- Email: [email protected]
Balance control in youth hockey players with and without a history of concussions during a lower limb reaching task
Clinical Biomechanics 67 (2019) 142–147
Contents lists available at ScienceDirect
Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Balance control in youth hockey players with and without a history of concussions during a lower limb reaching task
T
⁎
Katelyn M. Mitchell , Michael E. Cinelli Department of Kinesiology, Wilfrid Laurier University, Waterloo, ON, Canada
A R T I C LE I N FO
A B S T R A C T
Keywords: Balance control Concussion Visuomotor task Youth athletes Go/No-Go task
Background: Sport-related concussion (SRC) is a functional injury that affects several clinical domains, including balance and cognition. The purpose of this study was, 1) to determine whether a lower limb visuomotor task could identify balance control differences between youth athletes with and without previous SRC; and 2) if balance is affected by training over time. Methods: Youth hockey players (n = 34) who reported previous SRC (CONCUSSED; n = 12; mean age = 14.4 yrs., SD = 1.6, mean time from injury = 1.9 yrs., median = 1.7 yrs. [0.6–4.6]) and no history of SRC (CONTROL; n = 22; mean age = 14.7, SD = 1.5) were tested twice over 70 days. Participants stood in single support on a Nintendo Wii Balance board sampled at 100 Hz and performed Go/No-Go tasks with each foot. Five FitLight Trainer™ (Aurora, ON) lights were arranged on the floor at 60°, 30°, and 0° and illuminated in random GREEN (Go) or RED (No-Go). Balance was assessed using root mean square displacement and velocity of CoP in anterior-posterior and medial-lateral directions. Findings: CONCUSSED had significantly lower velocity of CoP in the anterior-posterior (F(1, 32) = 13.81, p < .001) and medial-lateral (F(1, 32) = 13.80, p < .001) directions than CONTROL, with no learning effects over time (anterior-posterior: F(1, 32) = 0.30, p = .137: F(1, 32) = 0.91, p = .346; medial-lateral: F(1, 32) = 0.91, p = .346). These findings suggest that CONCUSSED consistently performed the task more conservatively. Interpretation: A lower limb Go/No-Go task may objectively identify differences between youth athletes with and without previous SRC. These visuomotor and balance control deficits may persist beyond clinical recovery.
1. Introduction A sport-related concussion (SRC) is a transient, functional injury that affects several neurological domains, including balance, cognition, and vestibular-ocular functioning (McCrory et al., 2017). The roles of the visual and the vestibular systems are particularly important for maintaining postural control and guiding goal-directed movement in a constantly evolving environment (Drew et al., 2008). The complexity of sport requires an athlete to effectively extract and interpret sensory information from their surroundings for the rapid execution of motor tasks. Due to deficits of the sensorimotor system, previous reports suggest that athletes who have sustained a concussion may have a greater risk of sustaining a subsequent injury upon return-to-sport (RTS) (Cross et al., 2015). A recent review has suggested that this risk may be related to reduced postural control and even more so with the integration of a concurrent cognitive task (Howell et al., 2018a). According to the 5th Consensus Statement on Concussion in Sport from Berlin (2016), the approximate recovery time to for an adult is
⁎
14 days, and for children and adolescents, a minimum of 4 weeks (McCrory et al., 2017). Clinical recovery of these sensory systems is typically based on subjective report of symptoms during vestibularocular assessment, progressive activity, as well as observation of balance in different sensory conditions (Echemendia et al., 2017; McCrory et al., 2017; Mucha et al., 2014). However, increasing evidence suggests that neurophysiological deficits affecting balance control can persist beyond clinical recovery that may not be detected through subjective observation (Baker and Cinelli, 2014; Buckley et al., 2013; Powers et al., 2014; Slobounov et al., 2008). Reports have attempted to identify a physiological timeline of recovery; however, it remains unknown due to the variability of individual presentation, assessment measures, and time course of SRC (Kamins et al., 2017). Powers and colleagues (Powers et al., 2014), demonstrated that collegiate football players had deficits in static balance control with eyes open and eyes closed conditions in the anterior-posterior (A-P) direction with greater velocity of centre of pressure (vCoP) values that persisted beyond medical clearance for RTS. This report suggested that reduced balance control in the
Corresponding author at: Department of Kinesiology and Physical Education, 75 University Ave W, Waterloo, ON N2L 3C5, Canada. E-mail address: [email protected] (K.M. Mitchell).
https://doi.org/10.1016/j.clinbiomech.2019.05.006 Received 31 October 2018; Accepted 8 May 2019 0268-0033/ Crown Copyright © 2019 Published by Elsevier Ltd. All rights reserved.
Clinical Biomechanics 67 (2019) 142–147
K.M. Mitchell and M.E. Cinelli
A-P direction indicates an impairment of the lateral vestibulospinal tract (Highstein and Holstein, 2012; Masani et al., 2003; Powers et al., 2014). These balance deficits were not detected by a subjective observation of balance and required an objective method to characterize postural dysfunction beyond the resolution of symptoms. In recent years, various methods using objective measures have been used to quantify deficits for dynamic balance and gait tasks. Kinematic analysis of steady-state gait has revealed that collegiate athletes with a history of concussion have exhibited more conservative behaviours compared to sport- and gender-matched controls (Buckley et al., 2016; Martini et al., 2011). Subsequent studies have challenged balance control further with the addition of a concurrent cognitive task (e.g., Stroop task, counting backwards from 100 by 7). Persistent balance control deficits have been reported for athletes of various age groups with recent SRC during dual-task gait. These dynamic balance control deficits appear to be greater with adolescents than for young adult athletes during dual-task gait up to two months post-SRC (Howell et al., 2015; Howell et al., 2017). Therefore, the adolescent population may be at a greater risk for persistent deficits in not only balance, but the cognitive integration component as well. Several studies demonstrate balance control deficits in recently concussed athletes during steady-state or dual-task gait. In addition, there have been reports of post-concussion deficits during transitional gait tasks that exhibit different cortical mechanisms. Gait initiation is a transitional gait task that is considered an anticipatory postural adjustment (APA), that requires significantly greater visual and vestibular contributions for planning and execution (Massion, 1992). Therefore, it is may be more representative of the supraspinal mechanisms of balance control compared to steady-state gait, which can be modulated through spinal networks (Haghpanah et al., 2017). Recent findings revealed that athletes with previous SRC had altered postural control during a gait initiation task (Buckley et al., 2017). Currently, there is no previous research that has investigated performance of a similar gait initiation task with a cognitive component. Cognitive-motor integration requires even greater cortical mechanisms including the frontal-parietal network and the cerebellum (Molinari et al., 2002). Decreases in brain network activation using electroencephalography (EEG) during a Go/ No-Go decision-making task have been reported in youth and adolescents with previous concussion (Howell et al., 2018b; Kontos et al., 2016). For the current study, a similar decision-making task that incorporated response time and movement inhibition (Go/No-Go) was used during the lower limb reaching task. These cognitive components are very transferrable to a sports environment and may be a more effective measure of visuomotor function and balance control that is resistant to learning effects over time. Furthermore, since the vestibular and visual systems are significant components of balance control. The Vestibular-Ocular Motor Screen (VOMS) has been reported as an effective outcome measure to screen these sensory systems post-concussion in youth and adolescents. Provocation of symptoms with smooth pursuits and the vestibularocular reflex (VOR) in addition to balance impairments, have been reported to be a predictor of prolonged recovery in adolescents (Allum, 2012). The inclusion of the VOMS may identify possible dysfunction of the postural control system contributing to persistent balance deficits in athletes with and without history of previous concussion (Allum, 2012; Ellis et al., 2015; Master et al., 2018; Mucha et al., 2014). There is a significant demand for a more sensitive and feasible outcome measure to assess cognitive-motor balance control tasks to accurately monitor recovery of youth athletes with SRC. Thus, the necessity of effectively quantifying cognitive function and balance control that is immune to learning effects has great implications. Therefore, the purpose of the current study was to determine whether a novel, lower limb reaching task with a cognitive component (Go/No-Go task) could detect differences in balance control in youth hockey players with and without previous history of SRC over two time points. It was hypothesized that: 1) the athletes with previous SRC would exhibit more
Table 1 Participant demographics.
AGE (mean) SEX Most recent SRC (mean) Mean number of previous SRC
CONTROL (n = 22)
SRC (n = 12)
14.4 (SD ± 1.6) Male = 22 Female = 0 N/A
14.7 (SD ± 1.5) Male = 9 Female = 3 1.9 years (SD ± 1.3) 1.1
conservative dynamic balance control behaviours during the task compared to the athletes without history of SRC; and 2) the visuomotor balance task would be resistant to learning effects in youth hockey players over the two time points over a regular season. 2. Methods 2.1. Participants This study was approved by the Research Ethics Board at the authors' university. Informed consent was received by participants' parent (s) and/or guardian(s) as well as assent from each participant prior to conducting the study. Youth hockey players (n = 34; age 12–17 years) were recruited from a private hockey academy. Athletes provided a subjective report of their concussion history and recovery, including clearance for return to sport. Athletes who reported a previous history of SRC (CONCUSSED; n = 12) and those who reported no previous history of SRC (CONTROL; n = 22), (see Table 1). In the CONCUSSED group, only one athlete reported more than one concussion injury with two concussions reported at the time of testing (see Table 1). All athletes with previous SRC were asymptomatic and had returned to sport. Athletes with previous SRC were excluded from the study if the reported concussion injuries occurred < 6 months and > 5 years from the initial time point. The mean time from injury was 1.9 years (median = 1.7 years, range = 7.2 months to 4.8 years). All athletes who reported any significant lower extremity injuries, previous moderate or severe traumatic brain injury, neurological conditions, and/or had sustained an acute SRC and were symptomatic were excluded from the study. Furthermore, athletes who were in the CONTROL group at Time 1 and sustained a SRC between test periods were excluded from the study at Time 2 (n = 2). Athletes in the CONTROL group who demonstrated an average near point convergence (NPC) measuring ≥6 cm when screened with the VOMS at both time points were also excluded from the control group (Ellis et al., 2015). 2.2. Experimental design Participants were tested at initially at mid-season (December) and subsequently near end-of-season (February, t = 70-days). Due to the nature of training at the hockey academy, it was more appropriate to allow for new athletes to become accustomed to daily training for comparison. Each participant completed orthopaedic and concussion injury history questionnaires, including the 22-item post-concussion symptom scale (PCS) from the Sport Concussion Assessment Tool 5 (SCAT5) (Powers et al., 2014). Athletes performed the dynamic lower limb reaching task and then were assessed by a Registered Physiotherapist trained to administer the Vestibular-Ocular Motor Screen (VOMS). The VOMS consists of 7 items including, oculomotor function (smooth pursuit, saccades and NPC), and vestibular-ocular testing (vestibular-ocular reflex (VOR) and visual motion sensitivity). Items are subjectively rated on a10-point Likert scale based on provocation of symptoms (nausea, fogginess, headache, dizziness) and three NPC measurements (cm) were obtained (Ellis et al., 2015; Mucha et al., 2014). Participants performed the same lower limb reaching task for both test points at mid-season and end-of-season. 143
Clinical Biomechanics 67 (2019) 142–147
K.M. Mitchell and M.E. Cinelli
Fig. 1. Visuomotor task with five FitLights arranged at −60°, −30°, 0°, 30°, 60° about the midline of the Nintendo Wii balance board.
2.3. Experimental set-up
2.6. Statistical analysis
Participants stood in single support in the centre of a Nintendo Wii Balance Board (WBB; sampling frequency of 100 Hz) with the reaching limb elevated for the duration of each trial. A recent systematic review has confirmed that the WBB is a valid and reliable measurement tool for the assessment of balance control (Clark et al., 2018). Five FitLight Trainer™ lights (Aurora, ON, Canada) were arranged on the floor in a semi-circular pattern anterior to the participants at 60°, 30°, and 0° about the midline of the WBB (see Fig. 1). The radial distance of each FitLight was normalized to the tibial length of each athlete measured prior to beginning of the protocol. Each FitLight illuminated in a completely random order six times per trial, for a total of 30 illuminations per trial. Upon illumination, the FitLights were set to time-out after 0.70s with a delay of 0.90s between each illumination, therefore, each trial had minimal variability in duration length (approximately 55 s trials) depending on the speed at which the participant responded during the task.
A repeated-measures mixed analysis of variance (ANOVA) was conducted to analyze effects of group (CONCUSSED and CONTROL) and time (time 1 and time 2 [70 days post]). Interactions between the independent variables for each of the balance control measures (RMS dCoP and vCoP) were examined in both A-P and M-L directions. Statistical significance was set to an alpha-level of p < .05. 3. Results 3.1. RMS CoP displacement (dCoP) There was no interaction effect between group and time for dCoP in the M-L direction (Time 1: CONCUSSED = 0.92 cm (SD 0.18), CONTROL = 1.06 cm (SD = 0.30); Time 2: CONCUSSED = 0.87 cm (SD = 0.29), CONTROL = 1.03 cm (SD = 0.23); F(1, 32) = 0.14, p = .908). As well as no significant main effects of group (F(1, 32) = 3.48, p = .098) or time (F(1, 32) = 0.56, p = .461) (see Fig. 2A). The results revealed a significant interaction between group and time for dCoP in the A/P direction (Time 1: CONCUSSED = 1.54 cm (SD = 0.20), CONTROL = 1.52 cm (SD = 0.31); Time 2: CONCUSSED = 1.45 cm (SD = 0.28), CONTROL = 1.81 cm (SD = 0.33); F(1, 2 32) = 10.82, p < .05, η = 0.253), as the CONTROL group had an increase in A-P dCoP from Time 1 compared to Time 2 (see Fig. 2B). However, there was no significant main effect of group (F(1, 32) = 3.62, p = .066) or time (F(1, 32) = 3.05, p = .090) for dCoP in the A-P direction.
2.4. Experimental protocol Each light illuminated in random sequence as a green (Go) or red (No-Go) colour. Participants were instructed to hover their reaching (non-stance) limb as quickly as possible over the Green/Go lights (70% occurrence) returning to their starting position and to withhold movement for Red/No-Go lights (30% occurrence) prior to the illumination of the next light (0.9 s intervals). There were no practice trials and participants were monitored to ensure their stance foot did not shift and/or step off the board. Between trials participants were provided brief rest periods as needed. If participants stepped off the board, that trial was not included in CoP analysis and was retested. The task was performed in both left and right single support to eliminate effects of limb dominance, over three trials each for a total of six trials per participant.
3.2. RMS CoP velocity (vCoP) The findings from the study revealed no significant interaction effects between group and time for M-L vCoP (Time 1: CONCUSSED = 6.40 cm/s (SD = 0.91); CONTROL = 7.94 cm/s (SD = 1.36); Time 2: CONCUSSED = 6.05 cm/s (SD = 0.93), CONTROL = 7.18 cm/s (SD = 1.20); F(1, 32) = 0.91, p = .346). In addition, there was no interaction effect between group and time for A-P vCoP (Time 1: CONCUSSED = 8.60 cm/s (SD = 1.95), CONTROL = 11.38 cm/s (SD = 2.84) and Time 2: CONCUSSED = 7.76 cm/s (SD = 1.59), CONTROL = 10.72 cm/s (SD = 2.90); F(1, 32) = 0.3, p = .864). As well, there was no main effect of time for vCoP in the M-L direction (F(1, 32) = 0.91, p = .346) or the A-P direction (F(1, 32) = 0.30, p = .137). However, a significant main effect of group was revealed for the vCoP in the M-L direction (F(1, 32) = 13.80 cm/s, p < .01, η2 = 0.30) (see Fig. 3A) as well as for A-P direction (F(1, 32) = 13.81, p < .01, η2 = 0.30). The CONCUSSED group had significantly lower vCoP in both M-L and A-P directions compared to the CONTROL group (see
2.5. Data analysis The average anterior-posterior (A-P) and medial-lateral (M-L) location of the CoP for first 5 s of each trial, prior to the onset of lights illuminating, was used as a bias and removed from the rest of the CoP calculation in order to calculate Root Mean Square (RMS) of CoP displacement (dCoP). The CoP displacement over time was differentiated to calculate the RMS of COP velocity (vCoP). Both the dCoP and vCoP were calculated in both the A-P and M-L directions.
CoPRMS =
1/ n (x12 + x 22 + …x n2) 144
Clinical Biomechanics 67 (2019) 142–147
K.M. Mitchell and M.E. Cinelli
Fig. 2. Medial/Lateral RMS dCOP (A) had no significant differences between CONC and CONTROL (F(1, 32) = 0.14, p = .908), with no changes over time (Time 1: SRC = 0.92 cm (SD 0.18), CONTROL = 1.06 cm (SD = 0.30); Time 2: SRC = 0.87 cm (SD = 0.29), CONTROL = 1.03 cm (SD = 0.23)). Anterior/Posterior RMS dCOP (B) had a significant interaction effect (F(1, 32) = 10.82, p < .05, η2 = 0.253), as CONTROL improved from Time 1 to Time 2 (Time 1: SRC = 1.54 cm (SD = 0.20), CONTROL = 1.52 cm (SD = 0.31); Time 2: SRC = 1.45 cm (SD = 0.28), CONTROL = 1.81 cm (SD = 0.33);.
greater balance impairments. The results from the current study align with previous findings that revealed no differences in M/L or A/P dCoP during static balance, in asymptomatic collegiate athletes (Powers et al., 2014). The significant interaction observed between group and time for A/P dCoP may be due to a small learning effect in the control group. However, participants were instructed to move as quickly as possible in response to the FitLights during the lower limb reaching task. Due to the nature of the lower limb reaching task in the anteriorposterior direction, greater displacement in the sagittal plane was anticipated. A small increase (approximately 3 mm) in A/P dCoP cannot confirm that learning occurred due to training effects. It is recommended that analyzing dCoP alone may not be the most reliable method of characterizing balance control in either static or dynamic conditions. The major finding from the current study was that youth hockey players who reported a previous SRC did in fact have differences in dynamic balance control in comparison to players without previous SRC over time. There was a significant main effect of vCoP indicating that athletes with a history of SRC consistently had reduced vCoP in both M/L and A/P direction. During static balance conditions,
Fig. 3).
4. Discussion The purpose of the current study was two-fold: 1) to determine whether a novel, lower limb reaching task could detect differences in balance control in youth hockey players with and without reported previous SRC; and 2) to determine if the lower limb reaching task was immune to training/learning effects over time. It was believed that the athletes with previous SRC would exhibit reduced dynamic balance control through reduced vCoP measures compared to the group without history of SRC and that the visuomotor task would be resistant to learning (training) effects in youth hockey players throughout a regular season. Similar to previous findings, there were no significant main effects of dCoP during the dynamic visuomotor reaching task in either plane between the hockey players with and without SRC over time. CoP displacement is an indirect measure of the amount of body movement (sway) produced by an individual during a trial and dCoP demonstrates one's displacement variability over a trial (Clark et al., 2018; Winter, 1995). Individuals with larger dCoP values are believed to display
Fig. 3. Medial/Lateral RMS vCOP (A) had a significant main effect of group as CONTROL had a greater velocity compared to CONC (Time 1: SRC = 6.40 cm/s (SD = 0.91); CONTROL = 7.94 cm/s (SD = 1.36); Time 2: SRC = 6.05 cm/s (SD = 0.93), CONTROL = 7.18 cm/s (SD = 1.20); (F(1, 32) = 13.80 cm/s, p < .01, η2 = 0.30). Anterior/Posterior RMS vCOP (B) had a main effect of group as CONTROL had a greater velocity compared to CONC (Time 1: SRC = 8.60 cm/s (SD = 1.95), CONTROL = 11.38 cm/s (SD = 2.84) and Time 2: SRC = 7.76 cm/s (SD = 1.59), CONTROL = 10.72 cm/s (SD = 2.90); F(1, 32) = 13.81, p < .01, η2 = 0.30). There were no significant changes in velocity over time in either plane for each group. 145
Clinical Biomechanics 67 (2019) 142–147
K.M. Mitchell and M.E. Cinelli
however, the supraspinal origins of these deficits remain unknown. Future research should be conducted to determine the differences in higher order cortical activation patterns in individuals with a history of SRC that contribute to cognitive-motor deficits. There may be differences in cortical activation patterns within areas of the frontal-parietal network and cerebellum, that may result in conservative motor behaviours and visuomotor deficits (Molinari et al., 2002).
individuals with larger vCoP values are suggested to be making more corrections (i.e., faster moving CoP) to their balance to remain upright (Echemendia et al., 2017). However, in the current paradigm, a larger vCoP in the direction of the lower limb reaching motion (i.e., sagittal plane) is thought to demonstrate greater anticipatory control. Velocity is indicative of the intensity and direction of displacement; therefore, in the A/P plane it is associated with higher order sensory integration from the vestibular and visual systems (Highstein and Holstein, 2012; Masani et al., 2003; Powers et al., 2014). It can be inferred that a higher vCoP suggests greater efficiency of the sensory systems involved in cognitive-motor integration. The youth hockey players in the current study with previous SRC had no clinical symptoms and had returned to sport, yet they performed the task slower than the control group at both test points. The slower velocity may be due to a greater reliance on visual feedback control, greater cognitive load, and more conservative behaviours during the Go/No-Go reaching task used in the current study. Similarly, dynamic gait stability is reduced as dual-task complexity is increased in adolescents two months post-SRC (Howell et al., 2015). In contrast, the differences in vCoP may be due to reduced anticipatory control and response time in the athletes with previous SRC. It is likely that athletes were not put through a rigorous rehabilitation program prior to returnto-sport. It has been suggested that a greater buffer zone between becoming asymptomatic and returning to full contact would allow for a more gradual recovery of neurophysiological mechanisms that may persist beyond the clinical recovery (Kamins et al., 2017). Additionally, both groups performed the task without significant changes in vCoP in either plane over time, suggesting that the visuomotor reaching task was immune to training effects and may be considered an accurate representation of one's balance control capabilities. The novel visuomotor reaching task seemed to be challenging enough to negate training effects of a regular hockey season and highlight persistent balance impairments in youth athletes with recent concussion. The current task may be sufficient for comparison of a youth athlete during the acute, symptomatic phase of SRC and the asymptomatic, recovery phase to an age-matched teammate without history of SRC. The findings of the current study align with previous reports that suggest that a more rigorous approach of assessing dynamic balance with a cognitive component, may be a more suitable method of testing youth athletes beyond the symptomatic stages of SRC (Howell et al., 2015; Howell et al., 2017). Further research is necessary to determine the validity of the current or a similar visuomotor task for clinical application. This study is not without a number of limitations to be considered. The first of which is the reliability of subjective reporting from youth regarding their concussion injury history and time of injury. It would be beneficial to have a record of clinical diagnosis and progress of recovery to full RTS from a designated healthcare practitioner or physician. In addition, parent(s) and/or guardian(s) should be consulted to confirm the history of concussion diagnosis in adolescents younger than the age of 16 years old. A second limitation was that there were no female participants in the CONTROL group to compare to those in the CONCUSSED group. This was due to a lower number of females within the hockey academy, and that all female participants had reported sustaining a previous concussion. Therefore, these findings cannot conclude any sex differences for dynamic balance control within this sample. A recent study reported that adolescent females with previous SRC had reduced cadence during dual-task gait compared to adolescent males with previous SRC (Howell et al., 2017). Further research should be conducted to determine the sex differences in balance control during a lower limb cognitive-motor task. Furthermore, the previous literature based on assessment of gait may coincide with the results of this study, however, the differences in the execution of dual-task gait and a visuomotor reaching task may differ in neural correlates of control. These findings suggest that dynamic balance control deficits may persist beyond clinical recovery,
5. Conclusion In conclusion, the findings of this study suggest that youth hockey players with a history of SRC may exhibit dynamic balance control deficits during a lower limb visuomotor task. These deficits were characterized by greater utilization of visual feedback and more conservative movement behaviours. The novel visuomotor task had no significant learning effects over time, which may indicate that baseline testing is not necessary. Further research should be conducted to investigate the cortical mechanisms underlying dynamic stability during a visuomotor task. Declaration of Competing Interest None. Acknowledgements The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. The authors would like to thank Simon Jones from Toronto Rehab, for developing the software for the Wii Balance board. The authors would also like to thank the Natural Sciences and Engineering Research Council of Canada (05288-2014) for support. References Allum, J., 2012. Recovery of vestibular ocular reflex function and balance control after a unilateral peripheral vestibular deficit. Front. Neurol. 3 (83). Baker, C.S., Cinelli, M.E., 2014. Visuomotor deficits during locomotion in previously concussed athletes 30 or more days following return to play. Phys. Rep. 2 (12), e12252. Buckley, T.A., Munkasy, B.A., Tapia-Lovler, T.G., Wikstrom, E.A., 2013. Altered gait termination strategies following a concussion. Gait Posture 38 (3), 549–551. Buckley, T.A., Vallabhajosula, S., Oldham, J.R., et al., 2016. Evidence of a conservative gait strategy in athletes with a history of concussions. J. Sport Health Sci. 5 (4), 417–423. Buckley, T.A., Oldham, J.R., Munkasy, B.A., Evans, K.E., 2017. Decreased anticipatory postural adjustments during gait initiation acutely post-concussion. Arch. Phys. Med. Rehabil. 98 (10), 1962–1968. Clark, R.A., Mentiplay, B.F., Pua, Y.H., Bower, K.J., 2018. Reliability and validity of the Wii Balance Board for assessment of standing balance: a systematic review. Gait Posture 61, 40–54. Cross, M., Kemp, S., Smith, A., Trewartha, G., Stokes, K., 2015. Professional rugby union players have a 60% greater risk of time loss injury after concussion: a 2-season prospective study of clinical outcomes. Br. J. Sports Med. 50 (15), 926–931. Drew, T., Andujar, J.E., Lajoie, K., Yakovenko, S., 2008. Cortical mechanisms involved in visuomotor coordination during precision walking. Brain Res. Rev. 57 (1), 199–211. Echemendia, R.J., Meeuwisse, W., McCrory, P., Davis, G.A., Putukian, M., Leddy, J., ... Schneider, K., 2017. The sport concussion assessment tool 5th edition (SCAT5). Br. J. Sports Med. 51 (11), 848–850. Ellis, M.J., Cordingley, D., Vis, S., Reimer, K., Leiter, J., Russell, K., 2015. Vestibuloocular dysfunction in pediatric sports-related concussion. J. Neurosurg. Pediatr. (3), 248–255. Haghpanah, S.A., Farahmand, F., Zohoor, H., 2017. Modular neuromuscular control of human locomotion by central pattern generator. J. Biomech. 53, 154–162. Highstein, S.M., Holstein, G.R., 2012. The anatomical and physiological framework for vestibular prostheses. Anat. Rec. 295 (11), 2000–2009. Howell, D.R., Osternig, L.R., Chou, L.S., 2015. Adolescents demonstrate greater gait balance control deficits after concussion than young adults. Am. J. Sports Med. 43 (3), 625–632. Howell, D.R., Stracciolini, A., Geminiani, E., Meehan, W.P., 2017. Dual-task gait differences in female and male adolescents following sport-related concussion. Gait Posture 54, 284–289. Howell, D.R., Lynall, R.C., Buckley, T.A., Herman, D.C., 2018a. Neuromuscular control deficits and the risk of subsequent injury after a concussion: a scoping review. Sports Med. 1–19.
146
Clinical Biomechanics 67 (2019) 142–147
K.M. Mitchell and M.E. Cinelli
Master, C.L., Master, S.R., Wiebe, D.J., Storey, E.P., Lockyer, J.E., Podolak, O.E., Grady, M.F., 2018. Vision and vestibular system dysfunction predicts prolonged concussion recovery in children. Clin. J. Sport Med. 28 (2), 139–145. McCrory, P., Meeuwisse, W., Dvorak, J., et al., 2017. Consensus statement on concussion in sport—the 5th international conference on concussion in sport held in Berlin, October 2016. Br. J. Sports Med. 51 (11), 838–847. Molinari, M., Filippini, V., Leggio, M.G., 2002. Neuronal plasticity of interrelated cerebellar and cortical networks. Neuroscience 111 (4), 863–870. Mucha, A., Collins, M.W., Elbin, R.J., Furman, J.M., Troutman-Enseki, C., DeWolf, R.M., Kontos, A.P., 2014. A brief vestibular/ocular motor screening (VOMS) assessment to evaluate concussions: preliminary findings. Am. J. Sports Med. 42 (10), 2479–2486. Powers, K.C., Kalmar, J.M., Cinelli, M.E., 2014. Recovery of static stability following a concussion. Gait Posture 39 (1), 611–614. Slobounov, S., Cao, C., Sebastianelli, W., Slobounov, E., Newell, K., 2008. Residual deficits from concussion as revealed by virtual time-to-contact measures of postural stability. Clin. Neurophysiol. 119 (2), 281–289. Winter, D.A., 1995. Human balance and posture control during standing and walking. Gait Posture 3 (4), 193–214 Dec 1.
Howell, D.R., Meehan III, W.P., Barber Foss, K.D., Reches, A., Weiss, M., Myer, G.D., 2018b. Reduced dual-task gait speed is associated with visual Go/No-Go brain network activation in children and adolescents with concussion. Brain Inj. 1–6. Kamins, J., Bigler, E., Covassin, T., Henry, L., Kemp, S., Leddy, J. J., … & McLeod, T. C. V. (2017). What is the physiological time to recovery after concussion? A systematic review. Br. J. Sports Med., 51(12), 935–940. Kontos, A.P., Reches, A., Elbin, R.J., Dickman, D., Laufer, I., Geva, A.B., Collins, M.W., 2016. Preliminary evidence of reduced brain network activation in patients with post-traumatic migraine following concussion. Brain Imaging Behav. 10 (2), 594–603. Martini, D.N., Sabin, M.J., DePesa, S.A., Leal, E.W., Negrete, T.N., Sosnoff, J.J., Broglio, S.P., 2011. The chronic effects of concussion on gait. Arch. Phys. Med. Rehabil. 92 (4), 585–589. Masani, K., Popovic, M.R., Nakazawa, K., Kouzaki, M., Nozaki, D., 2003. Importance of body sway velocity information in controlling ankle extensor activities during quiet stance. J. Neurophysiol. 90 (6), 3774–3782. Massion, J., 1992. Movement, posture and equilibrium: interaction and coordination. Prog. Neurobiol. 38 (1), 35–56.
147
Contents lists available at ScienceDirect
Clinical Biomechanics journal homepage: www.elsevier.com/locate/clinbiomech
Balance control in youth hockey players with and without a history of concussions during a lower limb reaching task
T
⁎
Katelyn M. Mitchell , Michael E. Cinelli Department of Kinesiology, Wilfrid Laurier University, Waterloo, ON, Canada
A R T I C LE I N FO
A B S T R A C T
Keywords: Balance control Concussion Visuomotor task Youth athletes Go/No-Go task
Background: Sport-related concussion (SRC) is a functional injury that affects several clinical domains, including balance and cognition. The purpose of this study was, 1) to determine whether a lower limb visuomotor task could identify balance control differences between youth athletes with and without previous SRC; and 2) if balance is affected by training over time. Methods: Youth hockey players (n = 34) who reported previous SRC (CONCUSSED; n = 12; mean age = 14.4 yrs., SD = 1.6, mean time from injury = 1.9 yrs., median = 1.7 yrs. [0.6–4.6]) and no history of SRC (CONTROL; n = 22; mean age = 14.7, SD = 1.5) were tested twice over 70 days. Participants stood in single support on a Nintendo Wii Balance board sampled at 100 Hz and performed Go/No-Go tasks with each foot. Five FitLight Trainer™ (Aurora, ON) lights were arranged on the floor at 60°, 30°, and 0° and illuminated in random GREEN (Go) or RED (No-Go). Balance was assessed using root mean square displacement and velocity of CoP in anterior-posterior and medial-lateral directions. Findings: CONCUSSED had significantly lower velocity of CoP in the anterior-posterior (F(1, 32) = 13.81, p < .001) and medial-lateral (F(1, 32) = 13.80, p < .001) directions than CONTROL, with no learning effects over time (anterior-posterior: F(1, 32) = 0.30, p = .137: F(1, 32) = 0.91, p = .346; medial-lateral: F(1, 32) = 0.91, p = .346). These findings suggest that CONCUSSED consistently performed the task more conservatively. Interpretation: A lower limb Go/No-Go task may objectively identify differences between youth athletes with and without previous SRC. These visuomotor and balance control deficits may persist beyond clinical recovery.
1. Introduction A sport-related concussion (SRC) is a transient, functional injury that affects several neurological domains, including balance, cognition, and vestibular-ocular functioning (McCrory et al., 2017). The roles of the visual and the vestibular systems are particularly important for maintaining postural control and guiding goal-directed movement in a constantly evolving environment (Drew et al., 2008). The complexity of sport requires an athlete to effectively extract and interpret sensory information from their surroundings for the rapid execution of motor tasks. Due to deficits of the sensorimotor system, previous reports suggest that athletes who have sustained a concussion may have a greater risk of sustaining a subsequent injury upon return-to-sport (RTS) (Cross et al., 2015). A recent review has suggested that this risk may be related to reduced postural control and even more so with the integration of a concurrent cognitive task (Howell et al., 2018a). According to the 5th Consensus Statement on Concussion in Sport from Berlin (2016), the approximate recovery time to for an adult is
⁎
14 days, and for children and adolescents, a minimum of 4 weeks (McCrory et al., 2017). Clinical recovery of these sensory systems is typically based on subjective report of symptoms during vestibularocular assessment, progressive activity, as well as observation of balance in different sensory conditions (Echemendia et al., 2017; McCrory et al., 2017; Mucha et al., 2014). However, increasing evidence suggests that neurophysiological deficits affecting balance control can persist beyond clinical recovery that may not be detected through subjective observation (Baker and Cinelli, 2014; Buckley et al., 2013; Powers et al., 2014; Slobounov et al., 2008). Reports have attempted to identify a physiological timeline of recovery; however, it remains unknown due to the variability of individual presentation, assessment measures, and time course of SRC (Kamins et al., 2017). Powers and colleagues (Powers et al., 2014), demonstrated that collegiate football players had deficits in static balance control with eyes open and eyes closed conditions in the anterior-posterior (A-P) direction with greater velocity of centre of pressure (vCoP) values that persisted beyond medical clearance for RTS. This report suggested that reduced balance control in the
Corresponding author at: Department of Kinesiology and Physical Education, 75 University Ave W, Waterloo, ON N2L 3C5, Canada. E-mail address: [email protected] (K.M. Mitchell).
https://doi.org/10.1016/j.clinbiomech.2019.05.006 Received 31 October 2018; Accepted 8 May 2019 0268-0033/ Crown Copyright © 2019 Published by Elsevier Ltd. All rights reserved.
Clinical Biomechanics 67 (2019) 142–147
K.M. Mitchell and M.E. Cinelli
A-P direction indicates an impairment of the lateral vestibulospinal tract (Highstein and Holstein, 2012; Masani et al., 2003; Powers et al., 2014). These balance deficits were not detected by a subjective observation of balance and required an objective method to characterize postural dysfunction beyond the resolution of symptoms. In recent years, various methods using objective measures have been used to quantify deficits for dynamic balance and gait tasks. Kinematic analysis of steady-state gait has revealed that collegiate athletes with a history of concussion have exhibited more conservative behaviours compared to sport- and gender-matched controls (Buckley et al., 2016; Martini et al., 2011). Subsequent studies have challenged balance control further with the addition of a concurrent cognitive task (e.g., Stroop task, counting backwards from 100 by 7). Persistent balance control deficits have been reported for athletes of various age groups with recent SRC during dual-task gait. These dynamic balance control deficits appear to be greater with adolescents than for young adult athletes during dual-task gait up to two months post-SRC (Howell et al., 2015; Howell et al., 2017). Therefore, the adolescent population may be at a greater risk for persistent deficits in not only balance, but the cognitive integration component as well. Several studies demonstrate balance control deficits in recently concussed athletes during steady-state or dual-task gait. In addition, there have been reports of post-concussion deficits during transitional gait tasks that exhibit different cortical mechanisms. Gait initiation is a transitional gait task that is considered an anticipatory postural adjustment (APA), that requires significantly greater visual and vestibular contributions for planning and execution (Massion, 1992). Therefore, it is may be more representative of the supraspinal mechanisms of balance control compared to steady-state gait, which can be modulated through spinal networks (Haghpanah et al., 2017). Recent findings revealed that athletes with previous SRC had altered postural control during a gait initiation task (Buckley et al., 2017). Currently, there is no previous research that has investigated performance of a similar gait initiation task with a cognitive component. Cognitive-motor integration requires even greater cortical mechanisms including the frontal-parietal network and the cerebellum (Molinari et al., 2002). Decreases in brain network activation using electroencephalography (EEG) during a Go/ No-Go decision-making task have been reported in youth and adolescents with previous concussion (Howell et al., 2018b; Kontos et al., 2016). For the current study, a similar decision-making task that incorporated response time and movement inhibition (Go/No-Go) was used during the lower limb reaching task. These cognitive components are very transferrable to a sports environment and may be a more effective measure of visuomotor function and balance control that is resistant to learning effects over time. Furthermore, since the vestibular and visual systems are significant components of balance control. The Vestibular-Ocular Motor Screen (VOMS) has been reported as an effective outcome measure to screen these sensory systems post-concussion in youth and adolescents. Provocation of symptoms with smooth pursuits and the vestibularocular reflex (VOR) in addition to balance impairments, have been reported to be a predictor of prolonged recovery in adolescents (Allum, 2012). The inclusion of the VOMS may identify possible dysfunction of the postural control system contributing to persistent balance deficits in athletes with and without history of previous concussion (Allum, 2012; Ellis et al., 2015; Master et al., 2018; Mucha et al., 2014). There is a significant demand for a more sensitive and feasible outcome measure to assess cognitive-motor balance control tasks to accurately monitor recovery of youth athletes with SRC. Thus, the necessity of effectively quantifying cognitive function and balance control that is immune to learning effects has great implications. Therefore, the purpose of the current study was to determine whether a novel, lower limb reaching task with a cognitive component (Go/No-Go task) could detect differences in balance control in youth hockey players with and without previous history of SRC over two time points. It was hypothesized that: 1) the athletes with previous SRC would exhibit more
Table 1 Participant demographics.
AGE (mean) SEX Most recent SRC (mean) Mean number of previous SRC
CONTROL (n = 22)
SRC (n = 12)
14.4 (SD ± 1.6) Male = 22 Female = 0 N/A
14.7 (SD ± 1.5) Male = 9 Female = 3 1.9 years (SD ± 1.3) 1.1
conservative dynamic balance control behaviours during the task compared to the athletes without history of SRC; and 2) the visuomotor balance task would be resistant to learning effects in youth hockey players over the two time points over a regular season. 2. Methods 2.1. Participants This study was approved by the Research Ethics Board at the authors' university. Informed consent was received by participants' parent (s) and/or guardian(s) as well as assent from each participant prior to conducting the study. Youth hockey players (n = 34; age 12–17 years) were recruited from a private hockey academy. Athletes provided a subjective report of their concussion history and recovery, including clearance for return to sport. Athletes who reported a previous history of SRC (CONCUSSED; n = 12) and those who reported no previous history of SRC (CONTROL; n = 22), (see Table 1). In the CONCUSSED group, only one athlete reported more than one concussion injury with two concussions reported at the time of testing (see Table 1). All athletes with previous SRC were asymptomatic and had returned to sport. Athletes with previous SRC were excluded from the study if the reported concussion injuries occurred < 6 months and > 5 years from the initial time point. The mean time from injury was 1.9 years (median = 1.7 years, range = 7.2 months to 4.8 years). All athletes who reported any significant lower extremity injuries, previous moderate or severe traumatic brain injury, neurological conditions, and/or had sustained an acute SRC and were symptomatic were excluded from the study. Furthermore, athletes who were in the CONTROL group at Time 1 and sustained a SRC between test periods were excluded from the study at Time 2 (n = 2). Athletes in the CONTROL group who demonstrated an average near point convergence (NPC) measuring ≥6 cm when screened with the VOMS at both time points were also excluded from the control group (Ellis et al., 2015). 2.2. Experimental design Participants were tested at initially at mid-season (December) and subsequently near end-of-season (February, t = 70-days). Due to the nature of training at the hockey academy, it was more appropriate to allow for new athletes to become accustomed to daily training for comparison. Each participant completed orthopaedic and concussion injury history questionnaires, including the 22-item post-concussion symptom scale (PCS) from the Sport Concussion Assessment Tool 5 (SCAT5) (Powers et al., 2014). Athletes performed the dynamic lower limb reaching task and then were assessed by a Registered Physiotherapist trained to administer the Vestibular-Ocular Motor Screen (VOMS). The VOMS consists of 7 items including, oculomotor function (smooth pursuit, saccades and NPC), and vestibular-ocular testing (vestibular-ocular reflex (VOR) and visual motion sensitivity). Items are subjectively rated on a10-point Likert scale based on provocation of symptoms (nausea, fogginess, headache, dizziness) and three NPC measurements (cm) were obtained (Ellis et al., 2015; Mucha et al., 2014). Participants performed the same lower limb reaching task for both test points at mid-season and end-of-season. 143
Clinical Biomechanics 67 (2019) 142–147
K.M. Mitchell and M.E. Cinelli
Fig. 1. Visuomotor task with five FitLights arranged at −60°, −30°, 0°, 30°, 60° about the midline of the Nintendo Wii balance board.
2.3. Experimental set-up
2.6. Statistical analysis
Participants stood in single support in the centre of a Nintendo Wii Balance Board (WBB; sampling frequency of 100 Hz) with the reaching limb elevated for the duration of each trial. A recent systematic review has confirmed that the WBB is a valid and reliable measurement tool for the assessment of balance control (Clark et al., 2018). Five FitLight Trainer™ lights (Aurora, ON, Canada) were arranged on the floor in a semi-circular pattern anterior to the participants at 60°, 30°, and 0° about the midline of the WBB (see Fig. 1). The radial distance of each FitLight was normalized to the tibial length of each athlete measured prior to beginning of the protocol. Each FitLight illuminated in a completely random order six times per trial, for a total of 30 illuminations per trial. Upon illumination, the FitLights were set to time-out after 0.70s with a delay of 0.90s between each illumination, therefore, each trial had minimal variability in duration length (approximately 55 s trials) depending on the speed at which the participant responded during the task.
A repeated-measures mixed analysis of variance (ANOVA) was conducted to analyze effects of group (CONCUSSED and CONTROL) and time (time 1 and time 2 [70 days post]). Interactions between the independent variables for each of the balance control measures (RMS dCoP and vCoP) were examined in both A-P and M-L directions. Statistical significance was set to an alpha-level of p < .05. 3. Results 3.1. RMS CoP displacement (dCoP) There was no interaction effect between group and time for dCoP in the M-L direction (Time 1: CONCUSSED = 0.92 cm (SD 0.18), CONTROL = 1.06 cm (SD = 0.30); Time 2: CONCUSSED = 0.87 cm (SD = 0.29), CONTROL = 1.03 cm (SD = 0.23); F(1, 32) = 0.14, p = .908). As well as no significant main effects of group (F(1, 32) = 3.48, p = .098) or time (F(1, 32) = 0.56, p = .461) (see Fig. 2A). The results revealed a significant interaction between group and time for dCoP in the A/P direction (Time 1: CONCUSSED = 1.54 cm (SD = 0.20), CONTROL = 1.52 cm (SD = 0.31); Time 2: CONCUSSED = 1.45 cm (SD = 0.28), CONTROL = 1.81 cm (SD = 0.33); F(1, 2 32) = 10.82, p < .05, η = 0.253), as the CONTROL group had an increase in A-P dCoP from Time 1 compared to Time 2 (see Fig. 2B). However, there was no significant main effect of group (F(1, 32) = 3.62, p = .066) or time (F(1, 32) = 3.05, p = .090) for dCoP in the A-P direction.
2.4. Experimental protocol Each light illuminated in random sequence as a green (Go) or red (No-Go) colour. Participants were instructed to hover their reaching (non-stance) limb as quickly as possible over the Green/Go lights (70% occurrence) returning to their starting position and to withhold movement for Red/No-Go lights (30% occurrence) prior to the illumination of the next light (0.9 s intervals). There were no practice trials and participants were monitored to ensure their stance foot did not shift and/or step off the board. Between trials participants were provided brief rest periods as needed. If participants stepped off the board, that trial was not included in CoP analysis and was retested. The task was performed in both left and right single support to eliminate effects of limb dominance, over three trials each for a total of six trials per participant.
3.2. RMS CoP velocity (vCoP) The findings from the study revealed no significant interaction effects between group and time for M-L vCoP (Time 1: CONCUSSED = 6.40 cm/s (SD = 0.91); CONTROL = 7.94 cm/s (SD = 1.36); Time 2: CONCUSSED = 6.05 cm/s (SD = 0.93), CONTROL = 7.18 cm/s (SD = 1.20); F(1, 32) = 0.91, p = .346). In addition, there was no interaction effect between group and time for A-P vCoP (Time 1: CONCUSSED = 8.60 cm/s (SD = 1.95), CONTROL = 11.38 cm/s (SD = 2.84) and Time 2: CONCUSSED = 7.76 cm/s (SD = 1.59), CONTROL = 10.72 cm/s (SD = 2.90); F(1, 32) = 0.3, p = .864). As well, there was no main effect of time for vCoP in the M-L direction (F(1, 32) = 0.91, p = .346) or the A-P direction (F(1, 32) = 0.30, p = .137). However, a significant main effect of group was revealed for the vCoP in the M-L direction (F(1, 32) = 13.80 cm/s, p < .01, η2 = 0.30) (see Fig. 3A) as well as for A-P direction (F(1, 32) = 13.81, p < .01, η2 = 0.30). The CONCUSSED group had significantly lower vCoP in both M-L and A-P directions compared to the CONTROL group (see
2.5. Data analysis The average anterior-posterior (A-P) and medial-lateral (M-L) location of the CoP for first 5 s of each trial, prior to the onset of lights illuminating, was used as a bias and removed from the rest of the CoP calculation in order to calculate Root Mean Square (RMS) of CoP displacement (dCoP). The CoP displacement over time was differentiated to calculate the RMS of COP velocity (vCoP). Both the dCoP and vCoP were calculated in both the A-P and M-L directions.
CoPRMS =
1/ n (x12 + x 22 + …x n2) 144
Clinical Biomechanics 67 (2019) 142–147
K.M. Mitchell and M.E. Cinelli
Fig. 2. Medial/Lateral RMS dCOP (A) had no significant differences between CONC and CONTROL (F(1, 32) = 0.14, p = .908), with no changes over time (Time 1: SRC = 0.92 cm (SD 0.18), CONTROL = 1.06 cm (SD = 0.30); Time 2: SRC = 0.87 cm (SD = 0.29), CONTROL = 1.03 cm (SD = 0.23)). Anterior/Posterior RMS dCOP (B) had a significant interaction effect (F(1, 32) = 10.82, p < .05, η2 = 0.253), as CONTROL improved from Time 1 to Time 2 (Time 1: SRC = 1.54 cm (SD = 0.20), CONTROL = 1.52 cm (SD = 0.31); Time 2: SRC = 1.45 cm (SD = 0.28), CONTROL = 1.81 cm (SD = 0.33);.
greater balance impairments. The results from the current study align with previous findings that revealed no differences in M/L or A/P dCoP during static balance, in asymptomatic collegiate athletes (Powers et al., 2014). The significant interaction observed between group and time for A/P dCoP may be due to a small learning effect in the control group. However, participants were instructed to move as quickly as possible in response to the FitLights during the lower limb reaching task. Due to the nature of the lower limb reaching task in the anteriorposterior direction, greater displacement in the sagittal plane was anticipated. A small increase (approximately 3 mm) in A/P dCoP cannot confirm that learning occurred due to training effects. It is recommended that analyzing dCoP alone may not be the most reliable method of characterizing balance control in either static or dynamic conditions. The major finding from the current study was that youth hockey players who reported a previous SRC did in fact have differences in dynamic balance control in comparison to players without previous SRC over time. There was a significant main effect of vCoP indicating that athletes with a history of SRC consistently had reduced vCoP in both M/L and A/P direction. During static balance conditions,
Fig. 3).
4. Discussion The purpose of the current study was two-fold: 1) to determine whether a novel, lower limb reaching task could detect differences in balance control in youth hockey players with and without reported previous SRC; and 2) to determine if the lower limb reaching task was immune to training/learning effects over time. It was believed that the athletes with previous SRC would exhibit reduced dynamic balance control through reduced vCoP measures compared to the group without history of SRC and that the visuomotor task would be resistant to learning (training) effects in youth hockey players throughout a regular season. Similar to previous findings, there were no significant main effects of dCoP during the dynamic visuomotor reaching task in either plane between the hockey players with and without SRC over time. CoP displacement is an indirect measure of the amount of body movement (sway) produced by an individual during a trial and dCoP demonstrates one's displacement variability over a trial (Clark et al., 2018; Winter, 1995). Individuals with larger dCoP values are believed to display
Fig. 3. Medial/Lateral RMS vCOP (A) had a significant main effect of group as CONTROL had a greater velocity compared to CONC (Time 1: SRC = 6.40 cm/s (SD = 0.91); CONTROL = 7.94 cm/s (SD = 1.36); Time 2: SRC = 6.05 cm/s (SD = 0.93), CONTROL = 7.18 cm/s (SD = 1.20); (F(1, 32) = 13.80 cm/s, p < .01, η2 = 0.30). Anterior/Posterior RMS vCOP (B) had a main effect of group as CONTROL had a greater velocity compared to CONC (Time 1: SRC = 8.60 cm/s (SD = 1.95), CONTROL = 11.38 cm/s (SD = 2.84) and Time 2: SRC = 7.76 cm/s (SD = 1.59), CONTROL = 10.72 cm/s (SD = 2.90); F(1, 32) = 13.81, p < .01, η2 = 0.30). There were no significant changes in velocity over time in either plane for each group. 145
Clinical Biomechanics 67 (2019) 142–147
K.M. Mitchell and M.E. Cinelli
however, the supraspinal origins of these deficits remain unknown. Future research should be conducted to determine the differences in higher order cortical activation patterns in individuals with a history of SRC that contribute to cognitive-motor deficits. There may be differences in cortical activation patterns within areas of the frontal-parietal network and cerebellum, that may result in conservative motor behaviours and visuomotor deficits (Molinari et al., 2002).
individuals with larger vCoP values are suggested to be making more corrections (i.e., faster moving CoP) to their balance to remain upright (Echemendia et al., 2017). However, in the current paradigm, a larger vCoP in the direction of the lower limb reaching motion (i.e., sagittal plane) is thought to demonstrate greater anticipatory control. Velocity is indicative of the intensity and direction of displacement; therefore, in the A/P plane it is associated with higher order sensory integration from the vestibular and visual systems (Highstein and Holstein, 2012; Masani et al., 2003; Powers et al., 2014). It can be inferred that a higher vCoP suggests greater efficiency of the sensory systems involved in cognitive-motor integration. The youth hockey players in the current study with previous SRC had no clinical symptoms and had returned to sport, yet they performed the task slower than the control group at both test points. The slower velocity may be due to a greater reliance on visual feedback control, greater cognitive load, and more conservative behaviours during the Go/No-Go reaching task used in the current study. Similarly, dynamic gait stability is reduced as dual-task complexity is increased in adolescents two months post-SRC (Howell et al., 2015). In contrast, the differences in vCoP may be due to reduced anticipatory control and response time in the athletes with previous SRC. It is likely that athletes were not put through a rigorous rehabilitation program prior to returnto-sport. It has been suggested that a greater buffer zone between becoming asymptomatic and returning to full contact would allow for a more gradual recovery of neurophysiological mechanisms that may persist beyond the clinical recovery (Kamins et al., 2017). Additionally, both groups performed the task without significant changes in vCoP in either plane over time, suggesting that the visuomotor reaching task was immune to training effects and may be considered an accurate representation of one's balance control capabilities. The novel visuomotor reaching task seemed to be challenging enough to negate training effects of a regular hockey season and highlight persistent balance impairments in youth athletes with recent concussion. The current task may be sufficient for comparison of a youth athlete during the acute, symptomatic phase of SRC and the asymptomatic, recovery phase to an age-matched teammate without history of SRC. The findings of the current study align with previous reports that suggest that a more rigorous approach of assessing dynamic balance with a cognitive component, may be a more suitable method of testing youth athletes beyond the symptomatic stages of SRC (Howell et al., 2015; Howell et al., 2017). Further research is necessary to determine the validity of the current or a similar visuomotor task for clinical application. This study is not without a number of limitations to be considered. The first of which is the reliability of subjective reporting from youth regarding their concussion injury history and time of injury. It would be beneficial to have a record of clinical diagnosis and progress of recovery to full RTS from a designated healthcare practitioner or physician. In addition, parent(s) and/or guardian(s) should be consulted to confirm the history of concussion diagnosis in adolescents younger than the age of 16 years old. A second limitation was that there were no female participants in the CONTROL group to compare to those in the CONCUSSED group. This was due to a lower number of females within the hockey academy, and that all female participants had reported sustaining a previous concussion. Therefore, these findings cannot conclude any sex differences for dynamic balance control within this sample. A recent study reported that adolescent females with previous SRC had reduced cadence during dual-task gait compared to adolescent males with previous SRC (Howell et al., 2017). Further research should be conducted to determine the sex differences in balance control during a lower limb cognitive-motor task. Furthermore, the previous literature based on assessment of gait may coincide with the results of this study, however, the differences in the execution of dual-task gait and a visuomotor reaching task may differ in neural correlates of control. These findings suggest that dynamic balance control deficits may persist beyond clinical recovery,
5. Conclusion In conclusion, the findings of this study suggest that youth hockey players with a history of SRC may exhibit dynamic balance control deficits during a lower limb visuomotor task. These deficits were characterized by greater utilization of visual feedback and more conservative movement behaviours. The novel visuomotor task had no significant learning effects over time, which may indicate that baseline testing is not necessary. Further research should be conducted to investigate the cortical mechanisms underlying dynamic stability during a visuomotor task. Declaration of Competing Interest None. Acknowledgements The results of the study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. The authors would like to thank Simon Jones from Toronto Rehab, for developing the software for the Wii Balance board. The authors would also like to thank the Natural Sciences and Engineering Research Council of Canada (05288-2014) for support. References Allum, J., 2012. Recovery of vestibular ocular reflex function and balance control after a unilateral peripheral vestibular deficit. Front. Neurol. 3 (83). Baker, C.S., Cinelli, M.E., 2014. Visuomotor deficits during locomotion in previously concussed athletes 30 or more days following return to play. Phys. Rep. 2 (12), e12252. Buckley, T.A., Munkasy, B.A., Tapia-Lovler, T.G., Wikstrom, E.A., 2013. Altered gait termination strategies following a concussion. Gait Posture 38 (3), 549–551. Buckley, T.A., Vallabhajosula, S., Oldham, J.R., et al., 2016. Evidence of a conservative gait strategy in athletes with a history of concussions. J. Sport Health Sci. 5 (4), 417–423. Buckley, T.A., Oldham, J.R., Munkasy, B.A., Evans, K.E., 2017. Decreased anticipatory postural adjustments during gait initiation acutely post-concussion. Arch. Phys. Med. Rehabil. 98 (10), 1962–1968. Clark, R.A., Mentiplay, B.F., Pua, Y.H., Bower, K.J., 2018. Reliability and validity of the Wii Balance Board for assessment of standing balance: a systematic review. Gait Posture 61, 40–54. Cross, M., Kemp, S., Smith, A., Trewartha, G., Stokes, K., 2015. Professional rugby union players have a 60% greater risk of time loss injury after concussion: a 2-season prospective study of clinical outcomes. Br. J. Sports Med. 50 (15), 926–931. Drew, T., Andujar, J.E., Lajoie, K., Yakovenko, S., 2008. Cortical mechanisms involved in visuomotor coordination during precision walking. Brain Res. Rev. 57 (1), 199–211. Echemendia, R.J., Meeuwisse, W., McCrory, P., Davis, G.A., Putukian, M., Leddy, J., ... Schneider, K., 2017. The sport concussion assessment tool 5th edition (SCAT5). Br. J. Sports Med. 51 (11), 848–850. Ellis, M.J., Cordingley, D., Vis, S., Reimer, K., Leiter, J., Russell, K., 2015. Vestibuloocular dysfunction in pediatric sports-related concussion. J. Neurosurg. Pediatr. (3), 248–255. Haghpanah, S.A., Farahmand, F., Zohoor, H., 2017. Modular neuromuscular control of human locomotion by central pattern generator. J. Biomech. 53, 154–162. Highstein, S.M., Holstein, G.R., 2012. The anatomical and physiological framework for vestibular prostheses. Anat. Rec. 295 (11), 2000–2009. Howell, D.R., Osternig, L.R., Chou, L.S., 2015. Adolescents demonstrate greater gait balance control deficits after concussion than young adults. Am. J. Sports Med. 43 (3), 625–632. Howell, D.R., Stracciolini, A., Geminiani, E., Meehan, W.P., 2017. Dual-task gait differences in female and male adolescents following sport-related concussion. Gait Posture 54, 284–289. Howell, D.R., Lynall, R.C., Buckley, T.A., Herman, D.C., 2018a. Neuromuscular control deficits and the risk of subsequent injury after a concussion: a scoping review. Sports Med. 1–19.
146
Clinical Biomechanics 67 (2019) 142–147
K.M. Mitchell and M.E. Cinelli
Master, C.L., Master, S.R., Wiebe, D.J., Storey, E.P., Lockyer, J.E., Podolak, O.E., Grady, M.F., 2018. Vision and vestibular system dysfunction predicts prolonged concussion recovery in children. Clin. J. Sport Med. 28 (2), 139–145. McCrory, P., Meeuwisse, W., Dvorak, J., et al., 2017. Consensus statement on concussion in sport—the 5th international conference on concussion in sport held in Berlin, October 2016. Br. J. Sports Med. 51 (11), 838–847. Molinari, M., Filippini, V., Leggio, M.G., 2002. Neuronal plasticity of interrelated cerebellar and cortical networks. Neuroscience 111 (4), 863–870. Mucha, A., Collins, M.W., Elbin, R.J., Furman, J.M., Troutman-Enseki, C., DeWolf, R.M., Kontos, A.P., 2014. A brief vestibular/ocular motor screening (VOMS) assessment to evaluate concussions: preliminary findings. Am. J. Sports Med. 42 (10), 2479–2486. Powers, K.C., Kalmar, J.M., Cinelli, M.E., 2014. Recovery of static stability following a concussion. Gait Posture 39 (1), 611–614. Slobounov, S., Cao, C., Sebastianelli, W., Slobounov, E., Newell, K., 2008. Residual deficits from concussion as revealed by virtual time-to-contact measures of postural stability. Clin. Neurophysiol. 119 (2), 281–289. Winter, D.A., 1995. Human balance and posture control during standing and walking. Gait Posture 3 (4), 193–214 Dec 1.
Howell, D.R., Meehan III, W.P., Barber Foss, K.D., Reches, A., Weiss, M., Myer, G.D., 2018b. Reduced dual-task gait speed is associated with visual Go/No-Go brain network activation in children and adolescents with concussion. Brain Inj. 1–6. Kamins, J., Bigler, E., Covassin, T., Henry, L., Kemp, S., Leddy, J. J., … & McLeod, T. C. V. (2017). What is the physiological time to recovery after concussion? A systematic review. Br. J. Sports Med., 51(12), 935–940. Kontos, A.P., Reches, A., Elbin, R.J., Dickman, D., Laufer, I., Geva, A.B., Collins, M.W., 2016. Preliminary evidence of reduced brain network activation in patients with post-traumatic migraine following concussion. Brain Imaging Behav. 10 (2), 594–603. Martini, D.N., Sabin, M.J., DePesa, S.A., Leal, E.W., Negrete, T.N., Sosnoff, J.J., Broglio, S.P., 2011. The chronic effects of concussion on gait. Arch. Phys. Med. Rehabil. 92 (4), 585–589. Masani, K., Popovic, M.R., Nakazawa, K., Kouzaki, M., Nozaki, D., 2003. Importance of body sway velocity information in controlling ankle extensor activities during quiet stance. J. Neurophysiol. 90 (6), 3774–3782. Massion, J., 1992. Movement, posture and equilibrium: interaction and coordination. Prog. Neurobiol. 38 (1), 35–56.
147