How sensory reweighting is affected by repetitive head impacts and concussions
Date
2022
Authors
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Publisher
University of Delaware
Abstract
BACKGROUND: There is a growing concern of detrimental effects on postural control due to long-term exposure to repetitive head impacts (RHI) and concussion and their recovery. Although studies have shown that RHI may not affect postural control, there remains concern about whether RHI may contribute to chronic traumatic encephalopathy. On the other hand, the concussion has been challenging to diagnose, assess, and manage due to the heterogeneity of post-concussion signs and symptoms. Postural control assessments have been used to investigate, measure, and manage concussions. Postural control is dependent on the fusion of multiple sensory modalities (vision, vestibular, and proprioceptive) for accurate estimation of body dynamics. We have developed a paradigm (i.e., 3-modality) that can assess how the nervous system changes the emphasis (i.e., reweights) of different modalities due to changing environmental conditions or neurological injury to help us understand potential mechanisms underlying such postural control deficits. ☐ While many studies confirm a relationship between concussion and impaired postural control, this dissertation research took the additional innovative step of addressing a particular mechanism that may contribute to the impairment, namely, sensory reweighting. The need for such work is motivated by current clinical assessments, often deemed too coarse to capture subtle deficits in postural control and risk premature return-to-play. While there may be other mechanisms underlying postural control deficits due to concussions, we have developed an innovative paradigm for sensory reweighting that has been used only sparingly concerning concussions. Here, four novel studies using the 3-modality paradigm could address such a gap in how we use sensory reweighting for postural control after RHI and concussion. This novel proposed paradigm may shift the RHI and concussion research paradigms for several reasons: ☐ Aim 1: A longitudinal study was applied to a contact sport using the 3-modality paradigm for the first time. We also addressed how deficits in postural control due to RHI develop and how long they may persist. Hypothesis 1a: We predict a transient sensory reweighing impairment immediately post-season compared to pre-season. Sensory reweighting will return to the baseline 2-3 months post-season. Hypothesis 1b: The sensory reweighting deficit will result in diminished upright posture control. ☐ Aim 2: Since we prospectively assessed concussion recovery, we determined if people who sustained a concussion have any residual deficits post-acutely and beyond reported clinical recovery time. Moreover, we will be able to determine whether any sensory system remains impaired. Hypothesis 2a: A sensory reweighting impairment will be evident within the first-week post-concussion. Hypothesis 2b: In the two subsequent evaluations (i.e., 2 and 4 weeks), sensory reweighting will be gradually less impaired but still impaired compared to controls. ☐ Aim 3: Sensory reweighting for postural control has not been studied in the PPCS population. Therefore, such an approach may explain why such symptoms persist. Hypothesis: An impairment in sensory reweighting will remain four weeks post-concussion compared to controls. ☐ Aim 4: We investigated how concussion history affects sensory reweighting for upright stance. Hypothesis: An impairment in sensory reweighting will remain after a year post-concussion compared to controls. ☐ PURPOSE: This dissertation focuses on whether inappropriate sensory reweighting contributes to postural control impairments after a concussion or after repetitive head impacts across a season of rugby. ☐ METHODS: Participants experienced simultaneous visual (virtual reality environment), vestibular (galvanic vestibular stimulation(GVS)), and proprioceptive (vibration to the Achilles tendon) stimuli at different frequencies to examine the independent contributions of each sensory system to upright stance control. There were two visual conditions (high-low amplitude) and two vibration conditions (on-off) to examine sensory reweighting. GVS was constant in each condition. Online surveys via Qualtrics assessed demographic information, sports participation history, medical history, daily living, and participant psychological history (e.g., psychiatric disorders, ADD/ADHD, Learning disability, etc.). On the day of the data collection, they completed the following online questionnaires: Post-Concussion Symptom Scale (PCSS), Brief Symptom Inventory (BSI-18), Dizziness Handicap Inventory (DHI), PTSD Checklist (Civilian Version (PCL-C)), Sleep Quality Assessment (PSQI), Resilience Scale, Short Form Health Survey (SF-12), Satisfaction with Life Scale (SWLS), Trail Making Test, Vestibular Ocular Motor Screening (VOMS), and the Sports Concussion Assessment Toll - 5th edition (SCAT-5). All questionnaires were applied to aims 2 and 3. This 3-modality protocol was used for the four aims of this dissertation on different populations: (Aim 1) 18 Female collegiate Rugby players (20±1.3 years) across three-time points (i.e., at pre-season, post-season, 2-3 months after post-season). A linear mixed model t by the restricted estimation maximum-likelihood was used to compare gain and phase relative to each sensory modality across time; (Aim 2) 8 acuteconcussed participants (23.9±3.4 years) were assessed three times (i.e., at 1-week, 2-weeks, and 4-weeks post-concussion), and 16 health matched controls (22.6±3.7 years) were evaluated once. For questionnaire outcomes, a Mann-Whitney test was performed for continuous variables, and Chi-Square (2) tests were used to determine if there were statistically signicant associations for nominal variables. For sensory reweighting outcomes, a between-groups repeated measures analysis of variance (ANOVA) was performed with Bonferroni adjustments for multiple comparisons; (Aim 3) 13 participants (24.1±5.5 years) with persistent post-concussive symptoms (i.e., more than 28 days post-concussion) were assessed once and compared with 13 health matched controls (23.5±5.5 years). For questionnaire outcomes, independent samples t-tests were used for continuous variables, and Chi-Square (2) tests were used to determine if there were statistically signicant associations for nominal variables. For sensory reweighting outcomes, a between-groups repeated measures analysis of variance (ANOVA) was performed with Bonferroni adjustments for multiple comparisons; and (Aim 4) 29 participants (21.4±3.6 years) with a history of concussion between 1 to 3 years after their last concussion was assessed and compared with 29 (21.5±3.6 years) matched healthy controls. A between-groups repeated measures analysis of variance (ANOVA) was performed with Bonferroni adjustments for multiple comparisons, and a repeated measures ANCOVA to test the effects of time of concussion (co-variant) for the group with a history of concussion. ☐ RESULTS: For Aim 1, there was a significant effect (p<0.05) for time on gain to GVS, Center of Mass (CoM) 95% area, and CoM sway velocity, whereas participants showed higher gains to GVS (p<0.05), greater 95% area (p<0.05), and greater sway velocity (p<0.05) at post-season than pre-season and 2-3 months after post-season. For Aim 2, the concussed group showed significance (p<0.05) on the following questionnaires: total number of symptoms, symptom severity score, BSI-18, DHI, PCL-C, MCS-12, and VOMS compared to healthy controls. There was no statistical difference in main effects for group and interactions for any dependent variable. For Aim 3, there was a significant association (p<0.05) for migraine history, depression history, and VOMS. There was a significant effect (p<0.05) for a total number of symptoms, symptom severity score, modified Balance Error Scoring System (BESS), BSI-18 (total score), BSI-18 somatization score, BSI-18 depression score, BSI-18 anxiety score, DHI, PCL-C, PSQI, Resilience Scale, PCS-12, MCS-12, and SWLS. The persistent post-concussive symptoms (PPCS) group had higher scores than healthy controls for all listed variables. There was a significant effect (p<0.05) for gains, CoM 95% area, and CoM sway velocity, where the PPCS group showed higher gains to GVS (p<0.05) and gains to vision (p<0.05), greater 95% area (p<0.05), and greater sway velocity (p<0.05). For Aim 4, there was no statistical difference in main effects for group and interactions for any dependent variable. No effects were also found when controlling for the time of concussion for the history of the concussion group. ☐ CONCLUSION: RHI may cause a transient effect on postural control after a season of contact sport. The Rugby players showed maladaptation because they presented greater CoM area and sway velocity. Participants who sustained a concussion acutely recovered their decits in sensory reweighting within the first-week post-concussion, even though within the first-week, they showed poorer questionnaire outcomes than controls. Individuals with PPCS showed sensory reweighting impairments, which may play a role in their incomplete recovery and diminished postural control. After at least one year post-concussion, our cohort could properly reweight their sensory system to maintain an upright posture. Investigating sensory reweighting can help us to understand the underlying mechanism of postural control impairmentsand can capture subtle postural control decits due to RHI and concussions (i.e., individuals who sustained PPCS). Moreover, this assessment can help clinicians: designmore precise rehabilitation interventions and prevent premature return-to-play decisions, consequently reducing the risk of subsequent concussion and/or musculoskeletal injury.
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Keywords
Sensory reweighting, Repetitive head impact, Concussion