Pediatric Physical Therapy:
Reliability and Diagnostic Accuracy of Clinical Tests of Vestibular Function for Children
Christy, Jennifer B. PT, PhD; Payne, JoAnne MA, CCC-A; Azuero, Andres PhD, MBA; Formby, Craig PhD
Department of Physical Therapy, School of Health Professions (Dr Christy), and Department of Community Health, Outcomes and Systems, School of Nursing (Dr Azuero), The University of Alabama at Birmingham, Birmingham, Alabama; Department of Communicative Disorders (Ms Payne and Dr Formby), College of Arts and Sciences, The University of Alabama, Tuscaloosa, Alabama.
Correspondence: Jennifer B. Christy, PT, PhD, Department of Physical Therapy, The University of Alabama at Birmingham, 1720 2nd Ave S, SHPB 360X, Birmingham, AL 35294 (firstname.lastname@example.org).
Grant Support: This study was funded by a research grant from the Section on Pediatrics, awarded to Dr Christy.
The authors declare no conflicts of interest.
Purpose: To determine reliability, diagnostic values, and minimal detectable change scores, 90% confidence (MDC90) of pediatric clinical tests of vestibular function.
Methods: Twenty children with severe to profound bilateral sensorineural hearing loss and 23 children with typical development, aged 6 to 12 years, participated. The Head Thrust Test, Emory Clinical Vestibular Chair Test, Bucket Test, Dynamic Visual Acuity, Modified Clinical Test of Sensory Interaction on Balance, and Sensory Organization Test were completed twice for reliability. Reference standard diagnostic tests were rotary chair and vestibular evoked myogenic potential. Reliability, sensitivity, specificity, predictive values, likelihood ratios, and MDC90 scores were calculated.
Results: Reliability ranged from an intraclass correlation coefficient of 0.73 to 0.95. Sensitivity, specificity, and predictive values, using cutoff scores for each test representing the largest area under the curve, ranged from 63% to 100%. The MDC90 for Dynamic Visual Acuity and Modified Clinical Test of Sensory Interaction on Balance were 8 optotypes and 16.75 seconds, respectively.
Conclusions: Clinical tests can be used accurately to identify children with vestibular hypofunction.
The reported incidence of vestibular-related deficits in children has grown.1,2 Impairments identified in this group are poor gaze stability with head movement, as well as delayed development of postural control and motor skills.3–6 These impairments persist and progress throughout childhood, adversely affecting high-level gross motor function, reading ability, and school performance.7–11 Although studies demonstrate the effectiveness of vestibular exercise in children with hypofunction,3,12,13 vestibular function is rarely tested because simple inexpensive clinical tests of vestibular function have not been developed for children. Because of the known adverse effect of vestibular impairment on motor function, postural control, and stability of gaze, there is a pressing need for valid, reliable, and simple tests to assess children's peripheral vestibular system integrity.
The development of valid and reliable testing tools for pediatric assessment is warranted because of increasing reports of vestibular dysfunction in children, including benign positional vertigo,14 vestibular neuronitis,15,16 otitis media,17 and drug-induced vestibulopathy.18 Variability of reported incidence of vestibular hypofunction (VH) (30%-100%) in children with sensorineural hearing loss (SNHL) exists because of differences in study populations and vestibular testing.19–23
Cushing et al20,21 measured vestibular function by using reference standard tests of caloric, rotary chair and vestibular evoked myogenic potential (VEMP).24 Caloric testing detects unilateral vestibular hypofunction (UVH) of the horizontal canal. Caloric testing is a potentially frightening experience for children since cold and warm water must be placed in the ear, which elicits vertigo.25 The rotary chair test also evaluates horizontal canal function. It uses natural rotational stimulation to detect bilateral vestibular hypofunction (BVH) and is tolerated by most children. Vestibular evoked myogenic potential tests the saccule, which contributes to the vestibulospinal system and postural control.24 Pediatric normative data are available for the rotary chair and VEMP tests.26–28 Cushing et al20 found that 9 of 9 children with profound deafness following bacterial meningitis had VH. Their balance scores, measured using the balance subscale of the Bruininks-Oseretsky Test of Motor Proficiency, were less than that of peers who were not hearing impaired and children with SNHL but normal vestibular function. In a separate study, Cushing et al21 tested 153 children with congenital and acquired SNHL of varying etiologies and found that 50% had measurable VH; 37% of these children had severe VH or areflexia.
Clinical tests of the vestibulo-ocular reflex or horizontal canal function include the Head Thrust Test (HTT; response to head turns right/left), the Dynamic Visual Acuity test (DVA; acuity difference with head still and moving at 2 Hz), and the Emory Clinical Vestibular Chair Test (ECVCT; time of nystagmus following rotations in the dark). A clinical test of utricular function is the Bucket Test of subjective visual vertical (SVV): ability to perceive a line as vertical in the absence of visual cues. Although reliability and validity of these tests have been reported for adults,29–32 the only test with reported reliability, sensitivity, and specificity for children is the DVA test.33,34 The DVA test had good inter- and intratester reliability (intraclass correlation coefficient [ICC] = 0.94 and 0.84, respectively) and 100% sensitivity/specificity for identifying children with confirmed BVH.33 The HTT had good sensitivity/specificity for adults with unilateral and bilateral caloric weakness.29,30 The ECVCT had moderate to good test-retest, intrarater, and interrater reliability for adults (r > 0.70). Sensitivity was 78%, specificity was 92% for identifying 5 adult subjects with VH.35 The Bucket Test is a low-technical version of the laser SVV that tests utricular function. Zwergal et al31 reported that healthy adults were able to perceive true vertical within 0.9 ± 0.7°. Subjects with vestibular deficits perceived vertical within 8.9 ± 5.4°. Inter- and intratester reliability of the Bucket Test were r = 0.90 and r = 0.92, respectively.
Postural control involves input from the vestibular, visual, and somatosensory systems. Studies have shown that children with VH also have poor postural control.3,22 A clinical test of postural control is the Sensory Organization Test (SOT). The SOT is not a direct measure of vestibulospinal function but determines how vestibular information is used to control posture.36 The ICC demonstrating reliability of the SOT was greater than 0.75 for children with and without VH.37,38 However, many clinics do not have access to the equipment required to complete the SOT. The Clinical Test of Sensory Interaction on Balance (CTSIB)39 was designed as a low-technical SOT and has been used in studies of postural control in adults40,41 and children.42,43 The original test had 6 conditions to mimic SOT. A dome was used for sway-referenced visual conditions and thick foam for sway-referenced somatosensory conditions. The pediatric version (P-CTSIB) also included tandem and single-legged stance conditions.42,43 The CTSIB was modified, dome conditions were removed, and the test was validated for adults at risk for falls.41,44 Good test-retest and interrater reliability (r ≥ 0.75), and moderate correlations with SOT, were reported for adults.41,45,46 Reliability and validity of the Modified Clinical Test of Sensory Interaction on Balance (MCTSIB), without extra conditions used in the P-CTSIB, have not been established for children.
The purpose of this preliminary study was to determine reliability, sensitivity, specificity, predictive values, likelihood ratios, and cutoff scores for clinical tests of vestibular function. The clinical tests (ie, HTT, Bucket Test, DVA, MCTSIB, and ECVCT) were compared with reference standard tests (ie, VEMP and rotary chair) in a small cohort of children with severe to profound SNHL.
A convenience sample was recruited from the Birmingham, Alabama, community. To be included, subjects had to be between 6 and 12 years of age and diagnosed with severe to profound SNHL as determined by audiometric testing. Subjects were excluded if they showed evidence of neurological, central visual, or musculoskeletal abnormalities, fear of darkness, motion sensitivity, or a history of neck trauma. Inclusion and exclusion criteria were determined via phone interview with a parent before the first testing session and via neuromuscular screen. Twenty children with severe to profound SNHL (mean age = 8.9 ± 1.8 years) and 23 children with typical development (mean age = 9.5 ± 2.9 years) participated (Table 1). The Institutional Review Boards at The University of Alabama at Birmingham and The University of Alabama, Tuscaloosa, approved this study. Parents and children provided informed consent.
After obtaining informed consent, subjects completed 3 testing sessions. The first session began with a neuromuscular screen composed of oculomotor tests (ie, smooth pursuit, saccades, vergence, ocular range of motion); cerebellar tests (ie, rapid alternating movements, heel to shin); manual muscle testing and range of motion. Children with abnormal results were excluded.
The same examiner, with 20 years of pediatric physical therapy experience and advanced training in vestibular rehabilitation, completed clinical tests (J.B.C.). Published methods29 were used for HTT. Facing the subject at eye level, the examiner flexed the neck 30° to maximally stimulate the horizontal canal. This was done using an imaginary line between the lateral canthus of the eye and the external acoustic meatus. The subject attempted to keep the eyes on the examiner's nose, which was decorated with a sticker. The subject's head was unpredictably and quickly turned to the right and left from center at an amplitude of 5° to 10°. The examiner watched for a corrective saccade following each HTT, and then the head was returned to center. This maneuver was randomly repeated 3 times in each direction. The HTT was positive if at least 2 corrective saccades were observed to the right and/or the left.
Modified methods were used for the modified ECVCT (m-ECVCT).35 The subject sat in a rotating office chair with the head centered and slightly flexed and eyes closed. The chair was rotated right for 30 seconds at 0.5 Hz, using a metronome. This timing differed from the original test,35 which rotated adult subjects for 60 seconds. During development of the protocol before data collection began, it was determined that younger children became restless and tried to open their eyes after 30 seconds. Therefore, after 30 seconds of rotation, the chair was stopped and the timer started. The subject did not open the eyes until infrared camera goggles were placed over the eyes, blocking fixation. The goggles were not placed on the eyes during rotation to avoid damage to the goggle cables. Nystagmus was observed on the monitor and timed until it subsided. The subject rested for 2 minutes or double the duration of nystagmus to dampen the effect of the first rotation.35 The test was then repeated to the left. All subjects received rightward and then leftward rotations. We used 2 examiners. One examiner rotated the chair and held the goggles on the subject's face. The other examiner timed duration of nystagmus. The examiners were trained by the primary investigator (J.B.C.) and practiced before testing. To determine interrater reliability, nystagmus was videorecorded so that raters could later watch and time the nystagmus. To determine whether or not goggles were necessary, the test was repeated without goggles. After rotating with eyes closed, the subject looked at a white sheet and nystagmus was timed. Nystagmus was again videotaped so that interrater reliability could be determined later. Four trained examiners scored the videos, and scored the same videos 1 week later. For intra- and interrater reliability of the m-ECVCT, fixation removed, 2 examiners scored the videos.
For the Bucket Test, a straight line was drawn into the bottom of an opaque bucket (23.5-cm diameter and 24-cm long). An angle finder was placed on the bottom of the bucket in the same plane as the line.31 Each subject practiced with the bucket held away from the face (ie, available visual cues) until the examiner was certain that the subject understood the task. Subjects also confirmed that the only object they could see when the bucket was held over the face was the line. After training, the subject was seated with eyes closed. The mouth of the bucket was placed around the subject's face and the examiner turned the bucket to set the line off vertical. The subject then opened the eyes. As the examiner slowly turned the bucket, the subject said “now” when the line reached vertical. The angle of degrees and direction off 0° was recorded for 10 trials of clockwise and counterclockwise rotations. The mean degrees off 0° and mode of direction tilted (ie, left, right, or straight) were calculated.
For the DVA test, the subject sat 10′ away from the Lea Symbols (ie, house, circle, heart, and square) chart. The chart had a total of 15 lines of 5 optotypes, ranging from Snellen acuity levels of 20/200 to 20/8. The subject began at an acuity level where all symbols on a line could be correctly identified, and continued to identify progressively smaller symbols until no symbol could be identified.33 The number of optotypes unable to be identified was static visual acuity. For the DVA, the neck was flexed 30° by using the same anatomical landmarks as for the HTT, the head was moved at 2 Hz (120° per second) to a metronome in the yaw plane, and the number of unidentified optotypes was recorded. The DVA was completed twice, averaged, and scored as the difference in optotypes missed between the DVA and static visual acuity tests.
For the SOT, the subject wore a safety harness and stood on the SMART EquiTest platform (NeuroCom, a division of Natus, Clackamas, Oregon). The subject stood still during 6 conditions: (1) stable platform, (2) stable platform eyes closed, (3) sway-referenced visual surround, (4) sway-referenced platform, (5) sway-referenced platform eyes closed, and (6) sway-referenced visual surround and platform. A blindfold was used for eyes closed conditions. Each condition lasted 20 seconds, and 3 trials were completed. On the basis of reports that children with hypofunction have low visual, vestibular, and somatosensory effectiveness ratios,3,47 these ratios were calculated as follows: somatosensory = 3/1; visual = 4/1; and vestibular = 5/1.48
For the MCTSIB, the subject stood barefoot with arms across the chest and feet together for 30 seconds during 4 conditions: (1) floor eyes opened; (2) floor eyes closed; (3) Neurocom foam eyes opened; and (4) Neurocom foam eyes closed. A blindfold was used for eyes closed conditions. On eyes opened conditions, subjects faced a white sheet. Three trials of each condition were completed only if the subject was unable to complete the entire 30 seconds on the first or second trial. If the child completed 30 seconds on the first trial, a score of 30 seconds was given for that condition. The mean of the 3 trials was calculated for each condition and then added for a total score (maximum = 120 seconds, 30 seconds for each of the 4 conditions).
The HTT, Bucket Test, DVA, MCTSIB, and m-ECVCT were completed a second time, 4 hours to 7 days later, for test-retest reliability. Some children were unable to be tested on 2 separate days, whereas others preferred to return on a different day. Given the nature of the tests, we felt that 4 hours was sufficient time to negate effects of the first testing session, and 7 days was short enough to negate effects of maturation. Reference standard tests were completed within 1 month after the clinical tests by an audiologist with 24 years of experience, blinded to clinical test results. Reference standard test results were not expected to change in 1 month.
Reference Standard Tests
The cervical VEMP (cVEMP) assessed the function of the saccule and inferior vestibular nerve following protocols previously reported.49,50 Before testing, subjects were examined with otoscopy and tympanometry to ensure the ears were free of obstruction. Subjects sat in a semireclined position during the test. Following electrode placement, subjects turned the head to activate the sternocleidomastoid. Electromyography with video feedback assured that baseline sternocleidomastoid muscle activity was between 35 and 50 μV. Tone burst stimuli (ie, 500 Hz with 2-0-2 rise-plateau-fall) were presented at 97 dB normal hearing level (nHL) or 105 dB nHL at a rate of 5 per second with rarefaction polarity. One subject had complete atresia of both ear canals, requiring protocol modification. For this subject, stimuli were presented via B71-10 bone conduction vibrator placed on the mastoid bone.51 Recordings were amplified with a gain of 5000×, for a bandpass setting of 2 to 250 Hz, and time window of 30 millisecond. The initial positive and negative peaks were marked, and the P1-N1 amplitude asymmetry ratio was calculated. Subject responses were compared with normative data.27,52 Responses greater than 2 SDs from the normative mean were considered positive.
Oculomotor tests, laser SVV, and sinusoidal harmonic acceleration (SHA) were completed as was step rotation testing using a Neuro Kinetics, Inc (Pittsburgh, Pennsylvania) Rotary Chair with VEST 6.10 software. Videonystagmography measured eye movements through infrared cameras on I-Portal 100-Hz binocular video oculography goggles. Subjects were seated in a chair with a computer-controlled motor within a closed booth in complete darkness. If necessary, small children sat in the lap of an adult. Calibration of eye movement was performed before testing. An adult investigator sat in the darkened room and used a radio for communication with the audiologist, who visually monitored the test via infrared cameras. Alerting tasks were used.12,27,28
Oculomotor tests (ie, smooth pursuit, saccades, and optokinetic nystagmus) were completed to rule out central visual problems. The gain and accuracy of eye movements were compared with pediatric normative data (Neuro Kinetics, Inc). The SVV paradigm was based on previously reported methods.53 The subject practiced the technique in room light until he or she understood. In complete darkness, the subject set the off-vertical laser line to perceived vertical, using buttons that rotated the line clockwise or counterclockwise in 0.1° increments. The subject said “now” when he or she perceived that the line was vertical. The test was repeated 5 times to each side and responses were averaged.
Rotary chair tests included the SHA and step rotations to measure horizontal canal function. The subject's head was pitched forward 30° and gently immobilized. For the SHA test, 5 frequencies were examined (ie, 0.01, 0.04, 0.08, 0.16, and 0.64 Hz) at 60° per second over 3 to 9 cycles. Data included phase, gain, and asymmetry of the vestibulo-ocular reflex response. Step rotation testing included a series of complete chair rotations to both the right and left (ie, 100° per second for 60 seconds). Pre- and postrotary time constants (ie, the amount of time required for nystagmus to decrease to 37% of its original strength) were measured. Results were compared with normative data and scored as follows: (1) negative, within 1.5 SDs of the comparative sample mean; (2) bilateral loss (positive), reduced gain values outside the comparative range; and (3) unilateral loss (also positive), abnormal phase and asymmetry values in the presence of normal gain values.12,27,28 If either the rotary chair (ie, SHA, step rotation) or cVEMP tests were positive, the vestibular result was classified as a “positive” diagnosis. Subjective visual vertical was not used for classification due to lack of pediatric normative data.
Descriptive statistics were computed for participant characteristics and clinical tests scores. For each clinical test, a receiver operating characteristic curve determined optimal cutoff scores for classification of VH as diagnosed by reference standard tests. The area under the ROC curve (AUC) was tabulated for comparison of accuracy among clinical tests. The closer an AUC to the maximum value of 1, the more accurate the test. After cutoff scores were determined, cross-tabulations between hypofunction status and clinical test results were conducted to estimate the frequencies of true positive (TP), false positive (FP), true negative (TN), and false negative (FN) classifications. Measures of sensitivity (TP/(TP+FN)), specificity (TN/(TN+FP)), positive predictive value (TP/(TP+FP)), negative predictive value (TN/(TN+FN)), positive likelihood ratio (sensitivity/(1 − specificity)) and negative likelihood ratio ((1 − sensitivity)/specificity), and 95% confidence intervals (CIs) were computed. The Delta logit method54 and the method by Simel et al55 were used to estimate proportion and likelihood ratio CIs, respectively. Repeated assessments estimated test-retest reliability and interrater reliability with the ICC;56 95% CIs for these measures were computed with the Fisher z transformation. Pearson correlations were used to examine linear associations. To determine the minimal detectable change (90% confidence) (MDC90), the following formula was applied:57 MDC90 = 1.65 × pooled SD × √(2[1 − ICC]). Analyses were conducted using SAS version 9.3 (SAS Institute, Cary, North Carolina).
Nineteen of 20 subjects with SNHL completed reference standard tests. All subjects had normal results on the neuromuscular screen and oculomotor tests. Of this group, 3 subjects had BVH, 5 had UVH, and 11 had normal vestibular function (NVF). One child, aged 6 years, refused reference standard testing but completed clinical tests. Two subjects with typical development (TD) completed reference standard and clinical tests. Twenty-three subjects with TD completed some or all of the clinical tests (Figure 1).
Test-retest reliability was good (ICC ≥ 0.73) for all clinical tests except for condition 4 of the MCTSIB (Table 2). Two tests that can be used to detect change due to intervention are DVA and MCTSIB. The MDC90 for these outcomes were 8 optotypes for DVA and 16.75 seconds for the MCTSIB total score. Intrarater reliability for the m-ECVCT in room light was good for the 4 raters. The ICC ranged from 0.76 (95% CI, 0.51-0.89) to 0.97 (95% CI, 0.92-0.99). However, interrater reliability was poor for the 4 raters on the m-ECVCT room light. The ICC ranged from 0.37 (95% CI, 0.10-0.62) for left rotations to 0.40 (95% CI, 0.13-0.65) for right rotations. Intra- and interrater reliability was high for 2 raters on m-ECVCT with fixation removed; ICC = 0.86 (95% CI, 0.67-0.93) for left + right rotations.
Moderate to good correlations were found between the m-ECVCT fixation removed, the m-ECVCT room light, and the rotary chair time constant. The m-ECVCT room light total score correlated with the m-ECVCT fixation removed total score (r = 0.59 [95% CI, 0.22-0.80]). The m-ECVCT fixation removed after spinning right/left correlated moderately with the rotary chair time constant after spinning right/left—right: r = 0.66 (95% CI, 0.31-0.84); left: r = 0.81 (95% CI, 0.55-0.92). A fair correlation was found between SOT composite scores and the MCTSIB total scores (r = 0.37; P = .02). However, a moderate to good correlation was found between the MCTSIB total scores and SOT vestibular ratios (r = 0.58; P < .001). The correlation between the Bucket Test mean degrees off center and laser SVV mean scores was not statistically significant (r = −0.34; P = .13).
Means and SDs for all clinical tests are provided in Table 3. The optimal cutoff scores to predict hypofunction for clinical tests, on the basis of the AUC, are summarized in Table 4. Positive and negative likelihood ratios with CIs are provided in Table 5. Except for the Bucket Test, all clinical tests had an AUC ranging from 0.64 to 0.89. The Bucket Test had an AUC of 0.55, indicating slightly better than chance prediction of hypofunction. The highest overall values were obtained with the HTT (sensitivity = 75%; specificity = 91%), the MCTSIB total score (sensitivity = 88%; specificity = 85%), the m-ECVCT fixation removed (sensitivity = 63%; specificity = 100%), the SOT vestibular ratio (sensitivity = 75%; specificity = 92%), and the DVA (sensitivity = 88%; specificity = 69%). Likelihood ratio CIs were wide because of the low prevalence of hypofunction in the sample.
All 5 subjects with UVH had a laser SVV result greater than 2°, tilted to the lesioned side in all but 1 subject. One subject with BVH had an abnormal laser SVV. Forty-five percent of subjects with normal rotary chair and cVEMP results had abnormal laser SVV results. Both subjects with TD who completed testing had laser SVV results less than 2°. Laser SVV results agreed with the Bucket Test results in only 38% of cases.
This is the first study to determine reliability and diagnostic accuracy for pediatric clinical tests of vestibular function. The HTT had good test-retest reliability and correctly predicted vestibular function scores with 88% agreement. Schubert et al29 tested subjects with UVH/BVH and compared the HTT with caloric tests. Sensitivities for subjects with UVH and BVH were 71% and 84%, respectively. Specificity was 82%. In the current study, we combined subjects with UVH (n = 5) and BVH (n = 3) because of low prevalence. Even so, the HTT was reliable (ICC = 0.73), sensitive (75%), and specific (91%). The HTT was simple and required no special equipment. However, clinicians should practice correct technique.
Similar to adult performance,41 the MCTSIB total score was reliable. The sensitivity, specificity, and predictive values were 78% or greater for a cutoff score of 110 total seconds. However, if only doing condition 4 of the MCTSIB, test-retest reliability decreased (ICC = 0.56). Therefore, we recommend that all conditions of the MCTSIB be completed. If using the MCTSIB as an outcome tool to measure improvement, then the MDC90 score of 16.76 seconds should be used. The moderate to good correlation between the SOT vestibular ratio and the MCTSIB score indicated that the latter provided information about vestibular input to postural control. This differed from the findings of Gagnon et al,58 who reported that the Pediatric CTSIB and SOT did not correlate and concluded that the 2 tests measured sensory organization differently. In the current study, we did not do tandem or single-legged stance conditions. We also used the vestibular ratio rather than the SOT stability scores. The clinical DVA test was reliable and predicted vestibular function test results with a 76% success rate, using a cutoff score of 10 optotypes (ie, 2 lines). This differed from a previous study that reported a 100% success rate for predicting hypofunction.33 Unlike original study methods, we continued testing until the subject missed all optotypes on a line and then counted the total number of missed optotypes, pushing subjects to their limit of the DVA. The original test33 ended when subjects missed 3 optotypes on a line. The DVA test can be used to determine whether or not gaze stability exercises are working.59 A change in the DVA score of greater than 8 optotypes (or approximately 1.6 lines) can be considered a change that is greater than error.
The m-ECVCT with fixation removed was reliable and predicted vestibular function with 86% accuracy, using a cutoff of 29.2 seconds (ie, following 30-second left + right rotations). It correlated moderately with the rotary chair time constant. The m-ECVCT in room light had good test-retest and poor interrater reliability. The cutoff score of 15.3 seconds yielded only 65% correct prediction. The 4 raters who participated in the interrater reliability study commented that it was difficult to determine when nystagmus stopped in room light. Some children fixated and stopped nystagmus immediately. Therefore, this test should be done with fixation removed.
The Bucket Test had good test-retest reliability of mean degrees off vertical, poor reliability for direction, and did not correlate with the laser SVV results. A cutoff score could not be determined because the AUC was only slightly better than chance. These results differed from those obtained by Zwergal et al,31 who found good reliability, sensitivity, and specificity of the Bucket Test. In adults, SVV in the acute stage following UVH tilts toward the side of the lesion. Studies differ as to when or if SVV ever fully compensates.60 We do not know how SVV compensates in children with VH because adult paradigms of utricular testing have not been tested in children.61,62 To our knowledge, this is the first study to report SVV results in children with VH. Given the results of the laser SVV in this study, it is tempting to hypothesize that the children with UVH had static uncompensated deficits, whereas the 5 subjects with normal vestibular function tests but abnormal performance for laser SVV had a utricular deficit. Except for 1, subjects with BVH did not have asymmetric SVV, which was expected. Utricular function should be tested in larger numbers of children with and without VH using the ocular VEMP, a laboratory test of utricular function.63
Cochlear implantation is increasingly being offered for individuals with severe to profound SNHL.64 The surgery involves an array of electrodes inserted into the cochlea to send electrical signals to the auditory nerve.65 Histological studies revealed saccular damage in some children who received cochlear implantation, ostensibly due to trauma during electrode insertion into the cochlea, which lies in close proximity to the saccule.66,67 In these cases, persisting vertigo occurred when the device was activated.66 In contrast, some subjects demonstrated better balance with the cochlear implant turned on than off.19,68,69 Importantly, children undergoing cochlear implant surgery should be screened for vestibular deficits.
The timing of vestibular injury is important. The vestibulo-ocular reflex develops rapidly during the first 2 years of life.70 The use of vestibular input for postural control does not become adult-like until after the age of 15 years.71 Therefore, an adult who developed typically and acquired VH will differ from a child who did not develop with a functioning vestibular system. The current study included subjects with chronic VH. It is possible that test results might differ in subjects with acute lesions.
To apply the results of this study in a clinical context, we will consider the subject who refused reference standard tests. This was a 6-year-old girl with SNHL, of unknown origin. She had bilateral cochlear implant surgery at the age of 4 years. She walked independently at 15 months of age and had a normal neurological and oculomotor screen. She presented with positive HTT bilaterally and a static visual acuity and DVA score difference of 34 (>10 optotypes cutoff). Her MCTSIB total score was 95.57 seconds (<110 cutoff). All conditions on the MCTSIB were normal except for the foam eyes closed condition (5.57 seconds). She refused the SOT. The m-ECVCT score was 23.3 seconds (<cutoff of 29.2 seconds). According to clinical tests, this child likely has BVH affecting gaze stability and balance. This child could potentially benefit from vestibular exercises.3,59
First, only 8 of 19 children with SNHL had confirmed VH. This contributed to the wide 95% CIs for diagnostic values and likelihood ratios. The low number of subjects may have also contributed to the low diagnostic capacities of the Bucket Test and condition 4 of the MCTSIB. More subjects with confirmed pathology are needed to add to this preliminary data. Second, the reliability of laser SVV in children has not been established. We do not know how development or the presence of a vestibular deficit affects SVV in children. Third, this study can only be generalized to children aged 6 to 12 years with severe to profound SNHL and without other neurologic problems. This battery of tests should be completed on other groups of children with VH.
The best tests to determine whether a child with an otherwise normal neurological system has VH include (1) the HTT, (2) the m-ECVCT fixation removed, (3) the DVA, (4) the MCTSIB, and (5) SOT vestibular ratio. The MDC90 scores should be considered if using the DVA and MCTSIB as outcome tools to detect improvement due to intervention. Tests of utricular function require further study in pediatric populations.
1. Rine RM. Growing evidence for balance and vestibular problems in children. Audiol Med. 2009;99999:1.
2. O'Reilly RC, Morlet T, Nicholas BD, et al. Prevalence of vestibular and balance disorders in children. Otol Neurotol. 2010;31(9):1441–1444.
3. Rine RM, Braswell J, Fisher D, Joyce K, Kalar K, Shaffer M. Improvement of motor development and postural control following intervention in children with sensorineural hearing loss and vestibular impairment. Int J Pediatr Otorhinolaryngol. 2004;68(9):1141–1148.
4. Rine RM, Spielholz NI, Buchman C. Postural control in children with sensorineural hearing loss and vestibular hypofunction: deficits in sensory system effectiveness and vestibulospinal function. In: Duysens j, Smits-Engelsman BCM, Kingma H, eds. Control of Posture and Gait. Amsterdam, the Netherlands: Springer-Verlag; 2001:40–45.
5. Inoue A, Iwasaki S, Ushio M, et al. Effect of vestibular dysfunction on the development of gross motor function in children with profound hearing loss. Audiol Neurootol. 2013;18(3):143–151.
6. Shall MS. The importance of saccular function to motor development in children with hearing impairments. Int J Otolaryngol. 2009;2009:1–5.
7. Braswell J, Rine RM. Evidence that vestibular hypofunction affects reading acuity in children. Int J Pediatr Otorhinolaryngol. 2006;70:1957–1965.
8. Kaga K. Vestibular compensation in infants and children with congenital and acquired vestibular loss in both ears. Otorhinolaryngology. 1999;49:215–224.
9. Rine RM, Cornwall G, Gan K, et al. Evidence of progressive delay of motor development in children with sensorineural hearing loss and concurrent vestibular dysfunction. Percept Mot Skills. 2000;90:1101–1112.
10. Hlavacka F, Mergner T, Krizkova M. Control of the body vertical by vestibular and proprioceptive inputs. Brain Res Bull. 1999;40(5/6):431–435.
11. Franco ES, Panboca I. Vestibular function in children underperforming in school. Braz J Otorhinolaryngol. 2008;74(6):815–825.
12. Casselbrant ML, Mandel EM, Sparto PJ, et al. Longitudinal posturography and rotational testing in children three to nine years of age: normative data. Otolaryngol Head Neck Surg. 2010;142(5):708–714.
13. Rine RM, Wiener-Vacher S. Evaluation and treatment of vestibular dysfunction in children. NeuroRehabilitation. 2013;32(3):507–518.
14. Saka N, Imai T, Seo T, et al. Analysis of benign paroxysmal positional nystagmus in children. Int J Pediatr Otorhinolaryngol. 2013;77(2):233–236.
15. Monobe H, Murofushi T. Vestibular neuritis in a child with otitis media with effusion; clinical application of vestibular evoked myogenic potential by bond-conducted sound. Int J Pediatr Otorhinolaryngol. 2004;68:1455–1458.
16. Zannolli R, Zazzi M, Muraca MC, Macucci F, Buoni S, Nuti D. A child with vestibular neuritis. Is adenovirus implicated? Brain Dev. 2006;28(6):410–412.
17. Casselbrant ML, Villardo RJ, Mandel EM. Balance and otitis media with effusion. Int J Audiol. 2008;47(9):584–589.
18. Contopoulos-Ioannidis DG, Giotis ND, Baliatsa DV, Ioannidis JP. Extended-interval aminoglycoside administration for children: a meta-analysis. Pediatrics. 2004;114(1):e111–e118.
19. Buchman CA, Joy J, Hodges A, Telischi FF, Balkany TJ. Vestibular effects of cochlear implantation. Laryngoscope. 2004;114:1–22.
20. Cushing SL, Papsin BC, Rutka JA, James AL, Blaser SL, Gordon KA. Vestibular end-organ and balance deficits after meningitis and cochlear implantation in children correlate poorly with functional outcome. Otol Neurotol. 2009;30(4):488–495.
21. Cushing SL, Gordon KA, Rutka JA, James AL, Papsin BC. Vestibular end-organ dysfunction in children with sensorineural hearing loss and cochlear implants: an expanded cohort and etiologic assessment. Otol Neurotol. 2013;34(3):422–428.
22. Suarez H, Angeli S, Suarez A, Rosales B, Carrera X, Alonso R. Balance sensory organization in children with profound hearing loss and cochlear implants. Int J Pediatr Otorhinolaryngol. 2007;71(4):629–637.
23. Tribukait A, Brantberg K, Bergenius J. Function of semicircular canals, utricles and saccules in deaf children. Acta Otolaryngol. 2004;124:41–48.
24. Sheykholesami K, Kaga K, Megerian CA, Arnold JE. Vestibular-evoked myogenic potentials in infancy and early childhood. Laryngoscope. 2005;115:1440–1444.
25. Wuyts FL, Furman J, Vanspauwen R, Van de HP. Vestibular function testing. Curr Opin Neurol. 2007;20(1):19–24.
26. Eviatar L, Eviatar A. The normal nystagmic response of infants to caloric and perrotatory stimulation. Laryngoscope. 1979;89:1036–1045.
27. Valente M. Maturational effects of the vestibular system: a study of rotary chair, computerized dynamic posturography, and vestibular evoked myogenic potentials with children. J Am Acad Audiol. 2007;18(6):461–481.
28. Staller SJ, Goin DW, Hildebrandt M. Pediatric vestibular evaluation with harmonic acceleration. Otolaryngol Head Neck Surg. 1986;95(4):471–476.
29. Schubert MC, Tusa RJ, Grine LE, Herdman SJ. Optimizing the sensitivity of the Head Thrust Test for identifying vestibular hypofunction. Phys Ther. 2004;84(2):151–158.
30. Halmagyi GM, Curthoys LS, Cremer PD, et al. The human horizontal vestibulo-ocular reflex in response to high acceleration stimulation before and after unilateral vestibular neurectomy. Exp Brain Res. 1990;81:479–490.
31. Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt T, Strupp M. A bucket of static vestibular function. Neurology. 2009;72(19):1689–1692.
32. Hall CD, Hoover J, Jacobs M, et al. A new measurement tool for vestibular hypofunction: validity of the Emory Clinical Vestibular Chair Test. J Neurol Phys Ther. 2009;33(4):232.
33. Rine RM, Braswell J. A clinical test of Dynamic Visual Acuity for children. Int J Pediatr Otorhinolaryngol. 2003;69(11):1195–1201.
34. Rine RM, Roberts D, Corbin BA, et al. A new portable tool to screen vestibular and visual function: National Institutes of Health Toolbox Initiative. J Rehabil Res Dev. 2012;49(2):209–220.
35. Hall CD, Abbott KN, Lane EC, et al. Measurement of vestibular hypofunction: validity of the Emory Clinical Vestibular Chair Test (ECVCT). J Neurol Phys Ther. 2007;31(4):210–211.
36. Evans MK, Krebs DE. Posturography does not test vestibulospinal function. Otolaryngol Head Neck Surg. 1999;120(2):164–173.
37. Gabriel LS, Mu K. Computerized platform posturography for children: test-retest reliability of the sensory test of the VSR System. Phys Occup Ther Pediatr. 2002;22(3/4):101–117.
38. Rine RM, Rubish K, Feeney C. Measurement of sensory system effectiveness and maturational changes in postural control in young children. Pediatr Phys Ther. 1998;10:16–22.
39. Shumway-Cook A, Horak FB. Assessing the influence of sensory interaction on balance. Phys Ther. 1986;66:1548–1550.
40. Horak FB. Clinical measurement of postural control in adults. Phys Ther. 1987;67(12):1881–1885.
41. Cohen H, Blatchly CA, Gombash LL. A study of the clinical test of sensory interaction and balance. Phys Ther. 1993;73(6):346–351.
42. Crowe TK, Deitz JC, Richardson PK, Atwater SW. Interrater reliability of the pediatric clinical test of sensory interaction for balance. Phys Occup Ther Pediatr. 1990;10(4):1–27.
43. Westcott SL, Lowes L, Richardson PK. Evaluation of postural stability in children: current theories and assessment tools. Phys Ther. 1997;77(6):629–645.
44. Wrisley DM, Whitney SL. The effect of foot position on the modified clinical test of sensory interaction and balance. Arch Phys Med Rehabil. 2004;85(2):335–338.
45. Weber PC, Cass SP. Clinical assessment of postural stability. Am J Otol. 1993;14(6):566–569.
46. El-Kashlan HK, Shepard NT, Asher AM, Smith-Wheelock M, Telian S. Evaluation of clinical measures of equilibrium. Laryngoscope. 1998;108(March):311–319.
47. Enbom H, Magnusson M, Pyyko I. Postural compensation in children with congenital or early acquired bilateral vestibular loss. Ann Otol Rhinol Laryngol. 1991;100:472–478.
48. Charpiot A, Tringali S, Iionescu E, Vital-Durand F, Ferber-Viart C. Vestibulo-ocular reflex and balance maturation in healthy children aged from six to twelve years. Audiol Neurootol. 2010;15(4):203–210.
49. Akin FW, Murnane OD, Panus PC, Caruthers SK, Wilkinson AE, Proffitt TM. The influence of voluntary tonic EMG level on the vestibular-evoked myogenic potential. J Rehabil Res Dev. 2004;41(3B):473–480.
50. Halmagyi GM, Curthoys IS. Clinical testing of otolith function. Ann N Y Acad Sci. 1999;871:195–204.
51. McNerney KM, Burkard RF. The vestibular evoked myogenic potential (VEMP): air- versus bone-conducted stimuli. Ear Hear. 2011;32(6):e6–e15.
52. Zhou G, Kenna MA, Stevens K, Licamelli G. Assessment of saccular function in children with sensorineural hearing loss. Arch Otolaryngol Head Neck Surg. 2009;135(1):40–44.
53. Bohmer A, Mast F. Assessing otolith function by the subjective visual vertical. Ann N Y Acad Sci. 1999;871:221–231.
54. Agresti A. Categorical Data Analysis. 2nd ed. Hoboken, NJ: Wiley; 2002.
55. Simel DL, Samsa GP, Matchar DB. Likelihood ratios with confidence: sample size estimation for diagnostic test studies. J Clin Epidemiol. 1991;44(8):763–770.
56. Rousson V, Gasser T, Seifert B. Assessing intrarater, interrater and test-retest reliability of continuous measurements. Stat Med. 2002;21(22):3431–3446.
57. Haley SM, Fragala-Pinkham MA. Interpreting change scores of tests and measures used in physical therapy. Phys Ther. 2006;86(5):735–743.
58. Gagnon I, Swaine B, Forget R. Exploring the comparability of the Sensory Organization Test and the Pediatric Clinical Test of Sensory Interaction for Balance in children. Phys Occup Ther Pediatr. 2006;26(1/2):23–41.
59. Braswell J, Rine RM. Preliminary evidence of improved gaze stability following exercise in two children with vestibular hypofunction. Int J Pediatr Otorhinolaryngol. 2006;70:1967–1973.
60. Hafstrom A, Fransson PA, Karlberg M, Magnusson M. Subjective visual tilt and lateral instability after vestibular deafferentation. Acta Otolaryngol. 2006;126(11):1176–1181.
61. Clarke AH, Schonfeld U, Helling K. Unilateral examination of utricle and saccule function. J Vestib Res. 2003;13(4–6):215–225.
62. Bohmer A. The subjective visual vertical as a clinical parameter for acute and chronic vestibular (otolith) disorders. Acta Otolaryngol. 1999;119:126–127.
63. Iwasaki S, Smulders YE, Burgess AM, et al. Ocular vestibular evoked myogenic potentials in response to bone-conducted vibration of the midline forehead at Fz. A new indicator of unilateral otolithic loss. Audiol Neurootol. 2008;13(6):396–404.
64. Rubin LG, Papsin B. Cochlear implants in children: surgical site infections and prevention and treatment of acute otitis media and meningitis. Pediatrics. 2010;126(2):381–391.
65. James AL, Papsin BC. Cochlear implant surgery at 12 months of age or younger. Laryngoscope. 2004;114(12):2191–2195.
66. Basta D, Todt I, Goepel F, Ernst A. Loss of saccular function after cochlear implantation: the diagnostic impact of intracochlear electrically elicited vestibular evoked myogenic potentials. Audiol Neurootol. 2008;13(3):187–192.
67. Tien HC, Linthicum FH Jr. Histopathologic changes in the vestibule after cochlear implantation. Otolaryngol Head Neck Surg. 2002;127(4):260–264.
68. Ribari O, Kustel M, Szirmai A, Repassy G. Cochlear implantation influences contralateral hearing and vestibular responsiveness. Acta Otolaryngol. 1999;119(2):225–228.
69. Bonucci AS, Costa Filho OA, Mariotto LD, Amantini RC, Alvarenga KF. Vestibular function in cochlear implant users. Braz J Otorhinolaryngol. 2008;74(2):273–278.
70. Fife TD, Tusa RJ, Furman JM, et al. Assessment: vestibular testing techniques in adults and children: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology. 2000;55:1431–1441.
71. Ferber-Viart C, Onescu E, Orlet T, Roehlich P, Ubreuil C. Balance in healthy individuals assessed with Equitest: maturation and normative data for children and young adults. Int J Pediatr Otorhinolaryngol. 2007;71(7):1041–1046.
child; diagnostic tests/standards; postural balance; reproducibility of results; ROC curves; sensitivity and specificity; sensorineural hearing loss; vestibular function tests
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