Vestibular and ocular motor impairments have been commonly recognized following concussion and contribute to postconcussion symptoms.1,2 Studies have shown up to 80% of youths show vestibular and ocular abnormalities following concussion.1 Vestibular and ocular motor-related symptoms potentially include headache, dizziness, nausea, fogginess, and imbalance.3,4 Vestibular and ocular motor-related signs and symptoms have been associated with a longer duration of postconcussion symptoms,2,5 a longer time to return to full academic activities,1,5 and a longer time to return to full sport activities.1,6–8 Given the high prevalence and the prognostic utility of vestibular impairments and vestibular and ocular motor-related symptoms, accurate identification is critical. Furthermore, Reneker et al9 demonstrated improved recovery from concussion associated with early initiation of vestibular physical therapy targeting vestibular-ocular dysfunction.
The Vestibular/Ocular Motor Screening (VOMS) has been established as an important and commonly used screening tool in the evaluation of vestibular and ocular motor-related symptoms after concussion.3 Patients with positive VOMS assessments have been shown to experience longer recovery from concussion.6 The VOMS has been shown to have strong internal consistency and low false-positive rates in youth athletes.10–12 However, a VOMS assessment completed in a typical office setting while the patient is at rest may miss cases of vestibular-ocular dysfunction that are only provoked by physical exertion and could be suggestive of ongoing concussion deficits that warrant proper identification and targeted treatment.13 Failure to detect ongoing vestibular and ocular motor impairments with proper exertional tasks may be associated with reemergence of symptoms after return to sports, increased risk for subsequent injuries after concussion,14,15 and suboptimal sports performance.
The role of physical exertion in the management of sport-related concussion has been increasingly recognized. Supervised exercise challenges (SECs) have been used in the evaluation of sport-related concussion and have become an important tool in concussion management both in determining safe return-to-play and in guiding the rehabilitation of lingering concussion symptoms with interventions like subsymptom threshold exercise and vestibular physical therapy.16–18 Recent studies demonstrate the feasibility and clinical utility of SECs completed during an office visit, in part to determine recovery from concussion as measured by the presence or absence of symptom provocation. When used in addition to a comprehensive concussion evaluation, an SEC can inform management trajectories in patients who experience symptom reemergence or provocation with exercise.13 Some SECs include forms of dynamic exercise and may enhance the detection of vestibular and ocular motor-related symptoms that may otherwise be missed by SECs including only forms of aerobic exercise.13 Vestibular and ocular motor-related symptoms are movement-specific and therefore may be properly identified using various forms of physical exertion. While a period of rest after physical exertion may be recommended for some concussion evaluation tools, such as balance and cognitive testing,19–21 the VOMS demonstrated a stable response after physical exertion in healthy individuals.22 This raises the possibility that, when VOMS is performed after physical exertion, increased symptom provocation in concussed individuals is related to ongoing effects of concussion. The influence of an SEC on the VOMS performance in concussed athletes has not been examined. Since vestibular and ocular motor-related symptoms are both common following concussion and associated with worse recovery outcomes, identifying their provocation by physical exertion would have the potential to inform targeted rehabilitation and to promote recovery.4,23,24 Furthermore, failing to identify ongoing concussion symptoms that are only provoked through exertion may lead to a premature and unsafe return to sports.
The objective of this study was to determine whether an SEC increases the detection of vestibular and ocular motor-related symptoms. We hypothesized that concussed athletes undergoing an SEC will exhibit greater symptom provocation with the VOMS compared with a VOMS assessment performed at rest prior to an SEC.
Participants (58.3% male; n = 21/36) were prospectively recruited from a multidisciplinary sport concussion clinic at a tertiary care center to participate in this cross-sectional study. Participants who were eligible for this study were athletes between 10 and 18 years old diagnosed with concussion and receiving their clinical care within 30 days of injury. The concussion diagnosis was made by a physician who specializes in the care of sport-related concussion, in accordance with the most recent consensus statement on concussion in sport.25 Participants were excluded if they were receiving care for their concussion beyond 30 days of injury, if they were assessed to have recovered from their concussion, or if they had any medical contraindication to exercise, such as a cardiovascular, respiratory, or musculoskeletal comorbidity that would preclude safe participation. Table 1 lists relevant participant characteristics. This study was approved by the institutional review board at the authors' institution, and informed consent was provided for all participants.
Table 1 -
|Days from concussion to study visit
|Number of endorsed symptoms on SCAT5 at study visit (total 22)
|SCAT5 symptom severity score at study visit (total 132)
|Resting heart rate prior to SEC
|Average heart rate during SEC
|Peak heart rate during SEC
Abbreviations: SCAT5, Sport Concussion Assessment Tool, version 5; SEC, supervised exercise challenge.
Vestibular/Ocular Motor Screening
As part of this research study, VOMS assessments were performed as originally described by Mucha et al.3 VOMS assessments were completed immediately prior to and immediately following a standardized SEC protocol, described later. The VOMS items were performed in the following order: smooth pursuits, horizontal saccades, vertical saccades, near point of convergence (NPC), horizontal vestibulo-ocular reflex (VOR), vertical VOR, and visual motion sensitivity. Participants were queried about the presence of headache, dizziness, nausea, and fogginess, and they were asked to rate each symptom on a 0- to 10-point Likert scale at baseline prior to the resting VOMS assessment and following each component of the assessment. A score of 0 was defined as “absent” and a score of 10 was defined as “severe.” At baseline and for each testing item, a total symptom score was calculated by combining the individual scores for each of the 4 symptoms. Symptom change scores were used to determine symptom provocation for the individual VOMS items by subtracting the total baseline symptom score from the total symptom score for each VOMS item. For instance, if a participant's baseline total symptom score equaled 4, and their total symptom score for smooth pursuits equaled 6, then the symptom change score for smooth pursuits was 2. A symptom change score increase of 2 points or more compared with the total baseline score was considered positive symptom provocation for that item. This scoring method is consistent with the scoring method in the original VOMS investigation,3 as well as subsequent investigations examining various aspects related to VOMS.11,26 In addition to a symptom score, the NPC distance was measured from the point at which the participant reported diplopia on a target moving slowly toward their face. A tongue depressor with a 14-point font “X” at the tip was used as the target. The distance was measured using a ruler from the tip of the nose. Diplopia reported greater than 5 cm from the tip of the nose was considered a positive finding. When the VOMS was administered after the SEC, baseline symptoms were queried again, and a corrected post-SEC VOMS baseline symptom score was calculated by subtracting the raw postexercise VOMS baseline score minus the preexercise VOMS baseline score. The corrected post-SEC VOMS baseline adjusted for the increase in symptom provocation that occurred during the SEC and enabled the quantification of symptom provocation patterns occurring during VOMS items conducted after physical exertion. The same examining physician completed all VOMS assessments.
Supervised Exercise Challenge Protocol
As part of the study, each participant completed a standard SEC protocol guided by an athletic trainer in a gym space located at the clinic. The SEC protocol was adapted from previously studied protocols.13,18 The same athletic trainer directed all SECs, and all participants were taken through identical exercise protocols. Each SEC began with an aerobic SEC consisting of a 16-minute stationary bike workout. The goal of this portion of the SEC was to elevate heart rate while limiting the participant's body motion. A Keiser M3i (Fresno, California) stationary bike was used for all SECs. The workout began at a low intensity, corresponding to a low pace and resistance, which were then gradually increased in pace and/or resistance at 2-minute intervals. For instance, during the first 2-minute interval, a pace of 50 to 75 revolutions per minute (RPM) was targeted at a resistance setting of 3, corresponding to approximately 15 to 20 W. During the final 2-minute interval, participants cycled at a pace of 75 to 85 RPM at a resistance setting of 13, corresponding to approximately 185 to 215 W. Each stationary bike exercise consisted of eight 2-minute intervals, followed by a 2-minute rest period while sitting.
Immediately following this rest period, the participant completed a dynamic SEC consisting of a series of 3 different medicine ball exercises of increasing difficulty. The goal of this portion of the SEC was to add dynamic head movements and rotational maneuvers to uncover potential symptoms that are not provoked by a stationary exercise alone. Participants began with medicine ball wall tosses without visual tracking, in which they maintained stationary head and body positioning with their vision fixed to a target on the wall. They began by holding the ball at one hip, followed by bringing the ball to the center of their body and tossing the ball at the wall target directly in front of them, then catching the ball and repeating the motion by bringing the ball to the opposite hip. To add difficulty by way of increasing visual motion, participants next completed medicine ball wall tosses with added visual ball tracking, in which participants completed a similar motion to the previous exercise, but with their vision now moving with the ball rather than fixed to the wall target. Finally, to increase the difficulty further by the addition of angular rotational movements while maintaining visual ball tracking, participants completed medicine ball chops. Holding the ball in a standing position and moving to a half-squat position, the participants performed a “chopping” motion in which they raised the ball over one shoulder, and then brought the ball across their body to the opposite hip. All medicine ball exercises were performed using a ball weighing 2 lb. Participants first completed 3 sets of medicine ball wall tosses without visual tracking: the first set of 12 repetitions, the second set of 16 repetitions, and the third set of 20 repetitions. Next, participants completed 3 sets of medicine ball wall tosses with visual ball tracking: the first set of 8 repetitions, the second set of 12 repetitions, and the third set of 16 repetitions. Finally, participants completed 3 sets of medicine ball chops: the first set of 3 repetitions over each shoulder, the second set of 6 repetitions over each shoulder, and the third set of 9 repetitions over each shoulder. Each set of medicine ball exercises took approximately 1 to 2 minutes to complete.
All participants were fitted with a chest-worn Polar (Bethpage, New York) heart rate monitor to quantify some of the physiological effects of exercise. Symptom provocation was monitored during the SEC to determine whether there was a need to prematurely stop the exercise due to high levels of symptom provocation. To accomplish this, prior to the SEC, each participant was systematically queried on the presence of headache, dizziness, nausea, fogginess, light-headedness, and neck pain, and they were asked to rate each symptom from 0 to 10, with 0 corresponding to “absent” and 10 corresponding to “severe.” Symptom scores were recorded at 2-minute intervals throughout the exercise bike workout and after each set of medicine ball exercises. During the SEC, if any symptom increased by 3 or more points on the 10-point scale compared with the pre-SEC baseline, the intensity of the exercise was reduced to the previously tolerated interval, and the patient was observed over the next 2-minute interval. If the symptom failed to improve below the ≥3-point threshold or worsened, then that portion of the SEC was stopped. Participants also could request to stop the SEC at any time. The stationary bike workout was stopped early in 9 participants due to symptom provocation above the defined threshold, all after completing at least 8 minutes of the 16-minute workout. The medicine ball workout was stopped early in 7 participants due to symptom provocation above the defined threshold, all after fully completing at least the medicine ball wall tosses without visual tracking.
VOMS assessment outcomes are presented as the VOMS total symptom score increases and were calculated for both pre- and post-SEC VOMS assessments for each VOMS item. Pre- and post-SEC VOMS symptom provocation and NPC distances were compared using Wilcoxon ranked sum tests. Effect size was calculated using the formula r = z/√n.27 A small effect size corresponded to an r value between 0.1 and 0.29, a medium effect size corresponded to an r value between 0.3 and 0.49, and a large effect size corresponded to an r value greater than 0.5.28,29 The frequencies of positive assessments for each VOMS item were compared using McNemar's test. To account for multiple comparisons, a false discovery rate was used to determine statistical significance.30 When a participant had a negative VOMS assessment before the SEC but became positive after the SEC, they were defined as having a change in classification, and the initial pre-SEC VOMS assessment was considered a false negative. All statistical analyses were performed using SPSS Statistics, version 26 (IBM, Armonk, New York).
VOMS Symptom Provocation Scores
Following the SEC, significant differences exist in symptom provocation scores compared with the preexercise symptom provocation scores for all VOMS assessment items (Table 2). There were large effect sizes in symptom provocation difference for all VOMS items. Additionally, the mean postexercise NPC distance (6.68 ± 6.46 cm) was significantly greater compared with mean preexercise NPC distance (5.28 ± 5.38 cm), P = 0.002.
Table 2 -
Changes in VOMS Symptom Provocation Scores Pre- Versus Post-SEC
|VOMS Assessment Item
||Median Symptom Provocation Score Change (Range)
||FDR Critical Value
||Wilcoxon Rank Sum Score
|Visual motion sensitivity
z = 4.05, P < 0.001, r = 0.68
z = −3.82, P < 0.001, r = 0.64
z = −3.80, P < 0.001, r = 0.63
z = −3.71, P < 0.001, r = 0.62
z = −3.71, P < 0.001, r=0.62
z = 3.51, P < 0.001, r = 0.59
z = −3.37, P = 0.001, r = 0.56
Abbreviations: FDR, false discovery rate; SEC, supervised exercise challenge; VOMS, Vestibular/Ocular Motor Screening; VOR, vestibulo-ocular reflex.
Identification of Positive VOMS Assessments
In total, the post-SEC VOMS identified 29 participants (80.6%) as positive in at least 1 VOMS item compared with 21 participants (58.3%) identified as positive pre-SEC (P = 0.008). The proportion of patients with a positive finding after SEC was significantly different from the proportion of patients with a positive finding before SEC for 5 of the 8 VOMS items: smooth pursuits, vertical saccades, NPC symptoms, visual motion sensitivity, and horizontal VOR (Table 3). For vertical VOR, NPC distance, and horizontal saccades, there also were greater proportions of patients with positive findings after SEC compared with the proportion of patients with positive findings before SEC, but the differences in proportions for these items did not reach statistical significance.
Table 3 -
Changes of Classification and Frequencies of Positive VOMS Assessments Pre- Versus Post-SEC
||Change of Classification
||FDR Critical Value
|Visual motion sensitivity
Abbreviations: FDR, false discovery rate; NPC, near point of convergence; SEC, supervised exercise challenge; VOMS, Vestibular/Ocular Motor Screening; VOR, vestibulo-ocular reflex.
aP value below the FDR critical value was used as a cutoff for significance.
Changes From Negative to Positive VOMS Classification With Completion of Post-SEC VOMS
Compared with the pre-SEC VOMS, the post-SEC VOMS was associated with the identification of additional participants who were previously negative but became positive for all VOMS assessment items (Table 3). The largest change of classification from pre-SEC negative to post-SEC positive was seen for smooth pursuits (n = 13, 26.1%) and the smallest change of classification was seen for NPC distance (n = 5, 13.9%).
In this study, undergoing an SEC resulted in a greater number of participants being identified as VOMS positive after exercise compared with before exercise. Post-SEC VOMS symptom provocation scores were significantly greater in all symptom-based VOMS items compared with pre-SEC scores. Post-SEC, there were significantly greater numbers of positive assessments for 5 of the 8 VOMS items compared with pre-SEC. Additionally, there were changes of classification from negative to positive seen in all VOMS items following the SEC. Taken together, the results of this study suggest that including an SEC as part of the clinical evaluation following concussion allows for a greater identification of vestibular and ocular motor-related symptoms using the VOMS, as hypothesized. To our knowledge, this is the first study to measure the effects of an SEC on concussed athletes using a postexertion VOMS assessment.
The largest increase in the number of positive assessments, as well as in the change of classification from negative to positive, was seen in the smooth pursuit assessment. There were also significantly greater numbers of positive assessments after the SEC compared with before the SEC for vertical saccades, NPC symptoms, horizontal VOR, and visual motion sensitivity. It is notable that the identified post-SEC differences in VOMS assessments were most apparent in the symptom-based items of the VOMS rather than NPC distance. While the NPC distance was greater following the SEC, the proportion of participants who were positive by NPC distance was not significantly different after exertion. As an abnormal NPC distance by itself may not be diagnostic of convergence insufficiency,31 it follows that an SEC appears to reveal ocular motor impairments based on symptom provocation rather than physical changes (ie, NPC performance).
The identification of vestibular and ocular motor-related symptoms is important given their association with a worse recovery from concussion, but these symptoms may be missed during symptom reporting (such as from the SCAT5) or when VOMS items are completed only at rest.13 The results of this study provide further support that there may be a large number of false negatives when a VOMS is completed at rest before an SEC compared with after an SEC. For the entire VOMS assessment, there were 27.4% false negatives when the pre-SEC VOMS was compared with a post-SEC VOMS. There were no false positives when comparing the pre-SEC VOMS with the post-SEC VOMS. Thus, an SEC may help to better identify and target vestibular and ocular motor symptoms after concussion. Importantly, the early identification and targeted treatment of these symptoms, such as with physical therapy, are associated with accelerated recovery from concussion.9 Additionally, as the lack of symptom provocation during physical exertion is used as a metric to determine progression through a return-to-play protocol and for clearance to return to sport, this study offers further support for the use of in-clinic SECs to determine recovery from concussion.25,32
This study's results also suggest that, for some patients, symptom provocation by VOMS items may be direction specific (ie, horizontal vs vertical). Similar to the SEC protocol used in this study, a previous study has shown that SECs utilizing forms of multidirectional and rotational dynamic exercise, such as medicine ball exercises and agility drills, may enhance detection of symptoms that are potentially related to vestibular and ocular motor impairments, such as dizziness.13 Because some forms of aerobic exercise, such as stationary bike, limit body movement, they may fail to detect symptoms that are only provoked by movement. This study's SEC protocol included 3 forms of medicine ball exercises, which were chosen to provide increasingly difficult challenges to the vestibular and ocular motor systems through head and body movement as well as visual tracking. All participants completed all 3 sets of the initial medicine ball wall tosses without vision tracking. The second medicine ball exercise added visual tracking of the ball to increase vestibular and ocular motor demand through eye tracking; while all participants completed the first set of this exercise, there were 5 participants who were unable to complete the second and third intervals of the medicine ball tosses with visual tracking. The third medicine ball exercise (ie, medicine ball chops) added angular rotation movement of the head and body in addition to visual tracking and was intended to be the most difficult challenge to the vestibular and ocular system. All participants completed the first set of medicine ball chops, but there were an additional 2 participants who completed all medicine ball wall tosses (with and without visual tracking) but were unable to complete the second and third sets of medicine ball chops. Thus, to maximize identification of these symptoms during an in-clinic assessment such as an SEC, it is recommended to include dynamic exercises that challenge various planes of direction and rotation. Furthermore, it will be important for future studies investigating symptom provocation during SECs after concussion to consider including forms of both aerobic and dynamic exercises that are multidirectional and performed with rotational movement patterns.
It is possible that postexertional increases in VOMS symptom provocation may not be solely attributable to concussion, especially given the lack of a control group in the current investigation. Studies investigating the effect of exertion on performance of commonly used concussion measures did not yield results that are consistent across all concussion outcome measures. For instance, while worsened performance was observed for balance testing19,20,33 and cognitive testing21,34,35 performed after exertion, others have shown improved performance in other physical tasks such as finger-to-nose testing.36 Furthermore, the VOMS has previously shown a high test-retest reliability and low false-positive rate when tested shortly after physical exertion,22 and no effects of physical exertion were found with a test of dynamic visual acuity in healthy college athletes.37 It may be that, because the VOMS primarily detects symptom provocation, there is less influence of fatigue on its findings compared with performance measures such as balance testing, in which fatigue may be more expected to influence performance. In support of this, previous studies have demonstrated postexercise increases in fatigue-related symptoms (eg, “feeling slowed down” and “fatigue or low energy”) on the Sport Concussion Assessment Tool 3 symptom checklist, but no other symptoms such as headache or dizziness, which are queried as part of the VOMS.33,38 While a small increase in symptom provocation on the VOMS may be possible after exertion in healthy controls (ie, 3-point increase39), our study suggests that concussed athletes may exhibit a larger symptom increase (ie, 12 points) reflecting symptom provocation that is related to concussion. Future studies on postexertion VOMS assessments should include a control group to better determine the potential effects of physical exertion on symptom provocation that is attributable to concussion.
There are several additional notable limitations to this study. All participants in this study were adolescent athletes, with greater representation of male adolescents compared with females. Therefore, it is possible that the results of this study are not generalizable to a population with a wider age range or equal sex balance, and the results may not be applicable in a nonathlete population. The SEC used in this study included both aerobic and dynamic challenges, and so the individual influences of only aerobic or dynamic exercise on VOMS assessments remain a question. While the purpose of this study was not to identify the effects of only aerobic or dynamic exertion on VOMS assessments, future studies could identify whether either exercise type alone has a greater effect on the VOMS scores.
Vestibular and ocular motor-related symptoms after concussion are common and contribute to worse outcomes. An aerobic and dynamic SEC performed prior to a VOMS assessment may increase the detection of postconcussion vestibular and ocular motor-related symptoms that may be missed if the VOMS was performed only at rest. The inclusion of an SEC in conjunction with the VOMS during the evaluation of adolescents with sport-related concussion is recommended to maximize the identification of vestibular and ocular motor-related symptoms for which targeted rehabilitation may improve recovery from concussion.
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