Otology & Neurotology 35:932Y935 Ó 2014, Otology & Neurotology, Inc.

Letters to the Editor SAFE LEVELS OF ACOUSTIC STIMULATION: COMMENT ON ‘‘EFFECTS OF ACOUSTIC STIMULI USED FOR VESTIBULAR EVOKED MYOGENIC POTENTIAL STUDIES ON THE COCHLEAR FUNCTION’’

systems usually allow users to choose between clicks and tone bursts and generally specify stimulus intensity in decibel SPL or normal hearing level (nHL). However, these intensities do not reflect the total sound energy in a stimulus because the duration is not taken into account. Longer stimuli contain proportionately greater sound energy. The options for stimulus duration and shape are often limited in commercial systems, and sine waves sometimes require a minimum number of rise/fall or plateau cycles. Tone bursts of up to about 6 ms in duration are therefore quite common in the VEMP literature. LAeq is a measure of equivalent ‘‘A’’-weighted sound intensity over the measurement period, the usual reference being 1 second and thus gives a measure of energy delivered to the ear over the period specified. A-weighting is commonly used, possibly because this is similar to the attenuation of the middle ear (5). Total energy exposure is the product of sound intensity and time exposure and is also measured in decibels, where the reference energy (0 dB) is a pressure of 20 KPa applied for 1 second. An 87-dB LAeq stimulus given over 8 hours represents 132 dB of energy delivered to the ear, compared to this reference. Rosengren et al. (6) investigated the effects of different acoustic waveforms and energies on the VEMP and concluded that waveform energy was an important determinant of cVEMP amplitude. They calculated that, to stay within the required ‘‘upper exposure action values’’ (of 85 dB LAeq,8h, slightly less than the absolute upper limit of 87 dB), a 105-dB LAeq,1s stimulus could be presented at a rate of 5/s for a total of almost 5 minutes to each ear. For stimuli given at 5/s, a 105-dB LAeq,1s stimulus consisting of 0.1-ms duration click would be expected to have an intensity of 138 dB peak SPL; and for a 2-ms 500 Hz tone burst, an intensity of 131 dB peak SPL (see Appendix). Krause et al. (1) used a 500-Hz, 133-dB SPL stimulus to evoke cVEMPs, but the duration (10 ms) was longer than commonly used. The sound energy delivered by this stimulus (200 repetitions of a 500-Hz, 10-ms tone burst at 133 dB SPL at 5/s, assuming their intensity is measured as root mean square [RMS]) is equivalent to 133 dB. If all 200 stimuli are delivered, the energy slightly exceeds the maximum LAeq exposure specified by the EU limits (by 1 dB). The results of Krause et al. show that stimulating near the recommended limit in their sample of young subjects with normal hearing did not have any serious effects. But at this intensity/duration, there is little scope for safely increasing the number of stimuli given, which is needed when the reflex waveform is small or unclear, as often occurs in older subjects. Longer stimuli increase the amount of sound energy delivered to the ear but do not necessarily yield larger or clearer reflexes. Welgampola and Colebatch (7) showed

To the Editor: Krause et al. (1) have reported the effects on cochlear function of acoustic stimuli used in eliciting cervical vestibular evoked myogenic potentials (cVEMPs). They reported some subjective complaints of muffling of hearing, no significant change in pure-tone audiometry, but some reduction in distortion product otoacoustic emissions in the high-frequency range when measured 5 minutes after the cVEMP. Although the abnormal features settled the following day and were not considered to represent clinically relevant temporary hearing loss, the authors felt that patients need to be informed about the risk of adverse effects on hearing. The safety of diagnostic tests is an important consideration, although it is also recognized that some investigations do entail some risk to patients (e.g., ionizing radiation with conventional radiology). Any test that is to be used in large numbers of patients or in healthy volunteers should be as safe as possible. The cVEMP has become a popular additional investigation of inner ear function and can provide clinically relevant information in diseases such as superior canal dehiscence (SCD), otosclerosis, Me´neie`re’s disease, vestibular neuritis, and other conditions (2). The intensities of sound required to evoke the cVEMP are high (3), and correctly calibrated stimuli and audiometric equipment are essential. The technique has been widely used and very few side effects have been reported to date, although caution is suggested with patients with tinnitus. Although technically tone bursts are impulse noise, they are not typical of naturally occurring impulse noise and are probably better regarded simply as an interrupted sinusoidal waveform. Hearing damage is generally thought to relate to the peak intensity of sound pressure (blast-type injuries) or the total sound energy delivered to the ear (4). Industrial legislation in many countries reflects these concerns by specifying both the maximum sound pressure level (SPL) and the total sound energy exposure measured during a specified period (e.g., 8 h), with more intense sound requiring a reduction in the duration of exposure. For example, the European Union (2003) and U.K. (2005) guidelines for occupational exposure specify an upper limit of 200 Pa (140 dB peak SPL, C weighted) and an exposure equivalent to 87 dB LAeq,8h. Although these guidelines are not intended to cover medical contexts, it is prudent to consider the recommended levels and the reason behind them when selecting VEMP stimuli. Commercial VEMP 932

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LETTER TO THE EDITOR that VEMPs increased in amplitude with the duration of the 1-kHz stimulus to 7 ms and then decreased with longer stimuli. Corresponding results were reported by Cheng and Murofushi (8) and Lim et al. (9), who found a similar pattern for the 500-Hz tone bursts, with a maximum amplitude for a 6-ms stimulus, while a 10-ms stimulus had an average amplitude between that for a 2-ms and a 4-ms stimulus. A shorter stimulus given at the same peak intensity can be delivered for more repetitions without sacrificing the quality of the recording. For example, the 105-dB LAeq,1s stimulus used by Rosengren et al. (6) (namely 500 Hz, 2 ms) can be delivered 1,440 times at 5/s for a total of 130 dB of energy delivery, a total large enough to allow for additional repeated recordings when necessary. While long stimuli such as a 10-ms stimulus can be useful (e.g., in experimental contexts to provide sufficient duration for comparing different stimulus frequencies in tuning studies), they are uncommon in clinical settings. We recommend that in both clinical and experimental situations consideration be given to the total sound exposure when designing VEMP stimuli. The findings of Krause et al. (1) are interesting as they show that, even if sound exposure is greater than that typically used or required, there is no evidence of any permanent deleterious effects on cochlear function. Given that VEMP stimuli used in clinical settings are typically shorter, and provided that peak intensity limits are also not exceeded, VEMPs recorded for diagnostic purposes are unlikely to cause damage to the cochlea. James G. Colebatch, M.B., B.S., D.Sc

Prince of Wales Hospital Clinical School and Neuroscience Research Australia, University of New South Wales Sydney, Australia

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8. Cheng PW, Murofushi T. The effect of plateau time on vestibularevoked myogenic potentials triggered by tone bursts. Acta Otolaryongol 2001;121:935Y8. 9. Lim LJZ, Dennis DL, Govender S, Colebatch JG. Differential effects of duration for ocular and cervical vestibular evoked myogenic potentials evoked by air- and bone-conducted stimuli. Exp Brain Res 2013;224:437Y5.

APPENDIX Calculating Sound Energy Exposure A 500-Hz stimulus is attenuated by 3 dB under Aweighted filtering. Total sound energy exposure, where 0 dB = a pressure of 20 KPa given for 1 second, is as follows: Intensity (SPL) + 10  log10 (stimulus duration in seconds) where intensity is measured in dB RMS, A weighted. Thus, the reference of LAeq 87 dB for 8 hours gives an energy delivery of: 87 dB þ 10* log10 ð28; 800 sÞ ¼ 131:6 dBð132 dBÞ Likewise, the total energy delivery of Krause et al. is as follows: 133 dBj3 dBð A filterÞ þ 3 dBð2 s total durationÞ ¼ 133 dB:

RESPONSE TO: SAFE LEVELS OF ACOUSTIC STIMULATION: COMMENT ON ‘BEFFECTS OF ACOUSTIC STIMULI USED FOR VESTIBULAR EVOKED POTENTIAL STUDIES ON THE COCHLEAR FUNCTION’[

Sally M. Rosengren, Ph.D.

Royal Prince Alfred Hospital and Central Clinical School University of Sydney, Camperdown NSW, Australia The authors disclose no conflicts of interest. REFERENCES 1. Krause E, Mayerhofer A, G¨rkov R, et al. Effects of acoustic stimuli used for vestibular evoked myogenic potential studies on cochlear function. Otol Neurotol 2013;34:1186Y92. 2. Rosengren SM, Welgampola MS, Colebatch JG. Vestibular evoked myogenic potentials: past, present and future. Clin Neurophysiol 2010; 121:636Y51. 3. Colebatch JG, Halmagyi GM, Skuse NF. Myogenic potentials generated by a click-evoked vestibulocollic reflex. J Neurol Neurosurg Psychiatry 1994;57:190Y97. 4. Atherley GRC, Martin AM. EquivalentYcontinuous noise level as a measure of injury from impact and impulse noise. Ann Occup Hyg 1971;14:11Y28. 5. Zhang AS, Govender S, Colebatch JG. Tuning of the ocular vestibular myogenic potential (oVEMP) to AC sound shows two separate peaks. Exp Brain Res 2011;213:111Y16. 6. Rosengren SM, Govender S, Colebatch JG. The relative effectiveness of different stimulus waveforms in evoking VEMPs: significance of stimulus energy and frequency. J Vestib Res 2009;19:33Y40. 7. Welgampola MS, Colebatch JG. Characteristics of tone burstYevoked myogenic potentials in sternocleidomastoid muscles. Otol Neurotol 2001;22:796Y802.

In Reply: First, we want to thank the authors of the letter to the editor for their interest in our article, and for their valuable comments and additional notes. The aim of our study was to investigate the risk of cochlear side effects by acoustic stimuli, which are used for eliciting cervical vestibular evoked myogenic potentials (cVEMP). Although the cVEMP as an important diagnostic tool to test the sacculus function has become widespread in research and clinical practice, there were very few data about its safety. As the authors mentioned, we used 500 Hz tone burst stimuli with an intensity of 133 dB SPL, a tone burst duration of 10 milliseconds and a stimulus frequency of 5 per second. However, the stimuli were not applied over the entire 10 milliseconds at full intensity because a Hann window has been performed. To avoid excessive total sound energy exposure, we limited the repetition rate of the stimuli to n = 200. The total applied sound energy is relatively high but comparable with the values used in other research studies or clinical routine. Thus, the study results allow a meaningful and universal valid statement in relation to our question. In summary, we found that the acoustic stimuli used to elicit cVEMP have the potential to influence the cochlear function temporarily Otology & Neurotology, Vol. 35, No. 5, 2014

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LETTER TO THE EDITOR

(detected by DPOAE changes). On the other hand, a clinically relevant hearing loss was not found in healthy adult subjects. Subjective auditory symptoms were reversible within 24 hours. We agree with the authors that shorter stimulus duration (less than 10 ms) can reduce the exposure equivalent LAeq, 8hr and should protect the cochlea against overloading. In addition, it allows a higher repetition rate. Nevertheless, a residual risk persists. Our intention is to sensitize researchers and doctors to the potential risk of cochlear adverse effects by cVEMP stimuli. Therefore, we follow the recommendation of the authors of the letter to choose the stimulus duration as short as possible for the reduction of noise impact. As reported in the cited publications, 5- to 7-millisecond tone bursts seem to be optimal. Other options are to limit the repetition rate or to start with lower stimulus intensities and to increase it according to requirements (cVEMP thresholds). Eike Krause, M.D. Department of Oto-Rhino-Laryngology Head and Neck Surgery Ludwig Maximilian University of Munich Munich, Germany [email protected] Kai Boetzel, M.D. Department of Neurology Ludwig Maximilian University of Munich Munich, Germany The authors disclose no conflicts of interest. A STEP FURTHER IN VESTIBULAR TESTING FOR PATIENTS WITH VESTIBULAR SCHWANNOMA To the Editors: We read with great interest the article by Kinoshita et al. (1). As some papers early published (2,3), the author assessed cervical vestibular evoked myogenic potentials (cVEMPs), ocular vestibular evoked myogenic potentials (oVEMPs), and caloric test in 45 patients with vestibular schwannoma (VS) with the aim of clarifying the origin and pathway of oVEMPs after air-conducted sound (ACS). This article adds further elements to what was previously published in the same journal by Iwasaki et al. (4). VS sizes ranged from 6 to 50 mm (with a mean of 21.3 T 11.2 mm). Although it is not specified in the article, it could be guessed that most of the tumors had an extracanalicular component. It has been demonstrated that the rate of pathological responses on vestibular test for tumors extending toward the brainstem is dependant on tumor size (5). A correlation between vestibular tests in these conditions is very hard: VS is not an optimal model such as neurectomy or vestibular neuritis, even if we have small lesions (3,5). We studied 16 patients (62%) with intracanalicular tumors and only one case with a VS

sized more than 2 cm; despite that, we found substantial differences between results of vestibular tests and a different pattern of correlation between them (in particular we found no correlation between oVEMPs and caloric test, which was the most sensitive vestibular test). A more homogeneous sample across studies (especially considering only intracanalicular tumors) could allow a better comparison between results. On the other hand, we should consider that afferents running in every branch of the vestibular nerve come from different vestibular receptors, which may be more or less susceptible to damage. We do not believe that oVEMPs and caloric test results could be strictly matched because two different populations of vestibular fibers (irregular otolithic vs. regular canalar) are stimulated. Even if both responses run in the superior vestibular nerve, it must take into account that VS could affect each vestibular afferent in a complex way. We recently found in a subgroup of patients with small VS (G1 cm) a dissociation between results of the caloric test and of the video-head impulse test for each semicircular canal in more than 70% of cases (data presented at the XXVII Barany Society Meeting, Uppsala, 2012). ACS-oVEMPs are mainly mediated by the superior vestibular nerve, but we cannot exclude a contribution of the saccule in the genesis of these potentials (6). Why did the author not use the bone-conducted sound for cVEMPs, comparing results with ACS? The author found the absence of ACS-oVEMPs on both sides in about 25% of patients. This percentage is lower than ours, but still significant: have you hypothesized an explanation for this pattern? Finally, beyond the purely speculative aspects of the topic, a deeper clinical approach should not be forgotten every time we assess the vestibular test in patients with VS. We demonstrated that for small VS, vestibular evoked myogenic potentials were not useful as screening tests because of their low sensitivities, also reporting a case report in which a surgical sparing of the superior vestibular nerve was possible (3). In the article, there was a mention on seven patients in which the nerve origin of the VS was identified during surgery: did they perform vestibular tests in the follow-up? Did the pattern of response of preoperative vestibular tests influence postoperative symptoms? Was it possible to correlate results of vestibular tests to the hearing outcome? These are only some suggestions for future clinical trials to stimulate further and targeted research about the use of newer vestibular tests in this field. Gianluca Piras M.D. Giovanni Carlo Modugno M.D., Ph.D. Department of Experimental Diagnostic and Specialty Medicine (DIMES) ENT Unit, S.Orsola-Malpighi University Hospital University of Bologna Bologna, Italy [email protected] The authors disclose no conflicts of interest.

Otology & Neurotology, Vol. 35, No. 5, 2014

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LETTER TO THE EDITOR REFERENCES 1. Kinoshita M, Iwasaki S, Fujimoto C, et al. Ocular vestibular evoked myogenic potentials in response to air-conducted sound and boneconducted vibration in vestibular schwannoma. Otol Neurotol 2013;34:1342Y8. 2. Chiarovano E, Zamith F, Vidal PP, de Waele C. Ocular and cervical VEMPs: a study of 74 patients suffering from peripheral vestibular disorders. Clin Neurophysiol 2011;122:1650Y9. 3. Piras G, Brandolini C, Castellucci A, Modugno GC. Ocular vestibular evoked myogenic potentials in patients with acoustic neuroma. Eur Arch Otorhinolaryngol 2013;270:497Y504. 4. Iwasaki S, Murofushi T, Chihara Y, et al. Ocular vestibular evoked myogenic potentials to bone-conducted vibration in vestibular schwannomas. Otol Neurotol 2009;31:147Y52. 5. Suzuki M, Yamada C, Inoue R, Kashio A, Saito Y, Nakanishi W. Analysis of vestibular testing in patients with vestibular schwannoma based on the nerve of origin, the localization, and the size of the tumor. Otol Neurotol 2008;29:1027Y31. 6. Rosengren SM, Kingma H. New perspectives on vestibular evoked myogenic potentials. Curr Opin Neurol 2013;26:74Y80.

IN RESPONSE TO THE LETTER TO THE EDITOR: A STEP FURTHER IN VESTIBULAR TESTING FOR PATIENTS WITH VESTIBULAR SCHWANNOMA In Reply: We thank you for giving us the opportunity to respond to the comments and observations raised by our article entitled ‘‘Ocular vestibular evoked myogenic potentials in response to air-conducted sound and boneconducted vibration in vestibular schwannoma’’. The aim of our study was to investigate the neural origin of ocular vestibular evoked myogenic potentials (oVEMPs) to air-conducted sound (ACS) by comparing the results of oVEMPs to ACS with oVEMPs to boneconducted vibration (BCV), cervical vestibular evoked myogenic potentials (cVEMPs) to ACS, and caloric responses in patients with vestibular schwannoma (VS). We did not aim to predict the nerve origin of VS from the results of vestibular testing because we have previously demonstrated that the nerve origin of VS did not have a clear correlation with the results of the caloric test, cVEMPs, or auditory brainstem responses (1). However, we think that vestibular testing in VS patients is useful to better inform neurosurgeons of the involvement of each vestibular nerve before surgery and to predict the occurrence of vestibular symptoms after surgery. We did not

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include the results of cVEMPs to BCV in the present study because we performed cVEMPs to BCV in patients with conductive hearing loss. oVEMPs to ACS were absent on both sides in about 25% of patients in our study. This ratio is almost the same as the ratio of bilaterally absent oVEMPs to ACS in healthy subjects in our laboratory (2). We do not know the reason why many patients with VS showed absent oVEMPs to ACS on both sides in your laboratory. We are surprised to hear that there was no correlation between the results of oVEMPs and those of caloric tests in VS patients in your study. We agree in part with your explanation that the discrepancy between these two vestibular tests was caused by differences in the population of vestibular nerve fibers, which affects the result of each vestibular test. However, it is also possible that the discrepancy is caused by the difference in the degree of involvement of vestibular end-organ. VS can affect various parts of vestibular end-organ as well as vestibular nerves through obstruction of the blood supply to the inner ear (3). Although it is unclear why your results were different from ours, we agree with your opinion that a more homogenous study sample could allow a better comparison between results. Shinichi Iwasaki, M.D. Makoto Kinoshita, M.D. Department of Otolaryngology Faculty of Medicine University of Tokyo Tokyo, Japan [email protected] The authors disclose no conflicts of interest.

REFERENCES 1. Ushio M, Iwasaki S, Chihara Y, et al. Is the nerve origin of the vestibular schwannoma correlated with vestibular evoked myogenic potential, caloric test and auditory brainstem response? Acta Otolaryngol 2009;129:1095Y100. 2. Iwasaki S, Egami N, Inoue A, et al. Ocular vestibular evoked myogenic potential elicited from binaural air-conducted stimulations: clinical feasibility in patients with peripheral vestibular dysfunction. Acta Otolaryngol 2013;133:708Y13. 3. Telischi FF, Roth J, Stagner BB, Lonsbury-Martin BL, Balkany TJ. Patterns of evoked otoacoustic emissions with vestibular schwannomas. Laryngoscope 1995;105:675Y82.

Otology & Neurotology, Vol. 35, No. 5, 2014

Copyright © 2014 Otology & Neurotology, Inc. Unauthorized reproduction of this article is prohibited.

In response to the letter to the editor: a step further in vestibular testing for patients with vestibular schwannoma.

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