Dizziness, Psychosocial Function, and Postural Stability Following Sport-Related Concussion

Abstract

Objective:

To examine if self-reported dizziness is associated with concussion symptoms, depression and/or anxiety symptoms, or gait performance within two weeks of post-concussion.

Design:

Cross-sectional study.

Setting:

Research laboratory.

Participants:

Participants were diagnosed with a concussion within 14-days of initial testing (N=40). Participants were divided into 2 groups based on their Dizziness Handicap Inventory (DHI) score: 36–100= moderate/severe dizziness and 0–35= mild/no dizziness.

Interventions:

Participants were tested on a single occasion and completed the Dizziness Handicap Index (DHI), Hospital Anxiety and Depression Scale (HADS), Patient Health Questionaire-9 (PHQ-9), and Post-Concussion Symptom Inventory (PCSI). Three different postural control tests were use: modified Balance Error Scoring System (mBESS), single/dual-task tandem gait, and a single/dual-task instrumented steady-state gait analysis.

Main Outcome Measures:

Comparison of patient-reported outcomes and postural control outcomes between moderate/severe (DHI ≥36) and mild/no (DHI<36) dizziness groups.

Results:

Participants with moderate/severe dizziness (N=19; age=17.1±2.4 years; 63% female) reported significantly higher symptom burden (PSCI: 43.0±20.6 vs. 22.8±15.7, p=0.001), and had higher median HADS anxiety (6 vs. 2, p<0.001) and depression (6 vs. 1, p=0.001) symptom severity than participants with no/minimal dizziness (N=21; age=16.5±1.9; 38% female). During steady-state gait, moderate/severe dizziness group walked with significantly slower single-task cadence (mean difference=4.8 steps/minute, 95% confidence interval=0.8, 8.8; p= 0.02) and dual-task cadence (mean difference=7.4 steps/minute, 95% confidence interval=0.7, 14.0; p= 0.04) than no/mild dizziness group.

Conclusion:

Participants who reported moderate/severe dizziness reported higher concussion symptom burden, higher anxiety scores, and higher depression scores than those with no/mild dizziness. Cadence during gait was also associated with the level of dizziness reported.

Introduction

Concussion remains a common, yet clinically challenging sports-related injury. ^1,2 Defined as a traumatic brain injury caused by biomechanical forces, ^1,3 concussions are among the most commonly researched sports-related injury. Yet, due to the complexity and individuality of the injury, further understanding is required across the many different domains affected by concussion to improve clinical care. Currently, it is recommended that sports medicine professionals take a multifaceted approach when evaluating a possible concussion, ^2–4 including assessment of symptoms, physical signs, balance impairment, behavioral changes, cognitive impairment, and sleep/wake disturbance. ^1–4

Vestibular disturbances are common after concussion, and dizziness is among the most frequent concussion symptom, affecting approximately 50–90% of patients.^5–7 The mechanism underlying post-concussion dizziness remains difficult to discern. Despite having separate mechanisms within the brain, vestibular and oculomotor deficits post-concussion often overlap causing symptoms in each domain simultaneously, and may each contribute to dizziness. For example, gait and convergence measures appear to be associated following concussion.⁸ Specific concussion symptoms such as blurred vision, lightheadedness, and/or sensitivity to noise or light and dizziness may also relate to sensory disturbances. ⁹ Thus, sensory dysfunction may result in patient-reported instability or dizziness. Additionally, cervical spine disturbances, including neck muscle strain or tightness, may also cause symptoms such as headache, dizziness, and vertigo.¹⁰ A clinical assessment of each domain, as well as other possible diagnoses, in conjunction, may aid in differentiating various treatment pathways and may be individualized for patients.

Vestibular dysfunction not only includes sensory systems that may induce dizziness, but may affect motor systems responsible for balance and postural control. Balance and postural control dysfunction has been well documented after concussion.^7,9,11–14 Thus, clinical practice guidelines emphasize the addition of a motor control assessment to concussion evaluation.^9,15 Previous studies have emphasized the importance of identifying both sensory and motor vestibular function during an initial concussion evaluation due to its potential negative effect on recovery.^6,7,9,16,17 Those who self-reported vestibular-oculomotor symptoms (e.g. dizziness and imbalance) may also have an longer recovery time.^5,9 A prolonged recovery time, specifically for those who experience symptoms for >28 days after initial injury, have an overall increased risk of anxiety, depression, impaired school performance and quality of life.^6,13

Persistent dizziness can subsequently cause a disinterest in activities that provoke dizziness due to the onset feeing of instability and discomfort.¹⁸ In theory, the abnormal feeling of dizziness can negatively affect an individual’s overall well-being, especially if they are recovering from a concussion at a slow rate. Research regarding the effects of acute or chronic dizziness and its role in the development of anxiety and depression symptoms after a concussion is limited despite studies investigating dizziness as a general psychiatric condition.^12,18 Specifically, researchers emphasized the relationship that feeling dizzy had on the disinterest of daily activities that would have normally not provoked symptoms.¹⁸ Also noted were the concurrent feelings associated with both anxiety and depression due to dizziness, further emphasizing the need for an additional emotional evaluation following concussion,¹⁸ which can potentially be a crucial step for a clinician in determining an appropriate treatment plan.

The relationship between self-reported dizziness with postural control deficits and psychosocial functioning after a concussion requires further investigation, in order to better define how the perception of dizziness may affect behavior. Thus, the purpose of our investigation was to examine the association between self-reported dizziness with concussion symptom severity, depression and anxiety symptom severity, and postural control within two weeks of sustaining a concussion. We hypothesized that participants who endorsed a moderate to severe level of dizziness would report a more severe concussion symptom burden, more severe depression and anxiety symptoms, and worse postural stability.

Methods

Study Design and Participants

We conducted a cross-sectional study of youth and young adult athletes who were diagnosed with a sport-related concussion by a physician and underwent testing within 14 days of injury. Testing was performed within a single research laboratory on a single occasion. Concussion was defined according to the consensus statement from the conference on concussion in sport held in Berlin 2016.³ We included patients who were between the ages of 14–21 years, and could complete the test within 14 days of their injury. We excluded those who reported a post-concussion symptom inventory (PCSI) score < 9, to ensure the patient was not recovered from their concussion, a history of neurological surgery or seizure disorder, using medication or a medical device that would alter heart rate, blood pressure, or autonomic function, or currently had an orthopedic and/or medial connection that would impair gait. All concussed participants were diagnosed by a board-certified physician within a regional sports concussion clinic or emergency department (ED). Participants either self-presented for care, were referred from the ED or their primary health care provider. A research coordinator approached patients during their clinical evaluation, after eligibility screening. Participation was voluntary.

Ethical Considerations

Prior to the study, institutional review board approval was obtained. All participants and their parents/guardians (if < 18 years of age) provided written informed consent to participate in the study.

Patient Reported Outcomes

To assess dizziness, participants completed the Dizziness Handicap Inventory (DHI). This scale has been used previously to determine the impact of dizziness on daily life by measuring self-reported handicap.¹⁹ The DHI has been determined to have excellent test-retest reliability, as well as internal consistency for total vestibular impairment scores.¹⁹ All question responses were assigned point values: 0 (no response), 2 (sometimes response), and 4 (yes response) on 25 questions, and a total score was computed from these scores, ranging from 0 – 100. Scores were then categorized into no (< 16), mild (16 – 35), moderate (36 – 51), or severe (>51) dizziness.¹⁹ Validity of the scale was established as higher scores demonstrated an increased level of functional impairment.^19,20 To address our primary study purpose, we divided participants into two groups: those who reported moderate/severe dizziness, and those who reported no/mild dizziness.

To assess concussion symptoms, participants completed the Post-Concussion Symptom Inventory (PCSI). The PSCI has been developed and validated specifically within the youth and adolescent population.^21,22 The PSCI was previously determined to have strong internal consistency and test-retest reliability.²² This scale contains 26-self-reported items with focus in four domains: cognitive, emotional, sleep, and physical. Symptoms are rated on a 7-point Guttman scale indicating severity from 0 (absent) to 6 (severe).²² The total PCSI score was then calculated as the sum of all symptoms. To ensure participants were not recovered at the time of testing, those who scored < 9 on the PCSI were then excluded.

To examine depression and anxiety symptoms, participants completed the Hospital Anxiety and Depression Scale (HADS) and Patient Health Questionaire-9 (PHQ-9). Awareness of psychological burden post-concussion has increased among clinicians and researchers in recent years.²³ The HADS scale asks participants to answer questions related to general anxiety and depression symptoms. It is a valid and reliable measure aimed at determining patients’ “loss of pleasure response (anhedonia)”.^24–26 Depression and anxiety symptoms are scored on two sub-scales. Both scales are considered as useful elements for measuring depression and anxiety symptoms in both a primary care setting as well as the general population.^25,27 The scale is dimensional in nature rather than categorical, with 14 total items, 7 for depression and 7 for anxiety, that are rated on a 4-point severity scale.²⁷ Reponses range from 0 (not at all) to 3 (a great deal of the time). A score between 0–7 is considered “normal”, 8–10 is “suggestive of the presence of the respective state”, and a score of 11 and higher is indicative of a “probable case”.²⁷

The PHQ-9 is the most commonly used measurement for screening for depression symptoms in the primary care setting. Derived from the full Patient Health Questionnaire (PHQ), the shortened scale is half the length of many other depression measures.^28,29 The PHQ-9, specifically contains the nine criteria to measure depressive symptoms.²⁹ A cut-off score of 10 or above has been previously determined to maximize sensitivity and specificity in diagnosing major depressive disorder.²⁸

Postural Stability Evaluation

Participants completed three different postural control tests: the modified Balance Error Scoring System (mBESS) test, single/dual-task tandem gait test, and a single- and dual-task instrumented steady-state gait analysis. During the mBESS, participants stood for 20 s on a solid surface (as opposed to the original BESS where additional trials are conducted on a foam pad) with their eyes closed in three positions: double-leg stance, single-leg stance, and tandem stance. During double-leg stance, they stood on both feet placed side-by-side. During single-leg stance, they stood on the foot that they identified as their non-dominant leg, and during tandem stance they stood with their feet positioned where the non-dominant foot was placed directly behind the dominant foot. During all trials, they were instructed to remain with their eyes closed and hands on their hips. Errors were counted if the participant opened their eyes, lifted their hands off their hips, took a step, fell out of the testing position, lifted any portion of the foot off the ground, abducted the hip greater than 30 degrees, or stayed out of the test position for 5 seconds or more. The outcome variable was the total number of errors, and errors committed in each stance, with the maximum being 10 errors per position.

To complete the tandem gait test, participants walked along a straight line with a heel-to-toe gait pattern, where they walked with their heel and toe in close approximation on each step. Once they crossed beyond the end of the 3m piece of tape, they turned and returned to the original starting point without stepping off of the line, having a separation between the heel and toe, or touching the test administrator. The test administrator used a standard stopwatch to measure test completion time to the nearest hundredth of a second. During dual-task trials, they were asked to complete one of three cognitive tests simultaneously. These tests included spelling five-letter words backwards, subtracting by 6s or 7s from a two-digit number, or reverse month recitation beginning with a randomly selected month. The test administrator provided the auditory cue via verbal instructions prior to trial commencement, confirmed the participant knew how to respond and allowed for practice trials until the participant understood the task, and recorded accuracy (correct or incorrect) of responses on each trial.

To assess steady-state gait performance, participants walked without shoes at a self-selected speed over level ground toward a target placed 8m in front of them, walked around the target, and returned to the original starting position without any other instructions during both single-task and dual-task conditions. During the evaluation, participants wore a set of inertial measurement sensors to quantify postural control performance (Opal sensors, MobilityLab, APDM Inc., Portland, OR, USA).^30,31 MobilityLab and APDM Opal sensors have been determined to have excellent test-retest reliability and validity throughout numerous available postural control test plug-ins.³² We attached the sensors to the spine at the level of the lumbosacral junction (to approximate center-of-mass), and on the dorsum of each foot using a strap. Sensor data were acquired at a sampling frequency of 128 Hz, synchronized, and wirelessly transmitted to a laptop computer. Dual-task gait trials consisted of the same procedure as single-task trials, but participants simultaneously completed a cognitive task, similar to the dual-task tandem gait test outlined above. Participants completed five trials in each condition, in random order, and outcomes were derived by calculating averages across trials. Outcome gait variables included average gait speed, stride length, and cadence during single-task and dual-task conditions, used previously to identify post-concussion impairments.⁸

Statistical Analysis

Continuous variables are presented as means (standard deviation) or median [interquartile range] dependent on the normality distribution of the data, and categorical variables are presented as the number and percentage of the group. We compared demographic, medical history, patient-reported outcomes, and postural control outcomes between moderate/severe and no/mild dizziness groups using independent samples t-tests for normally distributed continuous data, Mann Whitney U tests for non-normally distributed continuous data, and Fisher’s exact tests for categorical data. In addition, to describe the linear correlation between DHI scores with each outcome variable, we also performed bivariate correlation analysis using Pearson’s r correlation coefficients. Any missing data were treated as such, and no imputations were performed. All statistical tests were two-sided, evaluated with a significance level of α= 0.05, and performed using Stata version 15 (StataCorp, College Station, TX).

Results

Forty participants completed the study: 19 (48%) who reported moderate/severe dizziness, and 21 (52%) who reported no/minimal dizziness (Table 1). The two groups did not significantly differ on any demographic, medical history, or injury characteristics (Table 1). The group who reported moderate/severe dizziness reported significantly more severe symptoms, higher PHQ scores, and higher HADS depression and anxiety scores than the no/minimal dizziness group (Table 2). Total DHI score was strongly (r > 0.6) correlated with PCSI total score, PHQ score, HADS depression score, and HADS anxiety score (Table 2). There were no significant differences between groups on any of the clinical postural control tests (mBESS or tandem gait), or on cognitive performance during the dual-tasks, and weak correlations between overall DHI score and clinical test performance (Table 3). During steady-state gait, however, the moderate/severe dizziness group walked with significantly lower single-task cadence (Figure 1B) and dual-task cadence (Figure 1E) than the no/mild dizziness group. We did not observe any between-group differences for single-task gait speed (Figure 1A), dual-task gait speed (Figure 1D), single-task stride length (Figure 1C) or dual-task stride length (Figure 1F). Correlations between overall DHI score and gait performance were weak for single-task gait speed (r = −0.18), dual-task gait speed (r = −0.22), single-task cadence (r = −0.23), dual-task cadence (r = −0.27), single-task stride length (r = −0.09), and dual-task stride length (r = −0.13).

Table 1.

Demographic characteristics of the moderate/severe dizziness and no/mild dizziness participant groups. P-values are based on t-test (for continuous variables) and Fisher’s exact test for categorical ones.

Variable	No/mild dizziness (n=21)	Moderate/severe dizziness (n=19)	P value
DHI Score	18.7 (9.3)	48.4 (12.6)	< 0.001
Age (years)	16.5 (1.9)	17.1 (2.4)	0.36
Sex (female)	8 (38%)	12 (63%)	0.21
Height (cm)	170.5 (10.9)	169.5 (7.8)	0.74
Weight (kg)	65.6 (14.3)	65.8 (8.9)	0.96
Race	White: 18 (86%) Native Hawaiian/Other Pacific Islander: 1 (5%) Asian: 1 (5%) More than one race: 1 (5%)	White: 14 (74%) More than one race: 3 (16%) Black/African American: 1 (5%) Unknown: 1 (5%)	0.27
Contact/collision sport played during injury	15 (71%)	16 (84%)	0.46
LOC at time of injury	4 (19%)	5 (28%)	0.71
Memory loss at time of injury	7 (33%)	7 (37%)	> 0.99
History of ADHD	3 (14%)	0 (0%)	0.23
History of anxiety	3 (14%)	5 (26%)	0.44
History of depression	2 (10%)	3 (16%)	0.65

Table 2.

Comparison of patient-reported concussion symptom, depression, and anxiety outcomes between moderate/severe dizziness and no/mild dizziness participant groups.

Variable	No/mild dizziness (n=21)	Moderate/severe dizziness (n=19)	P value	Correlation with DHI score (r)
PCSI Total Score	22.8 (15.7)	43.0 (20.6)	0.001*	0.62
PCSI Pre/Post Injury Score Difference	19.5 (14.4)	35.2 (23.0)	0.01*	0.48
PHQ Score	4.5 (2.9)	10.1 (4.2)	< 0.001*	0.78
HADS Depression Score†	1 [1, 3]	6 [3, 7]	0.001*	0.67
HADS Anxiety Score†	2 [0, 4]	6 [5, 8]	< 0.001*	0.74

^†Data were non-normally distributed, and are presented as median [interquartile range]. p-values are based on Mann-Whitney U test

Table 3.

Postural stability and cognitive task performance comparisons between moderate/severe dizziness and no/mild dizziness participant groups.

Variable	No/mild dizziness (n=21)	Moderate/severe dizziness (n=19)	P value	Correlation with DHI score (r)
Single-task tandem gait time (seconds)	20.7 (5.0)	20.2 (5.9)	0.77	−0.07
Dual-task tandem gait time (seconds)	26.2 (6.4)	25.5 (7.0)	0.76	−0.15
mBESS total errors†	3 [2, 9]	5 [4, 8]	0.16	−0.02
mBESS double stance errors†	0 [0, 0]	0 [0, 0]	0.91	0.11
mBESS single stance errors†	2 [1, 4]	3 [2, 5]	0.22	−0.04
mBESS tandem stance errors†	1 [0, 3]	2 [0, 3]	0.74	−0.07
Dual-task tandem gait: cognitive tasks completed†	22.5 [17, 27.5]	22 [15, 23]	0.59	−0.09
Dual-task tandem gait: cognitive accuracy (% correct) †	96 [91, 100] %	96 [93, 100] %	0.81	0.04
Dual-task steady-state gait: cognitive tasks completed†	19 [14, 23]	19 [16.5, 21]	0.97	0.04
Dual-task steady-state gait: cognitive accuracy (% correct) †	94 [90, 100] %	94 [89, 100] %	0.69	0.13

^†Data were non-normally distributed, and are presented as median [interquartile range]. p-values are based on Mann-Whitney U test.

Figure 1.

Single-task (A,B,C) and dual-task (D,E,F) steady-state gait performance comparisons between the moderate/severe and no/mild dizziness groups.

* Single-task cadence (mean difference = 4.8, 95% confidence interval = 0.8, 8.8) and dual-task cadence (mean difference = 7.4, 95% confidence interval = 0.7, 14.0) were significantly different between groups.

After removing the “Balance problems”, “Dizziness”, and “Move in a clumsy manner” elements from the total PCSI and pre/post PCSI score calculations, we observed the group who reported moderate/severe dizziness reported significantly more severe symptoms than the group who reported no/minimal dizziness (37.7±7 vs. 20.1±3.1; p=0.001). Similarly, the pre/post PCSI change after removing these elements was more severe for the moderate/severe dizziness group compared to the no/minimal dizziness group (30.7±4.5 vs. 17.2±12.7; p=0.01).

Discussion

Following a concussion, dizziness may affect different functional domains such as postural stability, return to sport, and quality of life.^5–7,13,16 The results from our study indicate patients who experience moderate/severe dizziness after a concussion also report more subjective symptoms (PSCI, HADS, DHI) than those with no/mild dizziness. Furthermore, those with moderate/severe dizziness walked with a slower cadence during both single- and dual-task trials than those with no/mild dizziness. These findings support our hypotheses that those with more severe dizziness report more severe concussion, anxiety, and depression symptoms, and demonstrate poorer postural stability.

A conservative gait strategy after concussion has been well-documented where walking kinematics are altered despite clinical symptom resolution.^9,33–35 It has been previously suggested that injured athletes may alter their gait pattern in order to reduce time in less stable positions following concussion.³³ Particularly for patients who experience a feeling of unsteadiness after concussion, a conservative gait may be a method for regulating their equilibrium,^35,36 and one strategy to achieve this is through a slower cadence (i.e. reducing step frequency). In a cohort of adults with diagnosed chronic subjective dizziness, researchers found that their overall cadence, and stride length was slower than healthy controls, and consequently they walked with slower gait speed.³⁶ In the present study, our participants who experienced a greater severity of dizziness walked with lower step frequency than those with mild to no dizziness. Interestingly, gait speed and stride length was not significantly different between groups. This may have occurred for different reasons, and our study was not equipped to specifically address this. The slower cadence for those with moderate/severe dizziness may have potentially been a conscious or subconscious decision to alter gait kinematics to ensure stability during forward locomotor progression. Regardless of the mechanism initiated to elicit this gait pattern, our results indicate a neurological adaptation to maintain a walking pattern that is stable among those with a perceived disturbance to the vestibular system. In addition, several of the clinical variables obtained such as tandem gait, dual-task cognitive performance, and static balance control did not show any significant association with dizziness severity. These approaches may have been less sensitive to subtle dizziness-related effects that were more apparent using instrumented gait analysis (i.e. our observation of an association between dizziness severity and walking cadence).

Our study participants who reported feeling moderate/serve dizziness also reported more severe anxiety and depression symptoms. This indicates a potential psychological association between participants based on their perceptual dizziness handicap, and suggests overlap in different domains of self-reported symptoms after a concussion. Previous work among adults suffering from either acute or chronic dizziness, regardless of severity, indicated emotional distress was correlated with anxiety and depression severity.^18,36 Anxiety has been noted to provoke and prolong vestibular symptoms due to the worry around doing activities that may provoke dizziness.¹⁸ In a different adult population with mild or moderate traumatic brain injuries, those with dizziness as a main symptom reported to have higher depression and anxiety scores, and were less likely to return to everyday activities than those without dizziness symptoms.³⁷ Both of these previous studies emphasize the need for clinicians to assess dizziness among patients being treated for concussion, and consider methods to evaluate vestibular dysfunction.

The return to play and recovery time after a concussion is individualized and based on numerous criteria, making prognosis and expectations challenging. The stress of coping with an injury without a known or expected recovery date and the possibility of prolonged symptoms may create an environment where there is a high psychological burden on an athlete.^23,38 Some patients may begin to wonder when or if future sport participation will begin again. Interestingly, previous work has identified that athletes who are recovering from a concussion often received less support from teammates and athletic trainers during treatment, when compared to those who suffer from a musculoskeletal injury.³⁸ Potentially due to the internal nature of a concussion relative to an external orthopedic injury, many athletes find that their peers do not understand the degree to which they are injured.³⁸ Normalizing what an athlete who has sustained a concussion is feeling after injury may influence their symptom burden and even duration of symptoms. In the case of vestibular symptoms, there is supporting evidence that suggests vestibular rehabilitation is effective in improving dizziness and postural control, as well as reducing time to medical clearance after concussion.^7,39 Implementing this therapy may help patients understand that their recovery from a concussion is unique to other orthopedic injuries.

Our investigation had several limitations and interpretation of our findings should be made in light of them. Our participants were tested at one point in time, at a single testing site, from a single recruitment location, and consisted of only youth and young adult athletes. Therefore, we cannot generalize or extrapolate our findings to other geographical locations or patient populations. Further longitudinal studies that monitor dizziness and its associations with gait and psychological symptoms of a concussion in various age groups and at various post-injury time points may assist in more individualized treatment plans for those who suffer from concussion. Additional objective measures of dizziness or vestibular-oculomotor function may also augment our findings in future studies, as our dizziness measure was obtained from a self-reported questionnaire.

Our results suggest that following concussion, moderate and severe dizziness are associated with more severe concussion symptom burden, anxiety symptoms, depression symptoms, and a more conservative gait pattern. Early identification of dizziness as a substantial part of symptom burden may lead to appropriate individualized clinical management of psychological symptoms during recovery.

List of Abbreviations:

DHI

Dizziness Handicap Inventory

HADS

Hospital Anxiety and Depression Scale

mBESS

modified Balance Error Scoring System

PCSI

Post-Concussion Symptom Inventory

PHQ-9

Patient Health Questionaire-9