Balance is one common measure integral to the diagnosis and management of a concussion because it is easily tested on the sideline and in clinical settings.1–4 Balance control requires neural processes that incorporate afferent sensory information from the somatosensory (proprioceptive), visual, and vestibular systems and integrate this feedback into accurately timed muscular responses with the appropriate magnitude to maintain stability.1,5–13 These neural structures and processes are susceptible to injury in the event of head trauma, including a concussion. A disturbance or injury anywhere in the processing or execution of this sensorimotor chain can lead to deficits in vestibular, visual, motor, or cognitive function and affect complex motor skills including balance.7,14
Balance changes and disturbances in sensorimotor integration are a common symptom of a concussion.5,15,16 A commonly used sideline balance assessment, the Balance Error Scoring System (BESS), has been shown to be insensitive to minor disturbances that may linger throughout recovery and only captures gross balance disruptions that are typically present at injury.17–21 The BESS is a version of a modified sensory organization test, sometimes called the modified Clinical Test of Sensory Interaction on Balance (mCTSIB), which is more commonly used in patient populations with balance decrements (eg, Parkinson's disease). These are all balance assessments that aim to challenge the balance system by perturbing one or more sensory inputs (vision by closing eyes and somatosensory by standing on a foam surface) and thus identifying deficits in balance. The sensory organization test and mCTSIB are typically completed on a force plate or instrumented balance system in a laboratory setting in an effort to obtain an objective measure of balance.
Athletes are able to compensate for changes in balance relatively easily and have been shown to be able to minimize postural instability under a single-task condition.22,23 To challenge the system, researchers have been implementing a dual cognitive task that requires athletes to focus on both the balance task and a cognitive task.24–29 In this paradigm, participants complete a secondary cognitive task (eg, subtracting 7s, reciting months backwards, and spelling words backwards) while doing a balance task in varying sensory conditions. The goal of these tasks is to provide a distraction task to see how athletes perform when having to use resources to complete both the balance and cognitive tasks.30
There has been some research assessing the relationship between balance and neurocognitive performance, most specifically using the Immediate Post-Concussion Assessment and Cognitive Test (ImPACT).22 It has previously been shown that visual motor speed and reaction time composite scores on the ImPACT are significantly correlated with sway index scores during the mCTSIB task. Specifically, reaction time increases and visual motor speed decreases as sway index scores increase.
Research has shown balance to be sensitive to lingering deficits following a concussion in both static and dynamic balance tasks.22,28,29,31 However, less is known in regard to balance performance while distracted with a dual-task and how this relates to neurocognitive performance and concussion history. The purpose of the current study was to assess balance performance using a mCTSIB with (dual-task) and without (single-task) a cognitive distraction. In addition, the researchers aimed to assess the relationship between balance dual-task performance, baseline neurocognitive performance, and concussion history. Understanding the relationship between neurocognitive performance and stability during a dual-task at baseline testing can help researchers and clinicians to better assess student-athletes in concussion testing.
One hundred sixty-five National Collegiate Athletic Association (NCAA) Division I student-athletes (84 male, 81 female; age: 18.2 ± 0.8 years; 45 football, 37 lacrosse, 36 soccer, 17 baseball, 13 basketball, 11 softball, and 6 volleyball) completed the single- and dual-task balance tests and the ImPACT testing. All participants agreed to participate in research in addition to their baseline concussion assessments as part of the university's concussion management protocol. All varsity student-athletes were baseline tested and none refused participation in the research. All participants were volunteers for this study and signed the informed consent forms that were approved by the university's review board.
All participants wore the same slip-resistant socks while standing comfortably with feet shoulder width apart on the Balance System SDTM (Biodex Medical Systems, Inc., Shirley, NY). The mCTSIB protocol was conducted, which includes four different conditions: eyes open firm surface, eyes closed firm surface, eyes open foam surface, and eyes closed foam surface (single-task). For the dual-task condition, participants did the same balance tasks while counting backward by 7s starting at a random 3-digit number (serial 7s task; eg, they may be given the number 932 and would have to subtract 7 consecutively: 925, 918, 911, etc.). Responses for the cognitive task were recorded and accuracy of cognitive performance was determined as the percentage of the number of right responses to the total number of responses. Cognitive performance was calculated only to determine that the participants were indeed attending to the cognitive task while balancing on the Biodex Balance System. Single-and dual-tasks were counterbalanced across participants, but within each participants performed conditions in the order of eyes open firm, eyes closed firm, eyes open foam, and eyes closed foam. Participants became familiar with the platform in a practice trial. Each condition trial was 30 seconds; a brief rest (< 30 seconds) occurred between each condition.
Sway index values were obtained directly from the Biodex Balance System. The sway index represents the standard deviation of the amount of sway with higher values of the sway index suggesting more sway performed by the participant. The sway index ranges from 0 to 4 (1 = minimal sway; 4 = fall). Recorded data were extracted using the Patient Data Collection Software at 20 Hz (Biodex Medical Systems, Inc.). Several measurements related to kinematic characteristics of center of pressure were calculated using custom scripts written using MATLAB software (MathWorks, Natick, MA). Mediolateral and anteroposterior range, total path length, and 95% elliptical sway area in addition to sway index scores were analyzed.22,32
To assess the impact of the sensory manipulations, sensory ratio scores were calculated for both the single-and dual-tasks.33,34 The vision ratio compared eyes open firm/eyes closed firm. The proprioception ratio compared eyes open firm/eyes open foam. The vestibular ratio compared eyes open firm/eyes closed foam. These sensory ratios were calculated for the sway index, and kinematic variables for both single- and dual-tasks.
All participants completed the baseline version of the ImPACT concussion management software (version 4.0; ImPACT Applications, Inc., Pittsburgh, PA). This Windows-based program is module based and takes approximately 30 minutes to complete. First, demographic information and health history was collected. Next, the neurocognitive tests, involving testing for attention span, working memory, recall, and response variability, were performed. The composite scores were used in this study and include: verbal memory, visual memory, visual motor speed, and reaction time. Most studies have demonstrated good test–retest reliability,35–37 whereas others have shown poor reliability.38
Accuracy of cognitive performance during the dual-task was assessed using one-way analysis of variance across the four conditions of the mCTSIB. This was done as a manipulation check to ensure participants were attending to the cognitive task. A 2 vision (eyes open or closed) × 2 surface (firm or foam) × 2 cognitive load (single- or dual-task) repeated measures multivariate analysis of variance was performed on all dependent variables (sway index and balance kinematic measures). In addition, a 2 cognitive load (single- or dual-tasks) multivariate analysis of variance was conducted for the vision, proprioception, and vestibular ratios. If either multivariate analysis of variance was significant, univariate analyses were reported. Partial eta-squared values are reported (0.01 = small effect size; 0.09 = medium effect size; 0.25 = large effect size). Pearson correlations were conducted across sway index and balance kinematic measures for sensory ratios and ImPACT composite scores in both single- and dual-tasks to examine the relationship between variables. Regression analyses were conducted for the sway sensory ratios to determine whether neurocognitive variables could predict sway ratio. The first step entered was number of previous concussions because it may influence neurocognitive performance.39 For the second step, the neurocognitive performance variables were entered in a stepwise manner to determine whether any were predictive of balance ratios. Significance was set at a P value of .05 for all analyses.
The mean cognitive performance was between 88% and 92% accuracy across all conditions with no significant differences (P > .05). This accuracy confirms participants did pay attention to the cognitive task during the distraction dual-task across all sensory conditions.
Balance Kinematic Measures
Multivariate analysis found significant effects for vision (F [5, 160] = 318.78, P < .001), surface (F [5, 160] = 562.35, P < .001), cognitive load (F [5, 160] = 33.41, P < .001), surface × cognitive load (F [5, 160] = 4.973, P < .001), vision × cognitive load (F [5, 160] = 17.87, P < .001), surface × vision (F [5, 160] = 194.35, P < .001), and surface × vision × cognitive load (F [5, 160] = 10.31, P < .001).
Means and standard deviations and results of univariate tests are reported in Table 1. All main effects and interactions were significant for sway index, mediolateral range, anteroposterior range, sway area except for cognitive effect, and total path length. Effect sizes are reported.
Mean ± SD and Significant Effects With Effect Sizes (η2) for Sway Index and Kinematic Balance Measures
Means and standard deviations for sensory ratios for all kinematic measures for both cognitive conditions are reported in Table 2. Significant Pearson correlations between composite scores (verbal memory, visual memory, visual motor speed, and reaction time) of the ImPACT and sensory ratio for the distraction dual-task are reported in Table 3. There were no significant correlations between ImPACT composite scores and sensory ratios in the single-task (P > .05) or the visual and proprioception ratios in the distraction dual-task (P > .05).
Cognitive and Non-cognitive Means ± SD for the Vision, Proprioception, and Vestibular Ratios
Correlations Between Composite ImPACT Scores and Vestibular Ratios for Sway and Kinematic Balance Measurements During the Distraction Dual-Task
A stepwise multiple regression was conducted to evaluate whether both the number of concussions and ImPACT composite scores predict the sway score vestibular sensory ratio in the distraction dual-task (VestSwayCog). At step 1 of the analysis, the number of concussions was entered into the regression equation and was significantly related to VestSwayCog (F [1, 162] = 5.10, P = .025; R2 = 0.031). At step 2, the only ImPACT composite score that entered the equation was visual motor speed composite (F [2, 161] = 4.91, P = .008, R2 = 0.058). Verbal memory, visual memory, and reaction time (P > .05 for all) did not enter the equation at step 2 of the analysis.
Overall results indicate that the student-athletes' balance performance declined when tested with their eyes closed and/or standing on a foam surface and/or while performing a dual-task. The vision × surface × cognitive load interaction suggests that student-athletes are affected by the distraction dual-task differently depending on vision and surface conditions. Specifically, in the eyes closed foam condition, measurements decreased and moved to a more “stable” position in the distraction dual-task, whereas in all other conditions measurements increased and moved to a less “stable” position in the dual-task condition. What exactly this means is difficult to determine, except that student-athletes' strategy of control is different in this specific condition and may suggest the combination of the task requirement changes attentional demands and consequently strategies of control. Perhaps the demands of maintaining balance control during the eyes closed foam condition while performing a concurrent cognitive task were so challenging that it required the athletes to adopt a “posture-first” strategy. Such differences in adopting a particular strategy have been documented in other populations.40
Sensory ratios (vision, proprioception, and vestibular) showed significant changes with the distraction cognitive dual-task with all ratios increased closer to the control condition (eyes open firm) numbers for each variable. This is similar to previous research, which has shown more stability and need for vestibular control with a cognitive dual-task.41–43 Although these results are not robust, it may suggest that they either attended more to the balance task using the posture-first strategy40 or that they compensated and adopted a more conservative balance strategy in the distraction dual-task to attend to the cognitive task. Another possibility may be that most of the student-athletes are used to playing under dual-task conditions (performing motor and cognitive tasks concurrently). This could potentially explain why they performed better under the dual-task condition compared to the single-task condition.
When these sensory ratios were correlated with neurocognitive performance, the vestibular ratio scores were significantly correlated with the visual motor composite scores. Student-athletes with higher visual motor scores had “less movement” in balance performance (sway area, anteroposterior range, and total path length), suggesting that student-athletes with higher visual motor processing speeds are able to maintain stability with less movement/lower sway scores. These findings are consistent with previous work by Evans et al.22 We cannot conclude from our data whether this is related to cognitive or attentional resources.
These results should only be clinically considered with skepticism because these correlations were low. There may potentially be implications for sport performance and injury risk, but more research is needed. Faster visual motor processing speeds may allow student-athletes to process their surroundings while making quick decisions and performing with speed and accuracy. Compromised visual motor speeds have been associated with higher anterior cruciate ligament injury and concussion risk.44 Additionally, deficits in balance and gait and visual motor processing have been preliminarily linked to musculoskeletal injuries. Research and injury prevention centers that train balance in conjunction with visual motor training show a reduction of injuries across the season.5,45 Research has shown previously that concentration on balance leads to more stability (decreased sway), but the natural way to balance is an unconscious process and some sway and range of motion is normal.42,43 Thus, changes from natural sway in either the positive or negative direction may be meaningful.1,6,22,26–29,46
Our data suggest that visual motor processing speed and number of concussions are predictive of performance on the balance task in the vestibular dual-task condition. Previous research has shown that the vestibular system is often disrupted with concussive injury; therefore, measurements that easily assess these potential deficits may be meaningful to clinicians.47–49 In addition, individuals with a history of concussions tend to have lingering vestibular deficits.47,48 Thus, the combination of this information may suggest that better understanding the link between visual motor processing speeds and balance performance may be important for both prevention and monitoring recovery in student-athletes.
Limitations of this study include the resolution of the Biodex Balance System. This is a system that is used clinically and so it is helpful to understand kinematic changes that may be occurring that are not captured by the sway score alone. It is of course not as detailed as a force plate with a higher sampling rate, which should be considered when interpreting data. From these data, however, the sway scores are giving us information similar to the underlying kinematics at this resolution.
Cognitive accuracy was measured; however, we did not measure speed of answers or control for it. We did measure accuracy across conditions that were unchanged (ranging from 88% to 92% accuracy, P > .05), but it is possible that participants could have slowed down answering speed to focus on balance. In addition, we randomized the starting number for the serial 7s cognitive load tasks and thus the number of answers completed could have been dependent on the task. This should also be considered in the interpretation of results. We do know that participants paid attention to the cognitive task and attempted to answer quickly and accurately in all conditions, which was the goal of our distraction task.
Implications for Clinical Practice
Due to the fact that most concussion management protocols include measures of balance at baseline, on the sideline, and after concussion, these measures should challenge the various systems involved with balance and should include perturbations to vision (eyes open and closed), surface (firm vs foam), and cognition (balance alone or with dual-task). This will allow for a more comprehensive picture of what the athlete is experiencing and where potential deficits may be occurring. Additionally, the findings in this study that visual motor processing speed might be related to balance, specifically the vestibular ratio, may suggest that visual motor processing speed in conjunction with balance scores or concerns about balance should be considered in making return-to-play decisions. Additionally, the link between visual motor processing speeds and balance performance may be important for prevention and could lead to interventions to train the visual system. These findings also suggest that there is still much unknown about what is considered “good” balance and objective balance measures may need to be used with caution.
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Mean ± SD and Significant Effects With Effect Sizes (η2) for Sway Index and Kinematic Balance Measures
|Parameter||Eyes Open Solid||Eyes Closed Solid||Eyes Open Foam||Eyes Closed Foam||Significant Effects/Effect Size (η2)a|
|Mediolateral range (cm)|
| Cognitive||0.70 ± 0.29||1.01 ± 0.67||1.7 ± 1.35||5.17 ± 1.81||V (0.76); S (0.88); C (0.08); V×C (0.17); S×C (0.07); V×S (0.74); V×S×C (0.11)|
| Non-cognitive||1.19 ± 1.08||1.35 ± 0.87||2.29 ± 1.23||4.69 ± 1.75|
|Anteroposterior range (cm)|
| Cognitive||1.26 ± 0.49||2.14 ± 0.91||2.24 ± 0.81||7.17 ± 2.02||V (0.85); S (0.90); C (0.13); V×C (0.28); S×C (0.09); V×S (0.78); V×S×C (0.1)|
| Non-cognitive||2.11 ± 1.49||2.61 ± 1.51||3.35 ± 1.64||6.55 ± 1.64|
|Sway area (cm2)|
| Cognitive||0.93 ± 0.66||2.32 ± 2.07||4.52 ± 8.1||39.32 ± 23.87||V (0.71); S (0.79); C (NS, 0.003); V×C (0.18); S×C (0.10); V×S (0.70); V×S×C (0.20)|
| Non-cognitive||3.28 ± 6.39||4.26 ± 5.94||9.12 ± 12.09||31.87 ± 17.3|
|Total path length (cm)|
| Cognitive||19.52 ± 5.99||29.64 ± 10.95||36.54 ± 11.56||113.73 ± 43.74||V (0.82); S (0.85); C (0.21); V×C (0.18); S×C (0.11); V×S (0.77); V×S×C (0.13)|
| Non-cognitive||29.66 ± 15.1||38.15 ± 17.09||46.74 ± 22.76||109.15 ± 39.79|
|Sway index (0–4 range)|
| Cognitive||0.45 ± 0.15||0.7 ± 0.27||0.81 ± 0.26||2.53 ± 0.61||V (0.88); S (0.93); C (0.18); V×C (0.36); S×C (0.11); V×S (0.84); V×S×C (0.19)|
| Non-cognitive||0.73 ± 0.49||0.87 ± 0.46||1.17 ± 0.49||2.32 ± 0.53|
Cognitive and Non-cognitive Means ± SD for the Vision, Proprioception, and Vestibular Ratiosa
|Parameter||Vision Ratio||Proprioception Ratio||Vestibular Ratio|
| Cognitive||0.69 ± 0.28||0.58 ± 0.23||0.18 ± 0.08|
| Non-cognitive||0.88 ± 0.41b||0.67 ± 0.38d||0.32 ± 0.21b|
| Cognitive||0.80 ± 0.38||0.46 ± 0.38||0.15 ± 0.08|
| Non-cognitive||0.96 ± 0.53c||0.55 ± 0.35c||0.27 ± 0.23b|
| Cognitive||0.65 ± 0.28||0.59 ± 0.27||0.19 ± 0.09|
| Non-cognitive||0.86 ± 0.40b||0.67 ± 0.38d||0.33 ± 0.21b|
| Cognitive||0.56 ± 0.49||0.28 ± 0.19||0.03 ± 0.03|
| Non-cognitive||0.91 ± 0.88a||0.41 ± 0.43a||0.11 ± 0.19b|
|Total path length|
| Cognitive||0.69 ± 0.16||0.55 ± 0.14||0.19 ± 0.07|
| Non-cognitive||0.81 ± 0.33b||0.67 ± 0.28b||0.29 ± 0.15b|
Correlations Between Composite ImPACT Scores and Vestibular Ratios for Sway and Kinematic Balance Measurements During the Distraction Dual-Taska
|Vestibular Ratio||Verbal Memory||Visual Memory||Visual Motor Speed||Reaction Time|
|Sway index||NS||NS||−0.18, P = .02||NS|
|Mediolateral range||NS||NS||−0.19, P = .01||NS|
|Anteroposterior range||−0.15, P = .05||NS||NS||NS|
|Sway area||NS||NS||−0.15, P = .05||NS|
|Total path length||NS||NS||NS||NS|