Subjective Visual Vertical Testing in Children and Adolescents

Transcription

1 The Laryngoscope VC 2015 The American Laryngological, Rhinological and Otological Society, Inc. Subjective Visual Vertical Testing in Children and Adolescents Jacob R. Brodsky, MD; Brandon A. Cusick, MBA, BBA; Margaret A. Kenna, MD, MPH; Guangwei Zhou, ScD Objectives/Hypothesis: Subjective visual vertical (SVV) is a vestibular test commonly used in adults that has not been well studied in children. In this test, the patient aligns a projected line with the perceived true vertical. Deviation of >28 is usually associated with utricular dysfunction and may also be seen with central vestibular lesions. The goal of this study was to determine the efficacy of SVV in children. Study Design: Prospective, controlled study. Methods: Thirty-three children aged 7 to 18 years with (n 5 21) and without (n 5 12) dizziness underwent static SVV. History, exam, rotary chair, and caloric testing were used to categorize subjects with dizziness into groups with peripheral vestibular loss (PVL), benign paroxysmal positioning vertigo (BPPV), central vertigo (CV), and nonvestibular dizziness (NVD). Results: Mean SVV deviation was significantly higher in the peripheral vestibular loss group (n 5 4; ) compared to BPPV (n 5 5; ), CV (n 5 7; ), NVD (n 5 5; ), and control (n 5 12; ) groups by one-way analysis of variance (P 5.002). SVV deviation >28 demonstrated a sensitivity of 100%, specificity of 75%, positive predictive value of 100%, and negative predictive value of 97% for PVL. Conclusions: SVV is a simple, noninvasive test that provides a valuable contribution to the assessment of peripheral vestibular function in children. Key Words: Subjective visual vertical, utricle, pediatric vestibular testing, vestibular neuritis. Level of Evidence: 3b Laryngoscope, 126: , 2016 From the Department of Otolaryngology and Communication Enhancement (J.R.B., B.A.C., M.A.K., G.Z.), Boston Children s Hospital, Boston, Massachusetts; and the Department of Otology and Laryngology (J.R.B., M.A.K., G.Z.), Harvard Medical School, Boston, Massachusetts, U.S.A. Editor s Note: This Manuscript was accepted for publication April 23, Presented at the Eastern Section of the Triological Society Combined Sections Meeting, Coronado, California, U.S.A., January 24, All financial support for this study was provided by the Department of Otolaryngology and Communication Enhancement at Boston Children s Hospital. The authors have no other funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Jacob R. Brodsky, MD, Department of Otolaryngology and Communication Enhancement, 300 Longwood Avenue, Boston, MA jacob.brodsky@childrens.harvard.edu DOI: /lary INTRODUCTION The vestibular labyrinth is comprised of three semicircular canals, which respond to rotational acceleration, and two otolith organs, the saccule and utricle, which respond primarily to linear acceleration. Objective clinical tests of vestibular end-organ function have been well established for the lateral semicircular canal (rotary chair and caloric tests) 1 and the saccule (cervical vestibular evoked myogenic potential test), 1 4 but options for testing the function of the other vestibular end organs are limited. The subjective visual vertical (SVV) test has been shown to be a useful test for unilateral peripheral vestibular impairment involving the utricle Acute injuries to central vestibular pathways can also affect SVV. 15,16 The SVV test requires patients to rotate a projected straight line until it is aligned with their perception of the true vertical. Numerous adult studies have shown SVV deviation >28 in patients with vestibular pathology. 6,11,17,18 The SVV test can be performed as a static test or as a dynamic test with off-axis rotation, with the latter showing increased sensitivity for detecting utricular impairment. 5,12,14 18 Variations of SVV also include a moving visual field 19,20 or tilting of the head or body. 5,6,23 The static SVV test does not involve rotation or stimulation of vertigo, which in our experience can sometimes be anxiety-provoking factors that limit the use of other vestibular tests, such as the rotary chair and caloric tests, in children. Objective vestibular testing plays a particularly important role in the evaluation of dizziness in the pediatric population, where the history and examination are often limited, and the differential diagnosis is extensive. 24 Vestibular tests that have been validated in adults require separate validation in children due to the varying maturity of the pediatric vestibular system. 25 The SVV test has not been studied in children with vestibular dysfunction. The objective of this study was to evaluate the efficacy of the static SVV test in identifying children with peripheral vestibular pathology. MATERIALS AND METHODS Patients Enrolled subjects consisted of 21 patients presenting to a pediatric vestibular clinic for evaluation of dizziness and 12 control patients presenting to a general pediatric otolaryngology clinic for evaluation of nonotologic problems (e.g., sinusitis, 727

2 TABLE I. Patient Diagnoses by Category. Category Diagnosis No. PVL, n 5 4 (12%) Vestibular neuritis 3 Labyrinthine concussion 1 BPPV, n 5 5 (15%) Unilateral posterior canal BPPV 5 CV, n 5 7 (21%) Postconcussion syndrome 4 Vestibular migraine 2 Chiari malformation 1 NVD, n 5 5 (15%) CSD 2 Chronic sinusitis 1 Hypothyroidism 1 Postural orthostatic tachycardia 1 Control, n 5 12 (36%) BPPV 5 benign paroxysmal positioning vertigo; CSD 5 chronic subjective dizziness; CV 5 central vertigo; NVD 5 non-vestibular dizziness; PVL 5 peripheral vestibular loss. tonsillitis) without any history of dizziness or balance impairment. Patients with a history of chronic middle ear disease, ear surgery, or brain surgery were excluded. All subjects were 18 years of age or younger at the time of testing. All subjects underwent a comprehensive otologic and neurologic examination by a pediatric otolaryngologist (J.R.B.) as part of their routine evaluation for their presenting complaint. Written consent was obtained from the subjects parents, and verbal assent was obtained from subjects who were <18 years of age at the time of study enrollment. Written consent was obtained directly from the two subjects who were 18 years of age at the time of study enrollment. All vestibular tests, including SVV, were conducted by a licensed audiologist (G.Z.) with the aid of a trained assistant. All subjects were given a gift card to an online media store as a token of appreciation for participation. This study was approved by the institutional review board at Boston Children s Hospital. Subjective Visual Vertical Testing All subjects underwent static SVV testing using the Micromedical System 2000 (Micromedical Technologies, Chatham, IL). Subjects were secured in a chair in a cylindrical enclosure in darkness. A laser line was projected onto the wall of the enclosure in front of the subject at a distance of approximately 1 m. The subject was then instructed to orient the line to their perceived vertical using a remote control device. Deviation of the calculated perceived vertical from the true vertical was recorded in degrees, with positive and negative values denoting rightward and leftward deviation, respectively. Additional Vestibular Testing Nineteen subjects in the dizziness group also underwent rotary chair testing (n 5 15) or bithermal water caloric testing (n 5 4) as part of their routine clinical vestibular evaluation. The rotary chair test was also performed with the Micromedical System 2000 and caloric testing was performed using the Micromedical VisualEyes with Aqua Stim system. Abnormal results were determined using manufacturer-supplied age-adjusted normative data ranges. Rotary chair testing was performed in a cylindrical enclosure in darkness using multifrequency sinusoidal harmonic acceleration. Rotary chair results were considered abnormal if gain values for all frequencies tested were below the age-adjusted normal range, the phase lead values for the lowest three frequencies tested were above the age-adjusted normal range, and the time constant was <12 seconds. Caloric testing was considered abnormal if the reduced vestibular response score was >20%. Diagnosis Categorization Subjects with dizziness were categorized by their primary diagnosis, which was determined by clinical history, examination, and testing results. Subjects with abnormal rotary chair or caloric testing results along with a history and examination consistent with an acute peripheral vestibular impairment were designated as the peripheral vestibular loss (PVL) group. The remaining subjects were categorized as having benign paroxysmal positioning vertigo (BPPV), central vertigo (CV), or nonvestibular dizziness (NVD). BPPV subjects were diagnosed by the presence of geotropic, torsional nystagmus during the Dix- Hallpike maneuver. CV and NVD were determined by the presence of findings on history, examination, and testing that were consistent with a neurologic vestibular disorder or a nonvestibular disorder, respectively, as the cause of the subject s dizziness. No subjects outside of the PVL group had abnormal rotary chair or caloric test findings, and no subjects outside of the BPPV group had abnormal Dix-Hallpike maneuver findings. Data Analysis The Statistical Program for Social Sciences (SPSS version 19; IBM, Armonk, NY) was used to perform statistical analyses. Absolute values of SVV scores were used. Power analysis (power ; a 5.05) using predicted mean SVV scores of standard deviation (SD) of 0.9 for non-pvl groups and 3.3 for the PVL group (2.5 SD above predicted non-pvl mean), based on a study of static SVV in 30 healthy adults, 24 yielded a projected sample size of four subjects per diagnosis group. Mean SVV scores for the PVL, BPPV, CV, NVD, and control groups were compared by one-way analysis of variance (ANOVA) with Tukey post hoc analysis of multiple comparisons. Effects of age and gender were assessed by multiple regression analysis. The BPPV, CV, NVD, and control groups were then combined and compared to the PVL group using cross-tab analysis to determine the sensitivity, specificity, positive predictive value (PPV), negative predictive value (NPV), and negative likelihood ratio of static SVV for detecting evidence of peripheral vestibular loss. Anecdotally, we have found children to vary in their ability to maintain focus consistently throughout the testing session. To account for this, we have used the approach of eliminating the two scores farthest from zero out of five consecutive trials performed by each subject prior to calculating individual mean SVV scores. RESULTS Twenty-one subjects with dizziness and 12 control subjects participated in the study. Subjects ranged in age from 7 to 18 years (mean SD). There were 22 girls and 11 boys. All participating children were able to complete the static SVV test without difficulty. Diagnosis Categories The breakdown of subjects into each of the five diagnostic categories and their specific diagnoses are outlined in Table I. Four subjects were categorized in 728

3 therapy. One NVD subject had a known history of hypothyroidism with resolution of dizziness following thyroidstimulating hormone correction by increasing her levothyroxine dose. One NVD subject had signs and symptoms of postural orthostatic tachycardia syndrome and resolution of dizziness with a combination of fludrocortisone and increased hydration. Fig. 1. Distribution of individual subjects mean SVV scores by diagnosis group. BPPV 5 benign paroxysmal positioning vertigo; CV 5 central vertigo; NVD 5 non-vestibular dizziness; PVL 5 peripheral vestibular loss; SVV 5 subjective visual vertical the PVL group based on the presence of either abnormal rotary chair (n 5 3) or caloric (n 5 1) testing results. Three PVL subjects showed symptoms and signs of acute vestibular neuritis (VN). The fourth PVL subject demonstrated abnormal rotary chair testing following an acute head injury without temporal bone fracture on computed tomography and with a normal neurological examination consistent with a labyrinthine concussion. Five subjects had abnormal Dix-Hallpike maneuver findings consistent with unilateral posterior canal BPPV. Rotary chair and caloric testing were performed on one and two BPPV subjects, respectively, all with normal results. Two BPPV subjects did not undergo rotary chair or caloric testing, though these subjects had a clinical history that was consistent with isolated BPPV without other symptoms or signs of an underlying PVL. Diagnosis and treatment of BPPV cases with canal repositioning maneuvers always occurred during a subject s office visit, which was prior to their vestibular test battery session, including SVV testing, in all cases. Four of the seven subjects in the CV group had onset of dizziness following a recent concussion with symptoms extending beyond 4 weeks postinjury consistent with a diagnosis of post-concussion syndrome. Two CV group subjects met criteria for vestibular migraine, as defined by the International Classification of Headache Disorders. 21 One CV group subject had evidence of a prominent Chiari I malformation on brain magnetic resonance imaging (MRI), and had downbeat nystagmus and exacerbation of symptoms in the supine, headhanging position. Three of the five subjects in the NVD group were diagnosed with chronic subjective dizziness, based on criteria outlined by Ruckenstein and Staab. 22 One NVD subject had symptoms of chronic sinusitis concurrent with dizziness onset and evidence of sinusitis on MRI, with complete resolution of dizziness on antibiotic SVV Scores Distribution of individual SVV scores by diagnosis group is represented in Figure 1. Mean SVV score was significantly higher in the PVL group (n 5 4; ) compared to the BPPV (n 5 5; ), CV (n 5 7; ), NVD (n 5 5; ), and control (n 5 12; ; P 5.004) groups by one-way ANOVA (P 5.002) and multiple comparison test (P <.05) comparing PVL with all other groups. There was no significant difference in mean SVV scores between the control group and the BPPV (P 5.970), CV (P 5.965), and NVD (P ) groups, respectively. Multiple regression analysis showed no statistically significant effects of age (P 5.92) or gender (P 5.38) on SVV score. SVV score >28 demonstrated a sensitivity of 100%, specificity of 75%, PPV of 100%, NPV of 97%, and a negative likelihood ratio of 0.25 for detecting a peripheral vestibular loss. The approach of using the best three of five trials to calculate each subject s SVV score produced the highest sensitivity, specificity, PPV, and NPV for detecting PVL out of all other possible combinations of one to five trials (e.g., best, worst, first, last, median). Multiple comparisons test comparing the PVL group to all other diagnosis groups was statistically significant (P <.05) when the best three trials were used, but not when all five trials were used. DISCUSSION This study provides evidence supporting the usefulness of the static SVV test as a tool for differentiating children with peripheral vestibular loss from children with other etiologies of dizziness and from healthy controls. This is a particularly beneficial vestibular test for children, because it does not involve rotation or stimulation of vertigo. The simplicity of this test has also resulted in versions that do not require large, expensive equipment. A version using a bucket and a protractor has shown comparable efficacy to traditional SVV methods in adults. 26,27 A smartphone application version of the SVV test has also been developed (Visual Vertical; Clear Health Media, Wonga Park, Australia), though its efficacy has not yet been demonstrated in children or adults. SVV deviation has been primarily localized to the utricle, based on adult studies demonstrating consistent ipsilateral SVV deviation in the presence of acquired, peripheral vestibular losses that typically affect the superior vestibular nerve (e.g., vestibular neuritis, vestibular schwannoma, vestibular nerve section). 3 5,17,28 30 This finding is particularly helpful in confirming suspected cases of vestibular neuritis in adults, where cervical vestibular-evoked myogenic potential testing is often normal due to sparing of the inferior vestibular nerve. 729

4 Patients with SVV deviation consistently demonstrate a tonic ipsilateral torsional deviation of eye position (ocular tilt reaction), which is a phenomenon that has been localized to the utricle, thus providing indirect evidence for an association between SVV deviation and utricular dysfunction. 4,5,15,16,18,31 The reflex pathways for the ocular tilt reaction pass through the brainstem and are modulated at the cortical level, so an acute injury (e.g., stroke) affecting the tegmental brainstem, posterolateral thalamus, or parietoinsular vestibular cortex can also cause temporary SVV deviation. 15,16 Such injuries are fortunately rare in children. None of the CV group subjects in our study had abnormal SVV scores. This is probably because all of these subjects had either chronic (postconcussive syndrome and Chiari malformation) or episodic (vestibular migraine) central vestibular disorders. Dynamic SVV testing, which incorporates eccentric rotation around the yaw axis, has shown increased sensitivity over the static SVV test for detecting peripheral vestibular loss. 12,14,23,28,32,33 Dynamic SVV testing has been successfully performed on children in our clinical laboratory, though a prospective, controlled study of this technique in the pediatric population has not yet been completed. Despite its improved sensitivity, dynamic SVV does not lend itself to simple bedside techniques, such as the bucket and smartphone versions of the static SVV test described above. Dynamic SVV also does not provide the advantage of avoiding rotation. The generally accepted normal range of SVV deviation for adults is 28 or less. 6,11,17,18 Our data demonstrate this range to also be appropriate for children. A recent study of the static SVV test in healthy 6- to 8- year-old children without vestibular pathology demonstrated high variability in accurate determination of SVV compared to young adults >18 years of age. 19 Multiple cortical sensory integration pathways appear to be involved in SVV testing, some of which may be immature in children. 19,34 We have also anecdotally found children to show variable focus throughout multiple consecutive trials of the static SVV test. Our approach of eliminating each subject s worst two scores out of five trials was helpful in accounting for some of this variability. We found this approach to be the most effective at identifying subjects with PVL compared to various other combinations of one to five trials. No BPPV subjects in our study demonstrated abnormal SVV scores, and the mean SVV score of the BPPV group did not differ from that of the control group. All BPPV subjects were tested after canalith repositioning maneuvers were performed. The findings of adult studies on the effect of BPPV on SVV have been variable, but most show deviations of SVV that normalize after successful canalith repositioning SVV scores in the BPPV and PVL groups may not have differed if SVV occurred prior to repositioning maneuvers. BPPV can occur in 10% to 16% of adults with VN, sometimes in a delayed fashion, which likely occurs by utricular degeneration and otoconial dislodgement. 38,39 No BPPV subjects in our study had evidence of VN, and no VN subjects had evidence of BPPV. 730 A limitation of our study is the small number of subjects of each individual age and in each diagnosis category, which may affect the generalizability of our results. This is primarily a result of the low incidence of acute peripheral vestibulopathies in children. Some of the most common causes of peripheral vestibular loss in adults, such as Menière s disease and vestibular schwannoma, are extremely rare in children. 24 The majority of subjects in the PVL group had VN, which is also less common in the pediatric population. SVV deviations in children with VN in our study were smaller than those reported in studies of static SVV in adults with VN This may be a result of more rapid compensation of vestibular function in children. This may also explain why one PVL subject who was tested 5 months after VN onset had a normal SVV score, whereas all other PVL subjects were tested <2 months from symptom onset. SVV deviation has been shown to normalize within a relatively short period of time following an episode of VN in adults, compared to rotary chair and caloric testing, which generally remain abnormal. 9,12,13 CONCLUSION The static SVV test is a useful method for detecting peripheral vestibular impairment in children and adolescents with acute dizziness (<2 months from symptom onset). A normal range of <28 of deviation is appropriate for use in the pediatric population. Further study is needed to determine if the addition of eccentric rotation to the SVV test increases its sensitivity in children like it does in adults. Validation of bucket and smartphone versions of the static SVV test in children would help to increase the availability and convenience of this test. Acknowledgments The authors thank Kosuke Kawai, Mark Berry, Lin Huang, Korinne Ivey, and Allison Bradley for their assistance with this study. BIBLIOGRAPHY 1. Baloh RW, Kerber KA. Clinical Neurophysiology of the Vestibular System. New York, NY: Oxford University Press; Colebatch JG, Halmagyi GM, Skuse NF. Myogenic potentials generated by a click-evoked vestibulocollic reflex. J Neurol Neurosurg Psychiatry 1994;57: Clarke AH, Schonfeld U, Helling K. Unilateral examination of utricle and saccule function. J Vestib Res 2003;13: Halmagyi GM, Curthoys IS. Clinical testing of otolith function. Ann N Y Acad Sci 1999;871: Bohmer A, Mast F. Assessing otolith function by the subjective visual vertical. Ann N Y Acad Sci 1999;871: Bohmer A, Rickenmann J. The subjective visual vertical as a clinical parameter of vestibular function in peripheral vestibular diseases. J Vestib Res 1995;5: Min KK, Ha JS, Kim MJ, Cho CH, Cha HE, Lee JH. Clinical use of subjective visual horizontal and vertical in patients of unilateral vestibular neuritis. Otol Neurotol 2007;28: Ogawa Y, Otsuka K, Shimizu S, Inagaki T, Kondo T, Suzuki M. Subjective visual vertical perception in patients with vestibular neuritis and sudden sensorineural hearing loss. J Vestib Res 2012;22: Park H, Shin J, Jeong Y, Kwak H, Lee Y. Lessons from follow-up examinations in patients with vestibular neuritis: how to interpret findings from vestibular function tests at a compensated stage. Otol Neurotol 2009; 30: Toupet M, Van Nechel C, Bozorg Grayeli A. Influence of body laterality on recovery from subjective visual vertical tilt after vestibular neuritis. Audiol Neurootol 2014;19: Vibert D, Hausler R, Safran AB. Subjective visual vertical in peripheral unilateral vestibular diseases. J Vestib Res 1999; 9:

5 12. Byun JY, Hong SM, Yeo SG, Kim SH, Kim SW, Park MS. Role of subjective visual vertical test during eccentric rotation in the recovery phase of vestibular neuritis. Auris Nasus Larynx 2010;37: Kim HA, Hong JH, Lee H, et al. Otolith dysfunction in vestibular neuritis: recovery pattern and a predictor of symptom recovery. Neurology 2008; 70: Hong SM, Yeo SG, Byun JY, Park MS, Park CH, Lee JH. Subjective visual vertical during eccentric rotation in patients with vestibular neuritis. Eur Arch Otorhinolaryngol 2010;267: Brandt T, Dieterich M. Cyclorotation of the eyes and subjective visual vertical in vestibular brain stem lesions. Ann N Y Acad Sci 1992;656: Yang TH, Oh SY, Kwak K, Lee JM, Shin BS, Jeong SK. Topology of brainstem lesions associated with subjective visual vertical tilt. Neurology 2014;82: Bohmer A, Mast F, Jarchow T. Can a unilateral loss of otolithic function be clinically detected by assessment of the subjective visual vertical? Brain Res Bull 1996;40: ; discussion Dieterich M, Brandt T. Ocular torsion and tilt of subjective visual vertical are sensitive brainstem signs. Ann Neurol 1993;33: Gaertner C, Bucci MP, Obeid R, Wiener-Vacher S. Subjective visual vertical and postural performance in healthy children. PLoS One 2013;8: e Dichgans J, Held R, Young LR, Brandt T. Moving visual scenes influence the apparent direction of gravity. Science 1972;178: The International Classification of Headache Disorders, 3rd edition (beta version). Cephalalgia 2013;33: Ruckenstein MJ, Staab JP. Chronic subjective dizziness. Otolaryngol Clin North Am 2009;42:71 77, ix. 23. Schonfeld U, Clarke AH. A clinical study of the subjective visual vertical during unilateral centrifugation and static tilt. Acta Otolaryngol 2011; 131: O Reilly RC, Greywoode J, Morlet T, et al. Comprehensive vestibular and balance testing in the dizzy pediatric population. Otolaryngol Head Neck Surg 2011;144: O Reilly R, Grindle C, Zwicky EF, Morlet T. Development of the vestibular system and balance function: differential diagnosis in the pediatric population. Otolaryngol Clin North Am 2011;44: Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt T, Strupp M. A bucket of static vestibular function. Neurology 2009;72: Cohen HS, Sangi-Haghpeykar H. Subjective visual vertical in vestibular disorders measured with the bucket test. Acta Otolaryngol 2012;132: Bohmer A, Mast F. Chronic unilateral loss of otolith function revealed by the subjective visual vertical during off center yaw rotation. J Vestib Res 1999;9: Schonfeld U, Helling K, Clarke AH. Evidence of unilateral isolated utricular hypofunction. Acta Otolaryngol 2010;130: Curthoys IS, Burgess AM, MacDougall HG, et al. Testing human otolith function using bone-conducted vibration. Ann N Y Acad Sci 2009;1164: Diamond SG, Markham CH. Ocular counterrolling as an indicator of vestibular otolith function. Neurology 1983;33: Faralli M, Ricci G, Molini E, Longari F, Altissimi G, Frenguelli A. Determining subjective visual vertical: dynamic versus static testing. Otol Neurotol 2007;28: Vingerhoets RA, Van Gisbergen JA, Medendorp WP. Verticality perception during off-vertical axis rotation. J Neurophysiol 2007;97: Lopez C, Mercier MR, Halje P, Blanke O. Spatiotemporal dynamics of visual vertical judgments: early and late brain mechanisms as revealed by high-density electrical neuroimaging. Neuroscience 2011;181: Angeli SI, Abouyared M, Snapp H, Jethanamest D. Utricular Dysfunction in Refractory Benign Paroxysmal Positional Vertigo. Otolaryngol Head Neck Surg 2014;151: Faralli M, Manzari L, Panichi R, et al. Subjective visual vertical before and after treatment of a BPPV episode. Auris Nasus Larynx 2011;38: von Brevern M, Schmidt T, Schonfeld U, Lempert T, Clarke AH. Utricular dysfunction in patients with benign paroxysmal positional vertigo. Otol Neurotol 2006;27: Balatsouras DG, Koukoutsis G, Ganelis P, et al. Benign paroxysmal positional vertigo secondary to vestibular neuritis. Eur Arch Otorhinolaryngol 2014;271: Mandala M, Santoro GP, Awrey J, Nuti D. Vestibular neuritis: recurrence and incidence of secondary benign paroxysmal positional vertigo. Acta Otolaryngol 2010;130: