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8 Ref 10
8 Ref 10
KEYWORDS
FIGURE 1
Consort diagram for patients included in final analysis.
At each visit, concussion symptoms were assessed using the Descriptive statistics were used to describe patient
Post-Concussion Symptom Inventory (PCSI), which asks patients demographics, characterize concussion history and injury
to self-report symptoms and symptom severity on a scale from 0 details, and self-reported progress with the VV-HEP. Our
(not a problem) to 6 (severe problem). Patients completed an primary analysis compared symptom endorsement and
age-specific PCSI based on age (8–12 or 13–18 years), both of symptom severity between patients who self-reported having
which demonstrate good test-retest reliability (8–12 years not started, those who were in progress, and those who had
intraclass correlation coefficient = 0.89, 13–18 years intraclass completed the VV-HEP. Kruskal-Wallis tests were used to
correlation coefficient = 0.79) (24). Primary outcomes from the determine if self-reported progress with the VV-HEP (“had not
PCSI included total symptom endorsement and total symptom done,” “in progress,” or “completed”) was associated with PCSI
severity. Visio-vestibular function was assessed using a visio- symptom endorsement or PCSI symptom severity. Post-hoc
vestibular examination (VVE), which is a battery of 9 subtests pairwise comparisons with Bonferroni adjustment (alpha =
including smooth pursuit, horizontal/vertical saccades, 0.017) were used to further delineate differences in symptom
horizontal/vertical VOR, near point of convergence (NPC), left reporting based on VV-HEP status. Effects sizes for symptom
and right monocular accommodation, and complex tandem gait reporting were calculated using eta squared (ƞ2). Our secondary
(Supplementary Material; Video VVE demonstration: https:// analysis used chi-square tests to compare VVE abnormalities by
www.chop.edu/video/pediatric-exams-concussion-evaluation). To self-reported progress with the VV-HEP. To adjust for 10
determine performance, the VVE considers presence of self- comparisons in our secondary analysis, Bonferroni adjusted
reported symptom provocation (including headache, dizziness, eye alpha was set to 0.005 a priori. Effect sizes for self-reported
fatigue, eye pain, or nausea) (yes/no), physical signs (yes/no), and progress with VV-HEP were calculated using Cramer’s’ V. Data
established repetition-based cut-offs allowing for increased were analyzed using SAS statistical software, version 9.4 (SAS
concussion diagnosis sensitivity and a more comprehensive Institute Inc., Cary, NC).
assessment of visio-vestibular function (25, 26). The VVE has
been feasibly administered across different health care settings (27,
28), and shows fair to moderate agreement between providers and
moderate to substantial agreement with the same provider (25).
Results
The primary outcomes from the VVE included subtest outcomes
A total of 527 patients were included in the final analysis
(normal vs. abnormal) and total VVE score (abnormal: ≥ 2
[female = 294 (55.8%), age = 14.4 ± 2.1 years] (Table 1). The
abnormal subtests) (28). The VV-HEP consisted of exercises
majority of patients reported with no prior concussion history
targeting visual and vestibular function including saccades, VOR,
(54.1%), with a sport-related mechanism for the current
convergence, and balance (Supplementary Material). Patients
concussion (69.1%), and a median lifetime concussions of 1
were instructed during their initial visit to complete exercises 1–2
(IQR = 1–2). Patients were seen for an initial visit an average of
times daily and were informed we would be following up with
11.1 ± 6.9 days after concussion and first follow-up an average of
their progress at subsequent visits but were not otherwise given
30 ± 13.2 days after concussion. Patients had a median of 2 (IQR
any reminders or incentive to comply with the VV-HEP.
= 1–4) abnormal VVE subtests at initial visit and a median of 2
Prior to the start of the clinical exam, patients completed a
(IQR = 0–5) abnormal VVE subtests at first follow-up. At first
demographic questionnaire, including age and patient-reported
follow-up, patients were seen an average of 19.0 ± 9.2 days after
medical history, and physicians used a standardized template
their initial visit and most patients self-reported being in
within the EHR to document injury and self-reported concussion
progress with the VV-HEP (n = 412, 78.3%), followed by patients
history details. During the exam, patients completed the VVE
and PCSI as a part of a comprehensive concussion assessment.
Following the exam, physicians indicated if the patient was
prescribed a VV-HEP. At each clinical follow-up, patients TABLE 1 Demographic information for patients at initial visit.
repeated the VVE and PCSI and self-reported their progress on
n = 527
the VV-HEP to the provider, who recorded the response in the Sex, n (%)
EHR from a drop-down list of options. Progress was categorized Male 233 (44.2%)
as “has not started,” “in progress,” or “has completed.” Responses Female 294 (55.8%)
recorded as having tried the HEP but stopped and patients who Age, years, mean (SD) 14.4 (2.1)
never tried the HEP were categorized as “has not started.” Race/Ethnicity, n (%)
Responses recorded as “is doing the HEP” were categorized as Non-hispanic white 383 (72.8%)
Non-hispanic black 49 (9.3%)
“in progress.” Responses recorded as “has completed the HEP”
Hispanic 29 (5.5%)
were categorized as “completed.” Patients were excluded if they
Non-hispanic Asian/Asian Pacific 65 (12.4%)
reported an invalid or missing date of injury [e.g., clinician or Islander/other/multiple race/unknown
patient failed to document date, missing month, day, or year, Concussion history, n (%) 242 (45.9%)
documentation error (date of injury is date of birth or a date in Lifetime concussions, median (IQR) 1 (1–2)
the future)], if they were not prescribed the VV-HEP, or if they Current concussion was sport-related, n (%) 364 (69.1%)
Days since injury, mean (SD) 11.1 (6.9)
had incomplete VVE or PCSI.
who had not started (n = 81, 15.3%), and patients who had Discussion
“completed” the program (n = 27, 5.1%).
When assessing concussion symptom endorsement and The purpose of our study was to utilize a large clinical
severity at initial visit, patients reported a median of 13 concussion registry to examine the effects of a VV-HEP on
symptoms (IQR = 8–17) and a symptom severity of 35 (IQR = symptom reporting and visio-vestibular function during follow-up
19–53) (Table 2). The most common symptoms endorsed at in concussed pediatric patients. Though a small proportion of
initial visit included headache (n = 406, 77.0%), difficulty patients had completed the VV-HEP within 60 days of injury, our
concentrating (n = 360, 68.3%), and light sensitivity (n = 360, findings indicate that those who did reported with lower symptom
68.3%). At first follow-up, patients who had completed the endorsement and severity as well as improved visio-vestibular
VV-HEP reported significantly lower symptom endorsement function relative to patients who did not complete the VVE-HEP.
(median = 1, IQR = 0–3) relative to patients in progress Active and early rehabilitation strategies, including vestibular
(median = 8, IQR = 3–14; p < 0.001) and to patients who had therapy, have been recommended in recent literature to improve
not started (median = 7, IQR = 1–13; p < 0.001). Similarly, concussion outcomes (3, 6, 7, 29). Previous literature assessing
patients who had completed the VV-HEP reported significantly aerobic exercise in adolescent patients have demonstrated faster
lower symptom severity (median = 1, IQR = 0–4) relative to recoveries following concussion (30) and reduced symptoms (31)
patients in progress (median = 15, IQR = 4–30; p < 0.001) and to and improved mood-related symptoms (32) in patients with
patients who had not started (median = 15.5, IQR = 2–32.5; p < persisting symptoms. Similarly, studies of visual and vestibular
0.001) (Table 3). rehabilitation have found reductions in overall concussion
At initial visit, 65.2% of patients reported with two or more symptoms (18) and reduced recovery times (20). However, some
abnormal VVE subtests and 53.4% of patients reported with two patients experience barriers to access these therapies throughout
or more abnormal VVE subtests at follow-up (Table 2). When their full course of care. Mohammed and colleagues (14) found
assessing VVE abnormalities by self-reported progress with the that disparities are evident when examining adherence to
VV-HEP at follow-up, we found that a significantly lower concussion care recommendations, some of which may be
proportion of patients who had completed the program reported addressed by using a cost-effective and equitable at-home
with abnormal VOR, tandem gait, and total VVE score relative program. Our findings indicate at-home exercise programs
to patients who had not started the program (p < 0.005) prescribed within 28 days of injury may be effective in reducing
(Table 4). Additionally, a significantly lower proportion of overall concussion symptoms. Median symptom endorsement
patients who had completed the VV-HEP reported with was reduced from 13 symptoms at initial visit to 1 symptom and
abnormal tandem gait and total VVE score relative to patients median symptom severity was reduced from 33 at initial visit to
who were in progress (p < 0.005) (Table 4). 1 at follow-up in patients who completed the VV-HEP. Similarly,
Storey et al. (18). found a reduction from a median of 9
symptoms to 0 symptoms after 2 in-office physical therapy visits
and that patients who completed in-office vestibular physical
TABLE 2 Clinical exam outcomes of all patients at initial visit and first therapy (median = 7 visits) had significantly lower overall
follow-up.
symptom burden relative to those who did not complete. The
Initial visit within First follow-up current study indicates that a VV-HEP may be comparably
28 days within 60 days effective to in-office therapy in reducing overall concussion
PCSI, median (IQR) symptoms. Additionally, our study found that patients who
Symptom endorsement 13 (8–17) 7 (2–13) reported being in progress with the VV-HEP demonstrated lower
Symptom severity 35 (19–53) 14 (2–30)
median symptom endorsement and severity relative to initial
Visio-vestibular exam presentation which suggests that the prescription of a VV-HEP
Pursuits, n (%) 215 (40.8%) 93 (17.7%)
does not exacerbate symptoms.
Saccades, n (%)
When assessing the effect of the VV-HEP on visio-vestibular
Horizontal 129 (24.5%) 230 (43.6%)
Vertical 125 (23.7%) 247 (46.9%)
function, we found that a lower proportion of patients who had
Vestibular-ocular reflex, n (%) completed the program reported with abnormal aspects of the
Horizontal 135 (25.6%) 249 (47.3%) VVE (horizontal and vertical VOR, tandem gait, total VVE
Vertical 142 (26.9%) 251 (47.6%) score) relative to patients who were in progress and patients who
Near point of 92 (17.5%) 67 (12.7%) had not started. Previous studies assessing both in-office and at-
convergence, n (%)
home vestibular rehabilitation programs in pediatric patients
Accommodation, n (%)
have demonstrated improvements in visio-vestibular function (18,
Left eye 96 (18.2%) 57 (10.8%)
Right eye 83 (15.8%) 49 (9.3%)
19, 22). Alsalaheen et al. (19) found that in-office vestibular
Tandem gait, n (%) 238 (45.2%) 113 (21.4%) therapy supplemented with home exercises significantly improved
Total VVE score, n (%) 320 (65.2%) 266 (53.4%) all elements of the Vestibular/Oculomotor Screening (VOMS)
Post-concussion symptom inventory (PCSI) scores reported as median (IQR) and assessment. Our results more closely align with a previous study
VVE subtests reported as the percentage of patients with an abnormal test. assessing an at-home program only, which found that a 4-week
TABLE 3 Symptom endorsement and severity of patients at follow-up by self-reported progress with the home visio-vestibular program and post-hoc
pairwise comparisons.
TABLE 4 Percentage of patients with abnormal VVE at follow-up by self-reported progress with the home visio-vestibular program and post-hoc
pairwise comparisons (α = 0.005).
at-home vestibular rehabilitation program significantly improved results may not be generalizable to patients presenting to other
horizontal and vertical VOR in concussed patients aged 12–18 health care providers or clinical settings. We were unable to
(22), suggesting that visio-vestibular function can be improved account for additional potential confounding factors between
with home exercises. The additional improvements of tandem initial visit and follow-up visit such as physical activity, school
gait and total VVE score found in our study can be attributed to participation, etc. We excluded patients with missing or invalid
the use of different visio-vestibular assessments. The VVE shares date of injury, which is likely not missing at random and reduces
domains with the VOMS (smooth pursuits, horizontal and the generalizability of the results. Additionally, we relied on
vertical saccades, horizontal and vertical VOR, convergence) with patients to self-report their compliance with the VV-HEP which
additional exam elements of monocular accommodation and is subject to recall bias.
complex tandem gait for a more comprehensive assessment of In summary, we found that patients who reported completing a
the visual and vestibular systems (25, 26). Using a similar VV-HEP at first follow-up within 60 days of injury had
assessment, Storey et al. (18) found that a larger proportion of significantly lower symptom endorsement and severity relative to
patients who did not complete in-office vestibular therapy had patients who had not started the program or were in progress.
abnormal tandem gait performance relative to those who Additionally, a lower proportion of patients who had completed
completed therapy. Our findings build on this, suggesting that an the VV-HEP demonstrated abnormal VOR (horizontal and
at-home program targeting visio-vestibular systems may also be vertical), tandem gait, and total VVE score. Our findings indicate
beneficial in improving tandem gait performance. that an at-home program targeting vision and vestibular function
Our study is not without limitations. Our patients were seen by is not only safe but may also be effective in improving clinical
physicians in a specialty care concussion clinic and therefore, our outcomes following concussion in pediatric patients. Future
research should continue investigating the utilization, compliance, and approved the final version. All authors contributed to the
and effectiveness of at-home therapy programs following article and approved the submitted version.
concussion in pediatric patients in order to improve the
accessibility of early and active concussion treatment interventions.
Funding
Data availability statement Research reported in this publication was supported by
National Institute of Neurologic Disorders and Stroke of the
The datasets presented in this article are not readily available National Institutes of Health (grant numbers R01NS097549 and
because data were queried from electronic health records of T32NS043126) and the Pennsylvania Department of Health. The
active patients. Requests to access the datasets should be directed funding sources did not have any involvement in study design,
to [email protected]. collection, analysis, or interpretation of data, writing of the
report, or the decision to submit the article for publication.
Ethics statement
The studies involving human participants were reviewed and
Conflict of interest
approved by Children’s Hospital of Philadelphia Institutional
The authors declare that the research was conducted in the
Review Board (IRB# 19-016019). Written informed consent from
absence of any commercial or financial relationships that could
the participants’ legal guardian/next of kin was not required to
be construed as a potential conflict of interest.
participate in this study in accordance with the national
legislation and the institutional requirements.
Publisher’s note
Author contributions
All claims expressed in this article are solely those of the
PR helped conceive of the presented study idea, contributed to authors and do not necessarily represent those of their affiliated
the design, derived and processed the data, analyzed the data, organizations, or those of the publisher, the editors and the
drafted the manuscript, and approved the final version. OP reviewers. Any product that may be evaluated in this article, or
helped conceive of the presented study idea, contributed to the claim that may be made by its manufacturer, is not guaranteed
study design, contributed to the interpretation of results, or endorsed by the publisher.
provided critical feedback to the draft, and approved the final
version. MG helped conceive of the presented study idea,
contributed to the study design, contributed to the interpretation Supplementary material
of results, provided critical feedback to the draft, and approved
the final version. KA and CM helped conceive of the presented The Supplementary Material for this article can be found
study idea, contributed to the study design, contributed to the online at: https://www.frontiersin.org/articles/10.3389/fspor.2023.
interpretation of results, provided critical feedback to the draft, 1064771/full#supplementary-material.
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