Twelve athletes sustained a concussion during their athletic season. Fourteen control athletes without concussion, matched by youth or collegiate level, were evaluated after competition/practice. For players who had a concussion, changes in scores from baseline were significant for both the K-D test (P = 0.002) and the timed tandem gait (P = 0.02, Wilcoxon signed-rank test, Table 1). Among concussed athletes, K-D worsened from baseline by an average of 5.2 seconds vs improvement by 6.4 seconds for nonconcussed control athletes.
In terms of continuous test scores, K-D showed the greatest capacity to distinguish concussed vs control groups based on changes from preseason baseline ROC curve areas from logistic regression models, accounting for age were K-D = 0.92, timed tandem gait = 0.87, and SAC = 0.68 (P = 0.0004 for comparison of ROC curve areas, Fig. 3A). A composite of tests including SAC, timed tandem gait, and K-D together (ROC curve area = 0.97) was a greater discriminator of concussed vs control athlete groups than was the combination of SAC and timed tandem gait as used in the SCAT3/Child-SCAT3 (ROC curve area, 0.88, Fig. 3B). The combination of timed tandem gait and K-D (ROC curve area = 0.98) was nearly identical to the composite of 3 tests (ROC area = 0.97). This means that athletic trainers had a 92% probability of correctly distinguishing a concussed vs nonconcussed athlete based on the result of the K-D test alone.
When the test scores were analyzed using published cutoffs for worsening from baseline in the setting of concussion, the SAC showed a 2 point or more worsening (12) in 2/10 concussed players (20%) and 3/14 controls (21%). The timed tandem gait showed worsening in 10/12 concussed players (83%) and 5/14 controls (36%). K-D times demonstrating worsening in 9/12 (75%) concussed players and 1/14 controls (7%).
Results of this investigation demonstrate that adding a rapid simple vision-based performance measure to cognitive and balance tests enhances the detection capabilities of current sideline assessments for concussion. Because rapid number naming captures visual function, K-D is a useful tool to aid in the diagnosis of concussed athletes at all levels of sport (14–16,19–22). Use of a measure that requires saccadic eye movements is particularly effective for several reasons. Studies have shown that patients with impaired saccades postconcussion have both cortical and subcortical deficits. These deficits correlate with worse scores for quality of life assessments (24). Saccadic eye movements require relay of information throughout the brain, including frontal eye fields, supplementary eye fields, dorsolateral prefrontal cortex, intraparietal sulcus, and deeper structures of the brainstem (25–27). Eye movement testing enables the analysis of a number of circuits throughout the brain including visual–spatial integration, motor planning, attention, motivation, and spatial organization (26). The wide distribution of neuronal networks required for saccades thus makes a vision-based sideline screening test particularly effective.
The K-D test has been successful in identifying concussion in boxers and Mixed Martial Arts fighters. In those studies, worse K-D scores were associated with lower scores for the Military Acute Concussion Evaluation, a brief cognitive test, both postfight (rs = −0.79, P = 0.0001) and regarding changes from prefight baseline (rs = 0.90, P < 0.0001) (19). Worsening of K-D times was associated with worsening SAC immediate memory scores (P < 0.001, R2 = 0.62) (16). Studies have shown that K-D scores correlate with Immediate Post-Concussion Assessment and Cognitive Testing (IMPACT) subscores that are visual in nature (14, 17, 28). As an added benefit, the K-D test can accurately and easily be performed by non-medically trained observers, including parents of youth athletes (18).
Another factor that adds to the simplicity and relevance of the K-D test in youth athletes is the use of preseason baseline scores. Baseline scores obviate the need for parents or others on the sidelines to determine normative values in the acute setting of an injury. Furthermore, as shown in this study, K-D time scores decrease (improve) with advancing age of youth athletes. Although these factors make determination of new baseline scores essential at the start of each athletic season, the use of baseline scores eases interpretation when time is of the essence. Using modern definitions, a concussion should be suspected when an athlete has 1) an impulse blow to the head or body and 2) any new neurological symptom. Tests such as K-D, therefore, are used to remove some of the guesswork from this process and should not substitute for clinical or parental judgment that a concussion has occurred.
In our youth athlete cohort, worse scores were noted among younger players for all sideline tests. K-D time scores in particular were significantly slower for younger players (P < 0.001). This association with age and improved overall K-D scores (faster times) could be explained by developmental changes in saccadic eye movements and cognition. Diffusion tensor imaging MRI studies have shown that both white matter and gray matter changes continue in the frontal lobes throughout childhood (29). Eye movement tasks, which require frontal lobe circuits, begin to reach stabilization around adolescence, in concert with other developmental changes in the brain (29).
Saccades have been described by their components: peak velocity, latency, and accuracy. Although changes in velocity of saccadic eye movements with age have been inconsistently described, saccadic latency decreases throughout childhood. Changes in accuracy also stabilize with age (29). Age-related changes in saccade latency and accuracy may extend beyond the ocular motor system and may reflect changes in cognitive processing (29). The K-D test, which requires saccadic eye movements with a superimposed cognitive task, may also be impacted by the normal developmental changes of the brain with age and that may explain the improved times we observed with increasing age.
Performance on test card 3 with the greatest degree of vertical visual crowding had the most variability in terms of testing times. Scores on this card improved with older age within the cohort of athletes younger than 18 years (Fig. 2, P < 0.001, linear regression). It is suspected that the effect on this specific card may also be secondary to visual crowding, an age-dependent ability to visualize objects among clutter (30).
Future studies of the K-D test will explore the possibility of age-related norms. In this study, baseline scores for collegiate athletes averaged 38.4 seconds, very similar to collegiate athlete scores in previous studies (average 37.0 seconds, range 36.0–40.2 seconds) (15). Reference ranges for baseline scores in children are under development; these are likely to correlate with age as suggested by our results and by literature suggesting an impact of the changing brain on measures of saccadic eye movement performance (30). Studies are also ongoing to examine the eye movement dynamics and correlates of K-D test performance using formal eye movement recordings. These investigations will determine how prolonged K-D test times may relate to transient slowing of saccades, saccadic inaccuracy, increased latency, or a combination of these factors. The potential role for antisaccades in eye movement-related tasks after concussion will also be examined.
To our knowledge, this is the first investigation to examine the use of timed tandem gait in children. Our data show that the timed tandem gait is a potentially useful tool in the assessment of concussions in youth athletes. In terms of sensitivity in our cohort, the timed tandem gait fell only slightly behind the K-D test as a diagnostic tool. Further investigation will determine test–retest reliability. In this cohort, we did not find SAC testing to be helpful in distinguishing the concussed athlete. A previous study of the SAC in a pediatric cohort presenting to the emergency department for concussion also did not find a significant difference in scores vs nonconcussed controls (31). Baseline SAC scores in youth populations can be very low, as observed in our study, making it difficult to find a decrement in SAC scores after concussion in certain athletes. Similar to the timed tandem gait, SAC testing requires further validation in youth population.
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