Egyptian Journal of Ear, Nose, Throat and Allied Sciences 18 (2017) 223–225

Contents lists available at ScienceDirect

Egyptian Journal of Ear, Nose, Throat and Allied Sciences

journal homepage: www.ejentas.com

Audiology Study of the relationship between cVEMP and ABR 500 Hz ⇑ Amani Mohamed El-Gharib , Trandil Hassan Elmahallawy

Audiology Unit, Department of ENT, Tanta Faculty of Medicine, Tanta University, Egypt article info abstract

Article history: Objective: To evaluate the possible contribution of the saccular projections in generation ABR 500 Hz at Received 8 February 2017 high intensity by investigating the relationship between cVEMP and ABR 500 Hz in normal subjects and Accepted 21 July 2017 those with unilateral saccular dysfunction. Available online 19 December 2017 Subjects: Twenty dizzy adults with unilateral affected cVEMP compared to twenty healthy subjects. Methods: All subjects were subjected to basic audiological evaluation (pure tone audiometry, speech Keywords: audiometry and immittancemetry), cVEMP and ABR using 500 Hz tone burst at 90 dB nHL. The dizzy cVEMP patients within the study group were subjected to VNG to exclude another vestibular affection. ABR 500 Hz The results: We found that patient’s abnormal cVEMPs response mostly had prolonged ABR 500 Hz wave Saccular dysfunction Dizziness V latency, whereas unaffected ears presented with normal findings. Conclusion: Using ABR 500 Hz in the battery approach tests of vestibular assessment can produce valu- able data for judgment on the site of a lesion. Ó 2017 Egyptian Society of Ear, Nose, Throat and Allied Sciences. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc- nd/4.0/).

1. Introduction at cells situated between the dorsal and posteroventral .7 The human vestibule has preserved an ancestral sound sensitiv- cVEMPs is evoked by a loud stimuli which may activate the main ity and so-called vestibular .1 The pattern of hypersensitiv- portion of the auditory brain, temporal gyrus and thus, called the ity of the to sound stimulation is consistent with vestibular sensitivity to sound.8 It provides a means of assessing sac- the clinical sign known as Tullio phenomenon, which was first cular function, which is elicited by the sound of low frequency and described by Pietro Tullio; as the generation of vestibular symp- loud intensity within the range (100–1000 Hz) of human hearing.9 toms during exposure to high-intensity sound.2 The continuous cVEMP testing may provide a useful and be noninvasive method observations led researchers to propose human’s as the for the assessment of saccular function as well as the functional end organ activated by sound.3 integrity of the inferior . Sound evoked cVEMP Cervical vestibular evoked myogenic potentials (cVEMPs) are a recorded from the neck are claimed to be almost completely uni- biphasic response positive-negative component with one or two lateral. But, it has its limitation in patients with neck muscle dis- latter components recorded from tonically contracted muscle (for eases, Mythania gravis, and cervical spondylosis and in example, sternomastoid, trapezius or splenius capitis) in response uncooperative patients. to loud sounds.4 Current data suggest that the cVEMPs is a In this work our objective is to investigate the possibility that vestibulo-collic reflex in and is almost entirely saccular in origin.5 the saccular projections may contribute to high intensity ABR According to Oh et al. cVEMP is mediated by the vestibular 500 Hz which generated from the central auditory pathway up to nuclei and uncrossed medial descending in the level of . The previous done by investigating the lower brainstem and .6 the relationship between cVEMP and ABR 500 Hz in normal sub- The saccular projections and the inferior branch of the vestibu- jects and those with unilateral saccular dysfunction. lar nerve run also, into the cochlear nucleus. These axons travel caudally through the descending vestibular nucleus, enter the 2. Subjects and methods cochlear nucleus at a level caudal to the subgroup y, and terminate 2.1. Subjects Peer review under responsibility of Egyptian Society of Ear, Nose, Throat and Allied Sciences. ⇑ Corresponding author. This case-control study involved twenty healthy volunteers as a E-mail address: [email protected] (A.M. El-Gharib). control group (CG) their age range 20–36 years and twenty https://doi.org/10.1016/j.ejenta.2017.07.001 2090-0740/Ó 2017 Egyptian Society of Ear, Nose, Throat and Allied Sciences. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 224 A.M. El-Gharib, T.H. Elmahallawy / Egyptian Journal of Ear, Nose, Throat and Allied Sciences 18 (2017) 223–225 selected cases with affected cervical VEMP as a study group (SG) presented at 95 dB nHL with alternating polarity, rate 5 Hz. their age range 31–41 years. All cases were presented to Audiology Affected cVEMPs was considered by prolonged latencies or unit, faculty of medicine, Tanta University hospital between: May absent waves P13 or N23. 2014 to April 2015. All SG was selected from patient complain of iv. ABR 500 Hz: elicited by SMART EPs of Intelligent hearing sys- dizziness. The inclusion criteria for the case group included tem using ER3A insert phone (IHS, Miami, USA). 500 Hz patients presented with normal peripheral hearing, normal middle tone-burst ABR (ABR 500 Hz) was done to all studied groups. ear pressure, normal word discrimination score, normal caloric test For ABR, the patients were placed in the supine position. results and unilateral affected cVEMP. Affected cVEMP was consid- Non-inverting electrode was placed on the high forehead ered by significant prolonged latencies or absent P13 or n23. and inverting electrode on ipsilateral mastoid and the The exclusion criteria: history of ear infections, cervical verte- ground electrode on the contralateral mastoid. Responses bral diseases, neurological degenerative disease, middle ear dis- to 2000 stimuli were averaged (rate of 37/s, filtered from eases, which can interfere with cVEMPs measurements and 30 to 3000 Hz, 500 Hz tone burst (R/F time 1 ms and plateau hearing loss. 2 ms), 120 dBSPL; contralateral noise = 90 dBSPL, the win- dow of 25 ms). 2.2. Methods v. Click ABR at 90 dB routinely done to exclude retro cochlear lesion or any dyssynchronization in nerve response. All subjects were subjected to the following: All patients were thoroughly counseled about the procedure, i. Basic audiological evaluation: by standard pure tone audiom- stating the values, the hazards and the aim of the study. A written etry GSI version 61 audiometer (Viasys USA) Flow Sensor for consent was obtained and signed by each participant. VIASYS AVEA Ventilator, New, Original) for pure tone Statistical analysis of the present study was conducted using audiometry using headphone TDH 39, acoustic immitance SPSS V.16. measurements (tympanometry/stapedial reflex) by intera- coustics AT235H impedance using low frequency 226 Hz 3. Results probe tone (Middelfart, Denmark). Pure tone audiometry was done and comparison between the right and left ear All subjects in CG and SG showed normal peripheral hearing in threshold was performed. the frequency range 0.25–8 kHz of the audiogram. For CG their ii. Videonystagmography test (VNG): using CHART ICS was done mean age 30.09 ± 7.84 years while, for SG their mean age 36.35 ± in order to eliminate the possibility of additional vestibular 14.84. pathology. All patients are selected to have normal VNG test cVEMP was recorded for all subjects from the control group results. (CG) while it was recorded with prolonged latencies in (SG) and iii. cVEMP: elicited by Smart EPs of Intelligent hearing system absent unilaterally in 3 ears of the them. The mean and standard using ER3A insert phone (IHS, Miami, USA). deviation of P13 and n23 latency and amplitude for both groups cVEMPs was conducted from sternocleidomastoid muscle. are presented in Table 1. The affected ear refers to the ear with During cVEMPs (air-conducted) recording, patients were affected cVEMP; while the unaffected ear refers to the ear con- instructed to turn and hold their heads as much as possible tralateral to the lesion in the study group (SG). toward the side contralateral to the stimulated ear. At that ABR 500 Hz wave V was recorded in the two studied groups point, patients were asked to maintain a contraction monaurally with the mean and standard deviation presented in throughout the test session. Electrode montage: Active elec- (Table 1). The comparison between ABR 500 Hz latency and ampli- trode was on the second half of sternocleidomastoid on one tude of wave V between the affected ear, the unaffected ear and a side, reference electrode was on the middle of the anterior control group are presented in (Table 1). This revealed significant surface of clavicle while the ground electrode was over fore- difference only in the ABR latency, but not in the amplitude head. The electro myography (EMG) was monitored between the three subgroups. Thus Tuckey test was conducted in throughout the test. The parameters used were 200 stimuli order to evaluate the cause of this significant difference. The test

Table 1 The mean and standard deviation of P13 and n23 (cVEMP) latencies and amplitude and ABR 500 Hz latency and amplitude in the studied groups.

Variable Affected ears SG Unaffected ears SG CG p-value Multiple comparison P13 Latency (ms) 18.4 ± 0.24 14.42 ± 2.77 13.22 ± 2.72 0.000** P1 0.000** P2 0.000** P3 0.163 Amplitude (lV) 3.09 ± 2.35 1.40 ± 0.79 1.94 ± 1.35 0.03* P1 0.003* P2 0.024* P3 0.417 n23 Latency (ms) 23.49 ± 2.21 21.04 ± 4.1 19.28 ± 3.1 0.000** P1 0.049* P2 0.000** P3 0.132 Amplitude (lV) 2.55 ± 1.65 2.19 ± 1.22 2.68 ± 1.77 0.549 — ABR Latency (ms) 6.89 ± 0.64 6.13 ± 0.63 5.61 ± 1.37 0.000** P1 0.042* P2 0.000** P3 0.190 Amplitude (lV) 0.19 ± 0.14 0.20 ± 0.16 0.23 ± 0.14 0.748 —

SG: study group. CG: control group. Where p1: comparison between affected ears & unaffected ears SG. P2: comparison between affected ears SG and CG. P3: comparison between unaffected ears SG and CG. A.M. El-Gharib, T.H. Elmahallawy / Egyptian Journal of Ear, Nose, Throat and Allied Sciences 18 (2017) 223–225 225

reported that rounded shape and longer latency of ABR 500 Hz wave V are the evidence for uncertain saccular projections in the brainstem pathway and insecure vestibular hearing. Therefore, safe vestibular hearing is effective for the improvement of the neural synchronization.11 Our results show high sensitivity of ABR 500 Hz in the presence of affected cVEMP and suggest that people with safe vestibular hearing have intact projections to cochlear nucleus, lateral lemnis- cus, and to the inferior colliculus which agreed with10,12 .This high sensitivity of ABR 500 Hz in detecting affected cVEMP suggested an interaction between saccular vestibular function and hearing, which appears in ABR 500 Hz latency. These are in accordance with Xu et al. who suggested that cochlear and saccule occurred in the same embryonic tissue structure is the cause of this interaction.13 Our results agree with Emami who reported that ABR 500 Hz had a predication role in saccular function and that there is a vestibular-auditory interaction. He also recommended the use cVEMP and ABR 500 Hz for the judgment on the site of lesion.14 Finally, we conclude that ABR 500 Hz can suspect vestibular lesion and may detect the site of a lesion; saccular or inferior vestibular nerve deficit especially when cVEMP is difficult to test or contraindicated. However substitution cVEMP test by ABR 500

Fig. 1. ABR traces in normal subjects in response to click stimuli above and to 500 Hz test cannot be accepted especially when there are cochlear Hz tone burst stimuli below. I = Peak of wave I of auditory brainstem response. III = hearing loss affect ABR 500 Hz test results. The low specificity of Peak of wave III of auditory brainstem response. V = Peak of wave V of auditory ABR 500 Hz makes it of limit use when compared to cVEMP. brainstem response.

Declaration of interests

Table 2 Sensitivity and Specificity of ABR 500 Hz in detection affection of cVEMPs. The authors declare no conflicts of interest in this work.

Test Value 95% Confidence interval (CI) Sensitivity 100% 83.16%–100% References Specificity 66.67% 53.31%–78.31% 1. Manzari L, Burgess AM, Curthoys IS. Effect of bone-conducted vibration of the midline forehead (Fz) in unilateral vestibular loss (uVL). Evidence for a new indicator of unilateral otolithic function. Acta Otorhinolaryngol Ital. 2010 revealed that there were significant differences when comparing Aug;30:175. wave V latency of the affected ear with control or with unaffected 2. Jacobson GP, McCaslin DL, Grantham SL, Piker EG. Significant vestibular system ear. There is no significant difference between the control ear and impairment is common in a cohort of elderly patients referred for assessment of falls risk. J Am Acad Audiol. 2008 Nov–Dec;19:799–807. the unaffected ear latency for wave V 500 Hz (Table 1)(Fig. 1). 3. Rosengren SM, Welgampola MS, Colebatch JG. Vestibular evoked myogenic The sensitivity of ABR 500 Hz in detecting affected cVEMP is potentials: past, present and future. Clin Neurophysiol. 2010 May;121 100% while its specificity was 66.6% (Table 2). These means that (5):636–651. 4. Zhou G, Cox LC. Vestibular evoked myogenic potentials: history and overview. every affected cVEMP patient showed affected ABR 500 Hz. While Am J Audiol. 2004 Dec;13:135–143. 66.6% of normal cVEMP showed normal ABR 500 Hz and 33.4% of 5. Akin FW, Murnane OD, Proffitt TM. The effects of click and tone-burst stimulus normal cVEMP showed affected ABR 500 Hz. parameters on the vestibular evoked myogenic potential (VEMP). J Am Acad Audiol. 2003 Dec;14:500–559. quiz 34-5. 6. Oh SY et al.. Vestibular-evoked myogenic potentials in central vestibular 4. Discussion disorders. J Neurol. 2016;263:210–220. 7. Gstoettner W, Burian M. Vestibular nuclear complex in the guinea pig: a cytoarchitectonic study and map in three planes. J Comp Neurol. The results of the current investigation showed prolonged ABR 1987;257:176–188. 500 Hz wave V latency in the affected ears when comparing it with 8. McNerney KM, Lockwood AH, Coad ML, Wack DS, Burkard RF. Use of 64-channel unaffected ear and normal. These results are attributed to the electroencephalography to study neural otolith-evoked responses. J Am Acad Audiol. 2011 Mar;22:143–155. abnormal function of the saccule, which cannot transmit low fre- 9. Emami SF, Pourbakht A, Sheykholeslami K, Kammali M, Behnoud F, Daneshi A. quency neural response from the vestibular endings to the cochlear Vestibular hearing and speech processing. ISRN Otolaryngol. 2010;1 :1–7 nucleus.10 In this research most cases with affected cVEMP, the Persian. 10. Emami SF, Gohari N. The vestibular-auditory interaction for auditory brainstem ABR wave V is broader than the control group. However, Emami response to low frequencies. ISRN Otolaryngol. 2014;2014:103598. and Gohari (2014)10 recorded that ABR 500 Hz amplitude was 11. Sheykholeslami K, Kaga K. The otolithic organ as a receptor of vestibular smaller in the affected ear when compared to unaffected ears hearing revealed by vestibular-evoked myogenic potentials in patients with anomalies. Hear Res. 2002;165:62–67. and normal ears which are discorded with our results showing 12. Emami SF, Daneshi A. Vestibular hearing and neural synchronization. ISRN no significant difference in ABR 500 amplitude; this is as result Otolaryngol. 2010;1:37–40. Persian. of the difference in the selection criteria as their patients were 13. Xu Z, Zhao P, Yang X, et al.. The hearing and vestibular evoked myogenic potentials test in patients with primary benign paroxysmal positional vertigo. BPPV cases with or without affected cVEMP. Moreover, there is Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2015;29:20–23. anatomical evidence of a projection from the saccular nerve into 14. Emami SF. Hypersensitivity of the vestibular system to sound and the cochlear nucleus; a number of specific brain areas may be pseudoconductive hearing loss in deaf patients. ISRN Otolaryngol. 2014;5. activated by the vestibular hearing. Sheykholeslami and Kaga Persian 817123.