Contributions of PCSS, CISS, and VOMS for Identifying Vestibular/Ocular Motor Deficits in Pediatric Concussions

Abstract

Background:

Vestibular/ocular motor dysfunction can occur in pediatric concussions, which can impair reading, learning, and participation in athletics. This study evaluated 3 clinical tools for identifying postconcussion vestibular/ocular motor dysfunction: (1) Post-Concussion Symptom Scale (PCSS), (2) Convergence Insufficiency Symptom Survey (CISS), and (3) Vestibular/Ocular Motor Screening (VOMS).

Hypothesis:

Evaluating vestibular/ocular motor dysfunction with multiple clinical tools will capture more symptomatic patients than any 1 tool alone.

Study Design:

Cross-sectional data from a prospective cohort study.

Level of Evidence:

Level 4.

Methods:

Patients were between 8 and 17 years old and seen in a tertiary care pediatric sports medicine clinic between August 2014 and February 2018. Data were collected from initial visit and included VOMS, PCSS, and CISS. Descriptive statistics, Pearson’s correlations, and logistic regressions were used to describe relationships between clinical tools.

Results:

Of the 156 patients (55.1% female; 14.35 ± 2.26 years old) included, this study identified 129 (82.7%) with vestibular/ocular motor dysfunction. Of these 129, 65 (50.4%) reported “visual problems” on PCSS, 93 (72.1%) had abnormal CISS, and 99 (76.7%) had abnormal VOMS. Together, VOMS and CISS identified 64 (49.6%) patients without reported “visual problems” on PCSS. Higher total PCSS scores predicted abnormal CISS (odds ratio [OR], = 1.11; 95% CI, 1.07-1.17) and abnormal VOMS (OR, 1.03; 95% CI, 1.01-1.06). “Visual problems” on PCSS did not predict abnormal CISS or VOMS.

Conclusion:

Vestibular/ocular motor dysfunction were identified in nearly 83% of study subjects when PCSS, CISS, and VOMS are used together.

Clinical Relevance:

These results suggest adding CISS and VOMS to the clinical evaluation of concussions can help clinicians identify post-concussion vestibular/ocular motor dysfunction.

A concussion is a mild traumatic brain injury with high prevalence in pediatric populations. In survey data of 13,088 US adolescents, close to 20% reported at least 1 concussion in their lifetimes. ²² Concussion diagnosis and management can be clinically challenging because of the broad range of nonspecific clinical signs and symptoms patients present.^9,14 Vestibular/ocular motor symptoms due to concussion can have significant effects on a child’s ability to read, learn, and perform athletic activities. Thus, it is important to identify patients who are symptomatic and coordinate appropriate care to best facilitate return to classroom and return to play.

Vestibular/ocular motor dysfunction is a common finding with concussions and may predict prolonged recovery in adolescents.^12,13 Several clinical tools exist to evaluate vestibular/ocular motor function.^6,10 These tools include patient self-report and Vestibular/Ocular Motor Screening (VOMS) assessment. However, data are limited on the relative contributions of each of these tools in identifying these symptoms in pediatric patients with concussions.

VOMS is performed as part of the physical examination and evaluates saccades, smooth pursuits, convergence, vestibulo- ocular reflex (VOR), and visual motion sensitivity. VOMS has some predictive value in identifying pediatric patients with concussions. ¹⁵

The Post-Concussion Symptom Scale (PCSS) is the most commonly used clinical tool to evaluate concussion symptoms and has been validated in children and adults.^3,7,8 Patients are asked to self-report 22 postconcussion symptoms by grading their severity on a 7-point Likert-type scale with scores from 0 to 6 on each symptom (Figure 1). ⁵ For vestibular/ocular motor symptoms, the PCSS includes the category, “Visual problems.” ⁶

Figure 1.

Post-Concussion Symptom Scale.

The Convergence Insufficiency Symptom Survey (CISS) is a 15-item survey for patients to self-report symptoms evoked while reading, with symptom severity measures from 0 to 4 for each item (Figure 2).^1,16,19 CISS was developed to track the rehabilitation of convergence insufficiency, an indication for which it is validated. Research on the utility of CISS in evaluating concussions is limited.^6,13,20

Figure 2.

Convergence Insufficiency Symptom Survey. Adapted from Convergence Insufficiency Treatment Trial (CITT) Study Group. ¹⁹

A previous study has highlighted the prevalence of “vision diagnoses” after concussion in pediatric patients using various evaluation methods. ¹³ The primary objective of this study is to further characterize the prevalence of vestibular/ocular motor dysfunction and evaluate the relative contributions of PCSS, CISS, and VOMS for identifying vestibular/ocular motor dysfunction in pediatric patients with concussions.

Methods

This study was approved by the institutional review board at Ann and Robert H. Lurie Children’s Hospital of Chicago. English-speaking patients aged 8 to 17 years who presented to a tertiary care hospital-based pediatric sports medicine clinic and diagnosed with concussion between August 2014 and February 2018 were invited to participate. For patients who had any neuroimaging studies, those who had structural abnormalities on neuroimaging were excluded.

Data were collected from the initial visit to the clinic after head injury. A diagnosis of concussion was made by the attending sports medicine physician based on diagnostic criteria from Consensus Statement on Concussion in Sport.^9,14 Data extracted from patients’ electronic medical records included age, sex, mechanism, or injury (sport- vs nonsport-related injury), number of previous concussions, number of days between injury and initial clinic visit, history of anxiety or depression, VOMS, CISS score, and PCSS total score and score for each PCSS symptom. CISS was routinely administered as part of the study starting January 2016. Data were entered in a Microsoft Excel spreadsheet and analyzed using RStudio.

All symptomatic patients were identified and coded based on binary variables denoting the presence or absence of vestibular/ocular motor dysfunction as follows. For VOMS, subjects were reported to have an abnormal VOMS if there was a deficit or symptom provocation with any of the following VOMS components: smooth pursuits, horizontal or vertical saccades, VOR, or near point of convergence >6 cm (Figure 3). ¹⁵ For PCSS, total PCSS score was measured, and the response for “Visual Problems” was analyzed and coded abnormal for any report greater than 0, indicating some level of self-reported vestibular/ocular motor dysfunction. For CISS, any score of ≥ 16 was coded as abnormal.^2,16

Figure 3.

VOMS assessment template.

Descriptive statistics were calculated for the outcome measures. Pearson’s correlation coefficients were used for correlations. A logistic regression was performed to evaluate significant contributors to abnormal CISS score (≥16) and abnormal VOMS. All significant levels were set at P < 0.05. ¹³

Results

Of the 614 patients screened and/or approached from August 2014 to February 2018, 87 (14.2%) declined to participate and 27 (4.4%) were found to be ineligible. Of the 500 enrolled, 182 (36.4%) patients were enrolled for this study from the time CISS was administered starting January 2016. Of the 182 patients enrolled, there were incomplete data for PCSS or CISS from 26 (14.29%) patients, leaving 156 patients (55.1% female) included in this study. Median age of patients included was 14.35 years (SD, 2.26). Median time between injury and initial clinic visit was 20 days (interquartile range [IQR], 10.7-32.0) (Table 1). The median score for CISS in this patient sample was 20 (IQR, 10-33.5), which is above the abnormal threshold of 16.

Table 1.

Patient characteristics

Characteristic	n	%	Range
Total patients, n	156
Female sex, n (%)	86	(55.1)
Age, y, mean (SD), range	14.35	(2.3)	8.3-17.9
Injury to visit, d, median (IQR), range	20	(10.7-32.0)	1-362
Sport injury, n (%)	112	(71.8)
Previous concussion, n (%)	77	(49.4)
History of anxiety, n (%)	35	(22.4)
History of depression, n (%)	17	(10.9)
PCSS score, median (IQR), range	24.5	(9-52.3)	0-99
CISS score, median (IQR), range	20	(10-33.5)	0-56

CISS, Convergence Insufficiency Symptom Survey; IQR, interquartile range; PCSS, Post-Concussion Symptom Scale.

Overall, we identified 129 (82.7%) patients with visual symptoms/dysfunction on at least 1 of the 3 modalities: VOMS, PCSS, and CISS. Of these 129 patients, 65 (50.4%) reported “visual problems” on PCSS, 93 (72.1%) had an abnormal CISS score, and 99 (76.7%) had an abnormal VOMS (Figure 4). There were significant positive correlations between each pair of clinical assessment tools. Abnormal CISS had a strong correlation with “vision problems” on PCSS (r = 0.64, P < 0.01) and a weak correlation with abnormal VOMS (r = 0.19, P = 0.02). Abnormal VOMS had a moderate correlation with “vision problems” on PCSS (r = 0.30, P < 0.01).

Figure 4.

Proportional Venn diagram of all patients identified to have vestibular/ocular motor dysfunction (n = 129) showing count and percentages (n, %) identified by each modality—Vestibular/Ocular Motor Screening (VOMS), Post-Concussion Symptom Scale (PCSS), or Convergence Insufficiency Symptom Survey (CISS). Note: The diagram is approximately proportional to the number represented. The size of the overlap does not always represent the value it carries. Created with the following acknowledgment: Hulsen T, de Vlieg J, Alkema W. BioVenn—a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics. 2008;9(1):488.

PCSS identified 3 (2.3%) patients reporting “visual problems” who did not have abnormal CISS or VOMS. CISS identified 14 (10.9%) patients with vestibular/ocular motor dysfunction who did not report “visual problems” on PCSS or have an abnormal VOMS. VOMS identified 27 (20.9%) patients with vestibular/ocular motor dysfunction who did not report “visual problems” on PCSS or have an abnormal CISS. VOMS and CISS together identified 64 (49.6%) patients who did not report “visual problems” on PCSS (Figure 4).

In a multivariate logistic regression, predictors of abnormal CISS score were older age (odds ratio [OR], 1.49; 95% CI, 1.15-2.01;P < 0.01) and total PCSS score (OR, 1.11; 95% CI, 1.07-1.17; P < 0.01) (Table 2). The only predictor of abnormal VOMS was total PCSS score (OR, 1.03; 95% CI, 1.01-1.06; P < 0.01) (Table 3).

Table 2.

Logistic regression for independent predictors of abnormal CISS score

Predictors	Abnormal CISS (≥16)
	Odds Ratios	95% CI	P a
(Intercept)	0.00	0.00-0.03	0.001
Female sex	0.80	0.26-2.46	0.70
Age on initial visit	1.49	1.15-2.01	0.004
Days: injury to visit	1.00	0.99-1.01	0.63
Sport injury	0.61	0.17-2.14	0.45
Previous head injury	1.20	0.41-3.51	0.74
History of anxiety	0.39	0.08-1.76	0.24
History of depression	0.24	0.03-1.47	0.14
Abnormal VOMS	0.96	0.34-2.66	0.94
PCSS: visual problems	3.01	0.94-10.31	0.07
Total PCSS score	1.11	1.07-1.17	<0.001
Observations	156

CISS, Convergence Insufficiency Symptom Survey; PCSS, Post-Concussion Symptom Scale; VOMS, Vestibular/Ocular Motor Screening.

^aBoldfaced P values indicate statistical significance (P < 0.05).

Table 3.

Logistic regression for independent predictors of abnormal VOMS

Predictors	Abnormal VOMS
	Odds Ratios	95% CI	P  a
(Intercept)	22.49	1.68-371.89	0.02
Female sex	0.48	0.20-1.11	0.09
Age on initial visit	0.85	0.70-1.02	0.08
Days: injury to visit	1.00	0.99-1.01	0.58
Sport injury	0.51	0.20-1.21	0.14
Previous head injury	0.66	0.30-1.45	0.31
History of anxiety	0.80	0.29-2.17	0.65
History of depression	0.99	0.29-3.49	0.98
Abnormal CISS	1.04	0.39-2.74	0.93
PCSS: visual problems	1.02	0.40-2.53	0.98
Total PCSS score	1.03	1.01-1.06	0.005
Observations	156

CISS, Convergence Insufficiency Symptom Survey; PCSS, Post-Concussion Symptom Scale; VOMS, Vestibular/Ocular Motor Screening.

^aBoldfaced P values indicate statistical significance (P < 0.05).

Discussion

This study identifies clinical predictors of abnormal CISS scores and abnormal VOMS. The main finding of this study is that of the 156 patients included, nearly 83% of patients were identified as having vestibular/ocular motor dysfunction when all three tools (PCSS, CISS, and VOMS) were used in the evaluation. When used alone, PCSS only identified 41.7% of these patients. The addition of CISS and VOMS increased identification of vestibular/ocular motor deficits. Children and adolescents may be able to identify vestibular/ocular motor dysfunction more readily when asked a series of specific questions about symptoms with reading on CISS, compared with when asked to simply report whether they have “visual problems” or not on PCSS. Similarly, VOMS may identify patients whose vestibular/ocular motor dysfunction is subclinical, especially younger children who may not be reading as much and therefore may not notice vestibular/ocular motor dysfunction. The findings of this study suggest that CISS and VOMS may be valuable additions to the clinical evaluation of children and adolescents with concussions, as they may help identify patients with vestibular/ocular motor dysfunction, and thereby optimize targeted treatment.

In this study, of the total enrolled patients, 63.5% of patients had abnormal VOMS and 59.6% had abnormal CISS scores. These percentages are similar to those reported in a previous study of 100 pediatric patients with concussions (age range 13.5-14.8 years) where 69% had abnormal VOMS and 66% had CISS scores ≥16. ¹³ The same study, however, found that 29% reported “visual problems” on PCSS, which is slightly less than the 41.7% that reported “visual problems” on PCSS in this study. This sample had a broader age range (8-17 years), which may explain these differences. Compared with younger patients, adolescent patients participate in activities with higher visual demands at school, such as more rigorous reading and writing, and therefore may be more likely to notice and report “visual problems” on PCSS.

In addition to identification of symptoms, this study examined the relationships between PCSS, CISS, and VOMS. In the regression model, higher total PCSS scores were predictors of both abnormal CISS scores and abnormal VOMS. For every 10-point increase on PCSS, there is 2.8 times greater odds of abnormal CISS and 1.3 times greater odds of abnormal VOMS. It is notable that, despite being positively correlated, reporting “visual problems” on PCSS did not predict either an abnormal CISS or abnormal VOMS once potential confounding factors were accounted for in the regression analysis. This highlights the importance of screening for vestibular/ocular motor dysfunction using these adjunctive tools regardless of whether patients report “visual problems” on PCSS, especially for those with higher symptom burdens.

It is interesting that while VOMS and CISS were positively correlated, neither was a significant predictor of the other when controlling for patient characteristics such as age, sex, and importantly, total PCSS score. Thus, the observed positive correlation was likely because patients with higher symptom burdens are more likely to present with both an abnormal CISS and abnormal VOMS. The absence of a predictive relationship suggests that CISS and VOMS may each have an independent contribution to the clinical evaluation of concussion-related vestibular/ocular motor dysfunction.

Older age was another independent predictor of abnormal CISS. While this may be interpreted that adolescent patients are at higher risk for vestibular/ocular motor dysfunction after a concussion injury, it is more likely that adolescent patients have higher visual demands at school compared to younger patients, and therefore may be more likely to notice and report symptoms of convergence insufficiency on CISS.

A previous study ⁴ of 399 pediatric patients with acute sports-related concussions and postconcussive syndrome found that older age, female sex, and history of depression were predictors of vestibular/ocular motor dysfunction measured by physical examination. This study, by contrast, did not find these patient characteristics to be significant predictors of abnormal VOMS. We suspect this is because the regression in this study accounted for overall symptom burden by including total PCSS score, and the previous study did not. It is possible that older age, female sex, and history of depression were associated with higher symptom burdens in the previous study, and the symptom burdens were driving the prediction of vestibular/ocular motor dysfunction rather than the patient characteristics.

This study has several limitations. The research was conducted in a large tertiary care center, which likely selects for patients with more severe symptom burdens so may not generalize to the larger population of pediatric concussion patients. Although days from injury to initial visit was not found to significantly predict abnormalities on VOMS or CISS in this study, the median time from injury to clinic visit was 20 days, with an IQR of 11 to 32 days, and therefore results cannot be extrapolated to patients presenting within shorter timeframes. For patients aged 8 to 12 years, the Child Sport Concussion Assessment Tool is preferred as it asks questions to patients and their parents, which would have been more appropriate for the younger patients in this study. ¹⁴ However, during creation and execution of this research, the clinic used PCSS for all patients enrolled, which may limit the interpretation of the age effect noted in this report. Additionally, there are limited data for the validity of CISS in patients younger than 11 years. We do not have preinjury PCSS, CISS, or VOMS for this patient population, so we cannot be sure the abnormalities are caused by the concussion. However, rates of convergence insufficiency in the general pediatric population are between 2% and 8%, which is much lower than that found in this study.^11,17,18 Also, we acknowledge that this study may underrepresent the number of patients reporting vestibular/ocular motor symptoms on PCSS, since we did not include the PCSS symptoms of “dizziness” and “balance problems,” which may also be reflective of vestibular/ocular motor symptoms. We chose not to include “balance problems” because this symptom may be due to deficits in the postural vestibular system rather than the vestibular ocular system. ¹⁵ We chose not to include “dizziness” because it tends to be less specific and can be due to a variety of contributing factors in addition to vestibular/ocular dysfunction, including dehydration, autonomic dysfunction, and somatosensory deficits. ²¹

This study is cross-sectional, as we only evaluated data from patients’ initial clinic visit. Future longitudinal studies will allow us to know whether identifying patients with vestibular/ocular motor dysfunction at their initial visit and connecting them with targeted treatment leads to quicker recovery or facilitates return to learning.

Conclusion

Vestibular/ocular motor dysfunction was identified in nearly 83% of pediatric patients with concussions when PCSS, CISS, and VOMS are used together. This is significantly more than the 42% identified using only PCSS. Predictors of abnormal CISS score included older age and higher total PCSS score. The only predictor of abnormal VOMS was higher total PCSS score. These findings suggest that a multifaceted approach including CISS and VOMS as adjuncts to PCSS may be helpful in identification of vestibular/ocular motor dysfunction in the setting of pediatric concussion.