterdam, the Netherlands, No: VCWE-2018-093. manual, athletes with impaired muscle strength are allocated to H3 and H4 classes mainly based on trunk muscle strength Experimental protocol and with SCI levels as a reference (Union Cycliste Internationale, Demographic information regarding age, sex and event dis­ 2020b). There is evidence of the negative impact that higher tance and location was available from the official UCI website. lesion levels have on cardiovascular parameters, and conse­ Information regarding the athlete’s para-cycling classification quently on endurance sports performance, as a result of an and impairment characteristics was provided by the UCI. Based impaired autonomic nervous system (ANS) (West et al., 2015, on muscle function and muscle innervation (Beaussier, 2013; 2014). This impact is predominant in athletes with autonomic McErlean & Migliozzi, 2017; Rozen et al., 2008; Sakamoto et al., complete cervical lesions, but athletes with high thoracic SCI 1996), participants were assigned to one of the four groups may as well present an impaired ANS (West et al., 2015, 2014). regarding their SCI level: Th1–Th5, including high thoracic However, in accordance with the IPC Athlete Classification lesions, from Th1 to Th5 lesion level, possibly affecting the Code (International Paralympic Committee, 2015; Tweedy & chest wall and below, and the sympathetic cardiac innervation; Vanlandewijck, 2011) such physiological parameters are not Th6-Th9, injuries affecting the upper abdominal wall and taken into account during Paralympic classification. As there is defined as lesions from levels Th6 to Th9; Th10–L1, injuries no scientific evidence of the association between trunk affecting the lower abdominal wall and defined as lesions strength and recumbent handcycling performance, the current from levels Th10 to L1; and last, ≤L2, lesions from L2 down classification system does not follow an evidence-based per­ which do not affect the trunk muscles. spective as advocated by IPC. The completeness of their lesion was based on the ASIA The main aim of this study was to investigate the association impairment scale (AIS), i.e., motor complete (AIS A-B) versus between trunk function and recumbent handcycling perfor­ motor incomplete (AIS C-D). mance in athletes from the H3 and H4 sport classes. To study The official handcycling time-trial results from 2014 to 2020 this aim, two complementary analyses were performed. The of each athlete were obtained retrospectively from the UCI’s first analysis aimed to investigate whether handcyclists’ trunk website (Union Cycliste Internationale, 2020c) for 24 events, JOURNAL OF SPORTS SCIENCES 3

Table 1. Number of time-trial results included in the analysis per sex and spinal age = 38 ± 9 years, body mass = 61 ± 12 kg) competing at the cord injury level group. 2018 Para-cycling Road World Cup (Emmen, the Netherlands) Time trials and at the 2018 Para-cycling Road World Championships Women Men Total (Maniago, Italy) volunteered to participate in this study. AIS AIS AIS AIS Initially, all participants registered for the competition event SCI level A/ C/ A/ C/ groups Agea Bb Dc Total Agea Bb Dc Total received an email from the UCI with the information letter of Th1–Th5 41 ± 10 17 0 17 42 ± 12 94 2 96 113 the respective study. Participants had to fulfil the following (high inclusion criteria: 1) internationally classified in one of the thoracic) existing handcycling sport classes; 2) registered for the time- Th6–Th9 (upper trial competition of the respective event; 3) no upper-limb abdominals) 33 ± 2 2 19 21 35 ± 6 79 16 95 119 impairments; 4) no health condition or active medical treat­ Th10–L1 (lower ment that could influence the testing outcomes; 5) being abdominals) 40 ± 11 84 3 87 40 ± 5 132 57 189 277 ≥18 years of age. When interested, participants could schedule ≤L2 (full 26 ± 3 4 5 9 33 ± 11 0 10 10 19 trunk) a meeting with the researcher for more information and if they Total 107 27 134 305 85 390 524d maintained the will to participate they had to sign an active aAveraged age and standard deviation of the group informed consent prior to the measurement session. From the b AIS A or B, equivalent to complete motor lesion 29 athletes registered, three male participants did not perform cAIS C or D, equivalent to incomplete motor lesion dThere are 4 additional participants not included in this table due to missing data the time-trial and were excluded from this analysis, leading to regarding AIS. The total sample is representative of 81 unique handcycling a sample of 26 athletes. Four male and two female participants athletes (64 males, 17 females). did not perform the isokinetic sprint test and were excluded, leading to a sample of 23 athletes for this particular analysis. The research was approved by the Scientific and Ethical Review resulting in a total of 528 time-trial results from 81 athletes Board of the Faculty of Behavioural and Movement Sciences, (Table 1). As a key measure of handcycling performance, aver­ Vrije Universiteit Amsterdam, the Netherlands, No: VCWE- age time-trial velocity (m/s) was calculated by dividing the 2018-093. time-trial results by the race distance, following a previously described procedure (Muchaxo et al., 2020). Experimental protocol Prior to testing in the field-lab, i.e., a standardised lab setting Statistical analysis that was arranged at the competition venue, participants were Statistical analyses were performed using R software (version interviewed regarding demographic information, sport experi­ 3.6.3). All data were visually inspected for the presence of out­ ence and health conditions, including impairment characteris­ liers. Following Tukey’s method (Komorowski et al., 2016), out­ tics. Each participant performed a set of two different liers were first identified based on the interquartile range (IQR), measurements in the following order: 1) a Trunk Flexion with outliers defined as 1.5 times the IQR below or above the Handheld-dynamometer Test and 2) a 20-sec Isokinetic Sprint first or the third quartile, respectively. Afterwards, the identified Test. outliers were individually analysed and processed according to Trunk flexion strength was assessed with the use of a previously described analysis (Muchaxo et al., 2020). a handheld dynamometer (MicroFET2 Digital Handheld Multilevel analyses (fixed effect) were conducted to assess Dynamometer, HOGGAN Scientific, USA.) (Figure 1), with the differences in average time-trial velocity among the four SCI participant supine in a semi-recumbent position on an exam­ groups of athletes. The SCI groups were dummy coded and ination table. The participant sat against a rigid backrest with three different models were built with the groups Th1–Th5, a 55-degree angle with the horizontal and the legs extended Th6–Th9, and Th10–L1 as reference (1). All models were and strapped with an adjustable Velcro belt to the table at adjusted for sex, age, distance, and motor completeness of thigh level. The dynamometer was placed at and perpendicular the SCI. Potential systematic differences among events and to the sternum. The participant was asked to perform athlete’s repeated measures were taken into account by build­ a maximal voluntary contraction by executing trunk flexion ing a two-level model with events as the first level and athletes during a “make” procedure, i.e., while the examiner provided as the second level. Significance level was set at α = 0.05, and a stable resistance (Figure 1). During the test, the hands of the effectsizes were calculated as Cohen’s d with the following cut- participant rested on the legs and the participant was offs: d < 0.01 for a trivial effect; 0.01 ≤ d < 0.2 for a very small; instructed to gradually increase the force exerted against the 0.2 ≤ d < 0.6 for small; 0.6 ≤ d < 1.2 for moderate; 1.2 ≤ d < 2.0 dynamometer without actively using the limbs. Following for large; and d ≥ 2.0 for a very large effect (Hopkings, 2002). a familiarisation trial, each participant performed four testing trials where maximal force was collected. When the trial was not performed correctly, an additional trial was performed. The Trunk flexion strength and handcycling performance maximal force (N) of four correct trials was averaged and used Participants as trunk flexion strength outcome for further analysis. Twenty-nine elite recumbent handcycling athletes from H3 and The second measurement was a 20-sec isokinetic all-out H4 sport classes (26 athletes with impaired muscle power and handcycle sprint test as a measure of handcycling performance three athletes with lower-limb deficiency; H3: (n = 17), in a controlled test setting. The participant’s handbike was age = 37 ± 9 years, body mass = 64 ± 11 kg; H4: (n = 12), attached to a cycle ergometer (Cyclus 2, RBM Electronics, 4 R. MUCHAXO ET AL.

Figure 1. Handheld dynamometer device (MicroFET2 ProCare) (left), and position of the athlete during trunk flexion test (right).

Leipzig, Germany) and the test started with a 5-min warm up at (52%; n = 277), had an SCI at the level of the lower abdominal a self-selected power output, followed by a 2-min rest. Adapted wall (Th10–L1 group) and only 4% (n = 19) had an injury of L2 or from Zeller et al. (2015) (Zeller et al., 2015), the 20-s isokinetic below (≤L2 group) sprint test started with an initial load of 20 N and had a cadence Table 2 presents the multilevel regression results regarding limitation of 130 rotations per minute. The highest power out­ differences in average time-trial velocity between SCI level put (POpeak (W)) and mean power output (POmean (W)) were groups after correction for age, sex and lesion completeness. determined after the 20-sec sprint test and used as outcome Results showed that the different lesion level groups did not measures of handcycling performance. exhibit significant differences in handcycling performance In addition, official time-trial results of the respective events (p > 0.05). In addition, all the comparisons exhibited very were collected from the UCI’s website (Union Cycliste small effect sizes (d < 0.2). However, in this sample the Th10– Internationale, 2020c) and average velocity (m/s) was calcu­ L1 group tended (p = 0.051) to have a higher velocity than the lated (1) and used as a measure of handcycling performance ≤L2 group, despite the minimal effect size (d = 0.11). in a field setting. À � À 1 Time trial=; average=; velocity ms Trunk flexion strength and handcycling performance DistanceðmÞ (1) ¼ In this athlete sample (n = 29) from two time-trial events, 25% Time=; of=; completionðmm : ss : msÞ � 24 � 60 � 60 (n = 7) were female, and 59% (n = 17) were classified as H3. Participants from the H3 sport class presented values of trunk flexion strength ranging from 0 N to 71 N (median = 37 N), Statistical analysis whereas participants from H4 sport class presented values from Statistical analyses were performed using R software (version 56 N to 344 N (median = 113 N). The medians of POpeak and 3.6.3). Prior to the analysis of the association between trunk POmean for H3 participants were 453 W and 358 W, respec­ flexion strength and handcycling performance, all data were tively, and 435 W and 361 W for H4 participants. During the visually inspected, tested for normality using the Shapiro–Wilk time-trial, median average velocity for H3 participants was test, and an α level of 0.05 was set. Data were not normally 9.4 m/s (33.9 Km/h), ranging from 6.2 m/s to 10.6 m/s (22.2–­ distributed; therefore, Spearman correlation coefficients were 38.1 Km/h), and for H4 participants was 10 m/s (35.9 Km/h), calculated between trunk flexion strength and the handcycling with a range between 7.3 m/s and 11.7 m/s (26.4–42.2 Km/h). performance outcomes, i.e., peak PO, mean PO, and average The scatterplot (Figure 2) displays trunk flexion strength time-trial velocity. Correlation coefficients were considered: versus average time-trial velocity for male/female and H3/H4 very small for rs<0.1; small for 0.1≤rs<0.3, moderate for classes. Spearman’s correlation coefficients between trunk flex­ 0.3≤rs<05, large for 0.5≤rs<0.7 and very large for ion strength and average time-trial velocity showed a non- rs≥0.7(Hopkings,2002). significant moderate association (rs = 0.36; p = 0.07). In addi­ tion, trunk flexion strength showed non-significant small to Results moderate associations with POmean (W) (rs = 0.31; p = 0.15) and POpeak(W) (rs = 0.27; p = 0.22) (Figure 3). SCI level & handcycling performance Table 1 describes the number of time-trial results included in Discussion the multilevel regression model, based on SCI level group and sex. From the time-trial results sample (n = 528), 26% (n = 135) The current study presents two research approaches to inves­ was from female athletes, and 21% (n = 112) was from athletes tigate the influence of trunk function on recumbent handcy­ who had a motor incomplete lesion. The majority of athletes cling performance. We retrospectively investigated the JOURNAL OF SPORTS SCIENCES 5

Table 2. Multilevel models (Levels: Event and Athlete) assessing the differences in average time-trial velocity among pairs of SCI groups, with Th1–Th5, Th6– Th9 and Th10–L1 as a reference after controlling for age, sex (male = 1; female = 0), and AIS differences (AIS A/B = 1; AIS C/D = 0). Β = unstandardised beta values; SE = standard error; CI = confidence interval. Model with Th1–Th5 as reference Fixed effect β SE CI (95%) z-value p-value Cohen’s d Constant 7.96 0.62 [6.75; 9.17] 12.91 < 0.00001 Th1–Th5:Th6–Th9 0.11 0.32 [−0.51; 0.73] 0.35 0.73 0.02 Th1–Th5:Th10–L1 0.49 0.30 [−0.09; 1.08] 1.66 0.10 0.08 Th1–Th5:≤L2 −0.51 0.56 [−1.60; 0.59] −0.91 0.36 0.08 Model with Th6–Th9 as reference Fixed effect β SE CI (95%) z-value p-value Cohen’s d Constant 8.07 0.58 [6.94; 9.21] 13.97 < 0.00001 Th6–Th9:Th1–Th5 −0.11 0.32 [−0.73; 0.51] −0.35 0.73 0.02 Th6–Th9:Th10–L1 0.38 0.28 [−0.17; 0.94] 1.36 0.17 0.07 Th6–Th9:≤L2 −0.62 0.53 [−1.66; 0.42] −1.16 0.25 0.10 Model with Th10–L1 as reference Fixed effect β SE CI (95%) z-value p-value Cohen’s d Constant 8.46 0.57 [7.34; 9.57] 14.91 < 0.00001 Th10–L1:Th1–Th5 −0.49 0.30 [−1.08; 0.09] −1.66 0.10 0.08 Th10–L1:Th6–Th9 −0.38 0.28 [−0.94; 0.17] −1.36 0.17 0.07 Th10–L1:≤L2 −1.00 0.51 [−2.00; 0] −1.95 0.051 0.11 Variables Controlleda Parameter β SE CI (95%) z-value p-value Sex 1.00 0.28 [0.46; 1.55] 3.60 0.0003 Age 0.003 0.01 [−0.02; 0.03] 0.23 0.82 AIS (motor function) −0.36 0.31 [−0.96; 0.25] −1.16 0.25 aThe values from the controlled variables did not change between models and therefore are presented separately for an easier visualization.

Figure 2. Scatterplot of trunk flexion strength and average time-trial velocity. Data points are identified by sex and by handcycling class. (H3: spinal cord injury with lesion levels between Th1 and Th10; H4 lesion levels below Th11 or amputations).

association between the handcyclists’ level of SCI and handcy­ their SCI level, were not significant in the sports classes inves­ cling performance in a sample of international H3/H4 elite tigated. Our findings corroborate earlier para-sport research handcyclists (n = 81). In addition, a cross-sectional experimental that found only small differences in trunk performance approach focussed on the association between trunk flexion between athletes with different levels of trunk function, e.g., strength and handcycling performance in (n = 29) international in wheelchair racing (Vanlandewijck, Verellen, Beckman et al., elite H3/H4 athletes. The findings of both research approaches 2011), although in our handcycling study, as a significant dis­ suggested that trunk function does not play a major role in tinct discipline, the influence of trunk function is even less recumbent time trial handcycling performance. prominent. The lack of differences among the trunk function groups H3/H4 is in line with previous research that suggested no differences regarding handcycling force effectiveness SCI level & handcycling performance between individuals with different paraplegia levels (Verellen As hypothesised, differences in average time-trial velocity et al., 2012b). Verellen et al. (2012) found that handcyclists with between athletes with more or less trunk function, based on a high thoracic SCI (Th1–Th8), i.e., with lack of trunk strength 6 R. MUCHAXO ET AL.

Figure 3. Scatterplots of trunk flexion strength and handcycling performance during a 20-sec isokinetic sprint: Mean PO (upper graph) and Peak PO (lower graph). data points are identified by sex and by handcycling class. (H3: spinal cord injury with lesion levels between Th1 and Th10; H4 lesion levels below Th11 or amputations). but no upper-limb impairments, presented values of fraction of demonstrated comparable performance, with minimal effect effective force during recumbent handcycling comparable to sizes, even when compared to groups with greater discrepancy handcyclists with low thoracic SCI (below Th10), i.e., who have regarding trunk function. Such findings may contribute to dif­ partial to full trunk strength (Verellen et al., 2012b). This is ferent assumptions: a) that impaired trunk function and/or particularly evident when comparing our Th1–Th5 group, impaired ANS, among high thoracic SCI, presents limited influ­ which included athletes with minimal trunk function, with ence on time-trial handcycling performance; b) that the sample groups with lower SCI levels. The non-significant differences may reflect a greater absence of athletes with impaired ANS and negligible effect sizes indicates comparable performance competing at an elite level because they will not make it to this across all groups. level. The influence of an impaired ANS varies among high Given the large aerobic component of a handcycling race thoracic SCI (Krassioukov & West, 2014), but literature has (Finch & Baggish, 2016), athletes with lesion levels above Th6 shown a general negative impact on sport performance, with might have a disadvantage due to a possible impaired emphasis on sports with greater demand for aerobic exercise response of the ANS to exercise (Krassioukov & West, 2014; capacity, like handcycling (West et al., 2015). However, it should Theisen, 2012; West et al., 2015). Reduced cardiac output and be noted that previous research has shown limited association deficient thermoregulation may eventually affect the perfor­ between motor/sensory completeness of the lesion and auto­ mance outcome (Krassioukov & West, 2014; Theisen, 2012; West nomic completeness (West et al., 2015). Although the results et al., 2015). However, in the present study, the group Th1–Th5 may suggest an underrepresentation of these athletes, we do JOURNAL OF SPORTS SCIENCES 7 not have sufficient data to verify the ANS assumption solely low in able-bodied participants performing recumbent hand­ based on the motor completeness of the lesion and additional cycling, and expected to be lower in elite athletes with SCI measurements to verify this are recommendable. (Quittmann et al., 2019), as the upper limbs are mainly respon­ Previous evidence has shown that the lesion level, includ­ sible for force generation and steering (Verellen et al., 2012). ing tetraplegia and paraplegia, may be a good predictor of Hence, it could be hypothesised that between H4 and H3 sports the maximal aerobic power in handcycling (De Groot et al., classes, trunk strength plays a minor role and differences 2019); however, it has also been shown that the level alone between these classes may be less than between and . may not be a good predictor of trunk function (Bjerkefors The findings of the present study are in line with previous et al., 2007). According to the UCI classification, athletes in studies and lead us to assume that the impact of trunk flexion class H3 present impairments corresponding to an SCI strength on performance will be considerably diminished when between Th1 and Th10, while athletes in class H4 present compared to the other para-sport modalities in which a more SCI below Th11 or equivalent (Union Cycliste Internationale, upright position is necessary. In a recent study, stronger rela­ 2020b). The classes are further detailed on the level of trunk tionships between wheelchair racing performance and iso­ stability and abdominal strength, separated by limited to very metric strength were found when combined arm–trunk limited in H3 and normal to almost normal in H4. In the strengths were included as predictors instead of trunk strength current study, we did not assess trunk stability as we do not only (Connick et al., 2017). In our study, trunk flexion strength consider trunk vertical stability to play a major role in was measured in an isolated manner and future research a recumbent position, where athletes are often positioned should focus on the measurement of multiple joints and muscle aerodynamically and strapped to the handbike. The findings functions, such as arm pulling while controlling for trunk posi­ of this first analysis suggest that handcycling athletes with tion. Nevertheless, the same wheelchair racing study has sug­ good upper-limb function exhibit comparable time-trial aver­ gested four different clusters associated with different age velocity at group level despite differences in trunk performance levels. Aside from the clusters that included ath­ function. letes with upper-limb impairments, it was remarkable to observe that the second least impaired cluster included ath­ letes with SCI levels from Th2 to Th12, comprising nearly the Trunk flexion strength and handcycling performance total range of athletes in H3 and H4. Differencesin performance were not observed between these different levels of trunk The findings in our cross-sectional analysis matched our initial function. Instead, differences were found between athletes hypothesis regarding weak to moderate associations between who did and did not have hip–leg connection (Connick et al., trunk flexion strength and handcycling performance. The asso­ 2017). ciation between trunk flexion strength and average time-trial In the present study, the results from the trunk flexion velocity showed a non-significant moderate correlation. strength (second analysis) are in agreement with the results A similar correlation was observed between trunk flexion from SCI level (first analysis), as well as with previous findings strength and PO during the isokinetic sprint test. In this mean on small differences between H3 and H4 time-trial handcy­ controlled test setting, a weaker association was found cling performance (Muchaxo et al., 2020). Although H3 and H4 between trunk flexion strength and PO . peak athletes present differences in trunk function and flexion H3 and H4 class profiles are similar to T53 and T54 from strength, the present study suggests that trunk flexion wheelchair athletics. The classification of these athletes is com­ strength is not an essential determinant of recumbent hand­ parable, as both classes include athletes with partial to full cycling performance in these classes, as similar values for trunk stability (International Paralympic Committee, 2017; average velocity and sprint power-output were found. These Union Cycliste Internationale, 2020b), although it should be results suggest that isolated trunk flexion strength should not noted that the T54 sport class includes a broader range, com­ be included as a discriminative factor in classification,contrary pared to the H4 sport class (Th11 and down). More specifically, to the current trunk perspective of the classification system, T53 includes a range of SCI levels from Th1 to Th7, while T54 which assesses trunk strength as an important method of class includes a broad range of SCI levels corresponding from Th8 allocation. and down (International Paralympic Committee, 2017). In Comparable performance between H3 and H4, i.e., compar­ a previous study, it was shown that athletes classified in T54 able average velocities and sprint power-outputs despite dif­ with different levels of trunk strength do not differ in perfor­ ferences in trunk function and flexionstrength imposes a threat mance based on acceleration test from standstill to the currently used hierarchical classification system. (Vanlandewijck, Verellen, Beckman et al.,2011). In recumbent However, notwithstanding the recent findings on the minor handcycling, elite athletes adopt a laying down aerodynamic involvement of trunk function and flexion strength in recum­ position (Stone, Mason, Bundon et al., 2019), which is expected bent time-trial handcycling performance, the scientific evi­ to reduce the involvement of trunk more than in sitting upright dence does not necessarily support merging of the H3 and H4 positions (Faupin et al., 2006, 2008; Quittmann et al., 2018; classes since other factors may play a role in performance. Stone, Mason, Warner, Goosey-Tolfrey et al., 2019; Stone, Determinants such as the ability to perform an active closed- Mason, Warner, Tolfrey et al., 2019; Verellen et al., 2012a). In chain with the lower limbs (Kouwijzer et al., 2018), combined addition, abdominal muscle activation has been found to be 8 R. MUCHAXO ET AL. joint function, core co-contraction, or impact of strapping may dynamometer has been considered a valid and reliable assess­ play more important roles in determining handcycling perfor­ ment tool for muscle strength in different body segments, mance and should be included in future studies. including trunk flexion (De Blaiser et al., 2018; Febrer et al., 2010; Karthikbabu & Chakrapani, 2017). Limitations Conclusion To investigate associations with a time trial event, which implies a significant endurance component, aerobic measures of perfor­ The involvement of the trunk in Paralympic sports is complex, mance capability could be used or maybe even preferred (Van and trunk function is not solely explained by trunk flexion Der Zwaard et al., 2018). For example, literature suggests signifi­ strength and lesion level. However, based on the two analyses cant strong correlations between peak aerobic PO (W) and hand­ conducted in this study, it can be concluded that trunk function cycling performance (Lovell et al., 2012; Stone et al., 2020). and flexion strength seem to have a minor impact on recum­ Correlations between endurance events and anaerobic measures bent handcycling time-trial performance of elite H3/H4 ath­ of performance might be less strong (Van Der Zwaard et al., 2018). letes. The first analysis showed that handcycling performance However Janssen et al. (1993) and De Groot et al. (2021) (De Groot was not significantly different among groups based on SCI et al., 2019) found strong associations between sprint PO and level. These findings were supported by the second analysis, peak aerobic capacity (oxygen uptake and aerobic POpeak) in where only non-significantsmall to moderate associations were individuals with SCI during wheelchair propulsion and arm crank­ found between trunk flexion strength and handcycling perfor­ ing, respectively. De Groot et al. (2012) (De Groot et al., 2012) mance. While generalisation of these findings should be found that individuals with neurological impairment presented addressed with caution, the insights of this study exposed the strong associations between sprint PO and oxygen uptake and need to pursue evidence-based research on other potential aerobic POpeak. Quittmann et al. (2018) showed strong associa­ determinants of handcycling performance that should be con­ tions between sprint PO and lactic power and Nooijen et al. sidered for the classification system. (Nooijen et al., 2021) found a significant association (r2= 0.61) between the 20-sec isokinetic PO and time-trial average velo­ mean Disclosure of potential conflicts of interest city in elite handcycling athletes competing at world cups and world championships. No potential conflict of interest was reported by the author(s). A limitation of the present study is the sample size. While in the first analysis a relatively large sample was used, the size of the most functional group is small and may influence the Funding comparison with the other groups. Although undesirable, this This project has been carried out with the support of UCI (Union Cycliste is a reflection of the competition, as athletes with hip–leg Internationale). The funding body was not involved in decisions concerning connection are distributed among recumbent and kneeling the design of this study, data analysis, interpretation of data or in reporting handbikes (H4 and H5 classes), dependent on additional func­ and publishing this project. tional characteristics. Similarly, in the second analysis, it was not possible to include a larger sample, despite the fact that the ORCID participants were elite athletes tested on-site at the World Cup and the World Championships. Research at events is often Rafael Muchaxo http://orcid.org/0000-0002-1796-2818 Sonja De Groot http://orcid.org/0000-0001-8463-2563 complicated by the obligations of the event for the athlete, Ingrid Kouwijzer http://orcid.org/0000-0003-1012-3509 while otherwise elite handcyclists are difficult to reach world­ Lucas Van Der Woude http://orcid.org/0000-0002-8472-334X wide in a standardised experimental protocol. Thomas Janssen http://orcid.org/0000-0001-6762-131X The assumptions made from the multilevel regression ana­ Carla F.J. Nooijen http://orcid.org/0000-0003-0146-9292 lysis may be limited due to the absence of data regarding the athlete’s fitness level. However, we do not have reasons to References believe there is a significant discrepancy in the number of unfit athletes between H3 and H4 classes, which composed Altmann, V. C., Groen, B. E., Groenen, K. H., Vanlandewijck, Y. C., Van Limbeek, J., & Keijsers, N. L. (2016). Construct validity of the trunk the SCI groups included in this analysis. In addition, there was impairment classification system in relation to objective measures of no information on whether the response of the ANS to exercise trunk impairment. Archives of Physical Medicine and Rehabilitation, 97(3), was limited in the athletes. Finally, rigid standardised strength 437–444. https://doi.org/10.1016/j.apmr.2015.10.096 testing setups may provide higher reliability and accuracy in Altmann, V. C., Groen, B. E., Hart, A. L., Vanlandewijck, Y. C., Van Limbeek, J., the assessment of trunk strength, compared with handheld & Keijsers, N. L. W. (2017). The impact of trunk impairment on performance-determining activities in wheelchair rugby. Scandinavian dynamometry, as it reduces the measurement errors from the Journal of Medicine & Science in Sports, 27(9), 1005–1014. https://doi.org/ tester. However, besides the impracticality of rigid strength 10.1111/sms.12720 setups during research at sporting events, we do not believe Beaussier, M. (2013). Innervation of the Abdominal Wall and Viscera. In the use of a handheld dynamometer has significantly impacted A. Atchabahian & R. Gupta (Eds.), The Anesthesia Guide (1st ed. ed., pp. the assumptions formulated in this current study as the trunk 646–649). McGraw-Hill Education/Medical. Bjerkefors, A., Carpenter, M. G., & Thorstensson, A. (2007). Dynamic trunk flexion trials showed similar ranges per participant. The differ­ stability is improved in paraplegics following kayak ergometer training. ences in trunk flexion strength were observed in alignment Scandinavian Journal of Medicine & Science in Sports, 17(6), 672–679. with trunk function, and in addition, the use of a handheld https://doi.org/10.1111/j.1600-0838.2006.00621.x JOURNAL OF SPORTS SCIENCES 9

Connick, M. J., Beckman, E., Vanlandewijck, Y., Malone, L. A., Blomqvist, S., & Lovell, D., Shields, D., Beck, B., Cuneo, R., & Mclellan, C. (2012). The aerobic Tweedy, S. M. (2017). Cluster analysis of novel isometric strength mea­ performance of trained and untrained handcyclists with spinal cord sures produces a valid and evidence-based classification structure for injury. Europen Journal Applied Physiology,112(9), 3431-3437. https:// wheelchair track racing. British Journal of Sports Medicine, 52(17), 1–7. doi.org/10.1007/s00421-012-2324-x http://dx.doi.org/10.1136/bjsports-2017-097558 Mannion, P., Toparlar, Y., Blocken, B., Clifford, E., Andrianne, T., & De Blaiser, C., De Ridder, R., Willems, T., Danneels, L., & Roosen, P. (2018). Hajdukiewicz, M. (2018). Analysis of crosswind aerodynamics for compe­ Reliability and validity of trunk flexor and trunk extensor strength mea­ titive hand-cycling. Journal of Wind Engineering and Industrial surements using handheld dynamometry in a healthy athletic Aerodynamics, 180, 182–190. https://doi.org/10.1016/j.jweia.2018.08.002 population. Physical Therapy in Sport, Internet]. ;34:180–186. Available McErlean, L., & Migliozzi, J. G. (2017). The nervous system. In I. Peate & from, . https://doi.org/10.1016/j.ptsp.2018.10.005 M. Nair (Eds.), Fundamentals of Anatomy and Physiology: For Healthcare De Groot, S., Dallmeijer, A. J., Bessems, P. J. C., Marcel, L., van der Students (2nd ed ed., pp. 403–438). John Wiley & Sons, Ltd. Woude, L. H. V., Janssen, T. W. J., et al (2012). Comparison of muscle Muchaxo, R. E. A., De Groot, S., Van Der Woude, L. H. V., Janssen, T. W. J., & strength, sprint power and aerobic capacity in adults with and without Nooijen, C. (2020). Do Handcycling Time-Trial Velocities Achieved by Para- Cerebral Palsy. Journal of Rehabilitation Medicine, 44(11), 932–938. Cycling Athletes Vary Across Handcycling Classes? Adapt Phys Act Q (pp. https://doi.org/10.2340/16501977-1037 1–20). De Groot, S., Kouwijzer, I., Valent, L. J. M., Van Der Woude, L. H. V., Nooijen, C., Muchaxo, R. E. A., Liljedahl, J., Bjerkefors, A., Janssen, T. W. J. , Nash, M. S., & Cowan, R. E. (2019). Good association between sprint Van Der Woude, L. H.V., Arndt, A., de Groot, S. (2021). The relation power and aerobic peak power during asynchronous arm-crank exercise between sprint power and time trial performance in elite paracyclists. in people with spinal cord injury. Disability and Rehabilitation, Internet]. Journal Of Science And Medicine In Sport / Sports Medicine Australia. 43(3), 1–8. Available from. https://doi.org/10.1080/09638288.2019. https://doi.org/10.1016/j.jsams.2021.04.014 1625978 Quittmann, O. J., Abel, T., Albracht, K., & Strüder, H. K. (2019). Reliability of Faupin, A., Gorce, P., Campillo, P., Thevenon, A., & Rémy-Néris, O. (2006). muscular activation patterns and their alterations during incremental Kinematic analysis of handbike propulsion in various gear ratios: handcycling in able-bodied participants during incremental handcycling Implications for joint pain. Clinical Biomechanics, 21(6), 560–566. in able-bodied participants. Sports Biomechanics, 1–16. https://doi.org/ https://doi.org/10.1016/j.clinbiomech.2006.01.001 10.1080/14763141.2019.1593496 Faupin, A., Gorce, P., Meyer, C., & Thevenon, A. (2008). Effects of backrest Quittmann, O. J., Meskamper, J., Abel, T., Albracht, K., Foitschik, T., Rojas- positioning and gear ratio on nondisabled subjects’ handcycling sprint­ vega, S., & Strüder, H. K. (2018). Kinematics and kinetics of handcycling ing performance and kinematics. The Journal of Rehabilitation Research propulsion at increasing workloads in able-bodied subjects. Sports and Development, 45(1), 109–116. https://doi.org/10.1682/JRRD.2006.10. Engineering, 21(4), 283–294. https://doi.org/10.1007/s12283-018-0269-y 0139 Rosso, V., Gastaldi, L., Rapp, W., Lindinger, S., Vanlandewijck, Y., Äyrämö, S., Febrer, A., Rodriguez, N., Alias, L., & Tizzano, E. (2010). Measurement of et al. (2019). Balance perturbations as a measurement tool for trunk muscle strength with a handheld dynamometer in patients with chronic impairment in cross-country sit skiing. Adapt Phys Act Q, 36(1), 61–76. spinal muscular atrophy. Journal of Rehabilitation Medicine, 42(3), https://doi.org/10.1123/apaq.2017-0161 228–231. https://doi.org/10.2340/16501977-0507 Rozen, W. M., Tran, T. M. N., Ashton, M. W., Barrington, M. J., Ivanusic, J. J., & Finch, J. A., & Baggish, A. L. (2016). Cardiovascular Evaluation and Treatment Taylor, G. I. (2008). Refining the course of the thoracolumbar nerves: of the Endurance Athlete. In T. L. Miller (Ed.), Endurance Sports Medicine: A new understanding of the innervation of the anterior abdominal wall. A Clinical Guide (pp. 3–20). Springer Nature. Clinical Anatomy, 21(4), 325–333. https://doi.org/10.1002/ca.20621 Hettinga, F. J., Valent, L., Groen, W., Van Drongelen, S., De Groot, S., & Van Sakamoto, H., Akita, K., & Sato, T. (1996). An anatomical analysis of the Der Woude, L. H. V. (2010). Hand-cycling: An active form of wheeled relationships between the intercostal nerves and the thoracic and mobility, recreation, and sports. Physical Medicine and Rehabilitation abdominal muscles in man. Cells Tissues Organs, 156(2), 143–150. Clinics of North America, 21(1), 127–140. https://doi.org/10.1016/j.pmr. https://doi.org/10.1159/000147839 2009.07.010 Stone, B., Mason, B. S., Bundon, A., & Goosey-Tolfrey, V. L. (2019). Elite Hopkings, W. A scale of magnitudes for effect statistics [Internet]. A New View handcycling: A qualitative analysis of recumbent handbike configuration of Statistics. 2002. Available from: https://www.sportsci.org/resource/ for optimal sports performance. Ergonomics, 62(3),449–458. Internet]. ;():. stats/index.html Available from. . https://doi.org/10.1080/00140139.2018.1531149 International Paralympic Committee. IPC athlete classification code Stone, B., Mason, B. S., Stephenson, B. T., & Goosey-Tolfrey, V. L. (2020). [Internet]. International Paralympic Committe; 2015. Available from: Physiological responses during simulated 16 km recumbent handcycling https://www.paralympic.org/sites/default/files/2020-05/ time trial and determinants of performance in trained handcyclists. 170704160235698_2015_12_17%2BClassification%2BCode_FINAL2_ European Journal of Applied Physiology, 120(7),1621–1628. Internet]. ;():. 0-1.pdf Available from. . https://doi.org/10.1007/s00421-020-04390-w International Paralympic Committee. (2017). World Para Athletics Stone, B., Mason, B. S., Warner, M. B., & Goosey-Tolfrey, V. L. (2019). Classification Rules and Regulations. Horizontal crank position affects economy and upper limb kinematics Janssen, T. W. J., Van Oers, C., Hollander, P., Veeger, H. E. J., & Van Der of recumbent handcyclists. Medicine & Science in Sports & Exercise, 51(11), Woude, L. H. V. (1993). Isometric strength, sprint power and aerobic 2265–2273. https://doi.org/10.1249/MSS.0000000000002062 power.Pdf. Medicine & Science in Sports & Exercise, 25(7), 863–870. Stone, B., Mason, B. S., Warner, M. B., & Tolfrey, V. L. G. (2019). Shoulder and https://doi.org/10.1249/00005768-199307000-00016 thorax kinematics contribute to increased power output of competitive Karthikbabu, S., & Chakrapani, M. (2017). Hand-held dynamometer is handcyclists. Scandinavian Journal of Medicine & Science in Sports, 29(6), a reliable tool to measure trunk muscle strength in chronic stroke. 843–853. https://doi.org/10.1111/sms.13402 Journal Clinics Diagnostic Research, 11(9), 09–12. Theisen, D. (2012). Cardiovascular determinants of exercise capacity in the Komorowski, M., Marshall, D. C., Salciccioli, J. D., & Crutain, Y. (2016). Paralympic athlete with spinal cord injury. Experimental Physiology, 97(3), Exploratory Data Analysis. In Secondary Analysis of Electronic Health 319–324. https://doi.org/10.1113/expphysiol.2011.063016 Records. Springer Open (pp. 185–203). https://doi.org/10.1007/978-3- Tweedy, S. M., & Vanlandewijck, Y. C. (2011). International Paralympic 319-43742-2_1 committee position stand-background and scientific principles of classi­ Kouwijzer, I., Nooijen, C., Van Breukelen, K., Janssen, T., & De Groot, S. (2018). fication in Paralympic sport. British Journal of Sports Medicine, 45(4), Effects of push-off ability and handcycle type on handcycling perfor­ 259–269. https://doi.org/10.1136/bjsm.2009.065060 mance in able-bodied participants. Journal of Rehabilitation Medicine, 50 Union Cycliste Internationale. Para-cycling results [Internet]. 2020a. Union (6), 563–568. https://doi.org/10.2340/16501977-2343 Cycliste Internationale. Available from: https://www.uci.org/para-cycling Krassioukov, A., & West, C. (2014). The role of autonomic function on sport /results performance in athletes with spinal cord injury. PM&R, 6(8), S58–65. Union Cycliste Internationale. Para-cycling. In: UCI Cycling Regulations https://doi.org/10.1016/j.pmrj.2014.05.023 [Internet]. 2020b. p. 1–97. Available from: http://www.uci.ch/mm/ 10 R. MUCHAXO ET AL.

Document/News/Rulesandregulation/16/80/73/1-GEN-20160101- exploratory study. In Analysis of Performance Determinants in E_English.pdf Handcycling (pp. 111–136). Doctoral dissertation, Katholieke Union Cycliste Internationale. Paracyclisme [Internet]. 2020c. Available from: Universiteit Leuven. https://www.uci.org/para-cycling/ Verellen, J., Meyer, C., Janssens, L., & Vanlandewijck, Y. (2012b). The impact Van Der Woude, L. H. V., Bosmans, I., Bervoets, B., & Veeger, H. E. J. (2000). of spinal cord injury lesion level on force generation effectivenessduring Handcycling: Different modes and gear ratios. Journal of Medical handcycling. In Doctoral dissertation, Katholieke Universiteit Leuven. Anal Engineering & Technology, 24(6), 242–249. https://doi.org/10.1080/ Perform Determ handcycling (pp. 79–94). 030919000300037168 Verellen, J., Meyer, C., Janssens, L., Vanlandewijck, Y., & Lacour, J. R. (2012). Van Der Zwaard, S., Van Der Laarse, W. J., Weide, G., Bloemers, F. W., Peak and submaximal steady-state metabolic and cardiorespiratory Hofmijster, M. J., Levels, K., Noordhof, D. A., Koning, J. J., Ruiter, C. J., & responses during arm-powered and arm-trunk-powered handbike ergo­ Jaspers, R. T. (2018). Critical determinants of combined sprint and endur­ metry in able-bodied participants. European Journal of Applied ance performance: An integrative analysis from muscle fiber to the Physiology, 112(3), 983–989. https://doi.org/10.1007/s00421-011-2051-8 human body. The FASEB Journal, 32(4), 2110–2123. https://doi.org/10. West, C. R., Gee, C. M., Voss, C., Hubli, M., Currie, K. D., Schmid, J., & 1096/fj.201700827R Krassioukov, A. V. (2015). Cardiovascular control, autonomic function, Vanlandewijck, Y. C., Verellen, J., Beckman, E., Connick, M., & Tweedy, S. M. and elite endurance performance in spinal cord injury. Scandinavian (2011). Trunk strength effect on track wheelchair start: Implications for Journal of Medicine & Science in Sports, 25(4), 476–485. https://doi.org/ classification. Medicine and Science in Sports and Exercise, 43(12), 10.1111/sms.12308 2344–2351. https://doi.org/10.1249/MSS.0b013e318223af14 West, C. R., Wong, S. C., & Krassioukov, A. V. (2014). Autonomic cardiovas­ Vanlandewijck, Y. C., Verellen, J., & Tweedy, S. (2011). Towards cular control in Paralympic athletes with spinal cord injury. Medicine & evidence-based classification in wheelchair sports: Impact of seating Science in Sports & Exercise, 46(1), 60–68. https://doi.org/10.1249/MSS. position on wheelchair acceleration. Journal of Sports Sciences, 29(10), 0b013e31829e46f3 1089–1096. https://doi.org/10.1080/02640414.2011.576694 Zeller, S., Abel, T., Smith, P. M., & Strüder, H. K. (2015). Influence of Verellen, J., Meyer, C., Janssens, L., & Vanlandewijck, Y. (2012a). An inte­ non-circular chainrings on physiological parameters in handcycling. grated kinetic, kinematic and EMG analysis to interpret gross mechanical Journal of Rehabilitation Research and Development, 52(2), 211–220. efficiency in arm powered versus arm trunk powered handcycling: An https://doi.org/10.1682/JRRD.2014.03.0070