Research Article Clinical Use of Skull Tap Vestibular...

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Research Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials for the Diagnoses of the Cerebellopontine Angle Tumor Patients Erdem Yavuz, 1,2 Magdalena Lachowska, 3 Katarzyna PierchaBa, 3 Krzysztof Morawski, 3 Kazimierz Niemczyk, 3 and Rafael E. Delgado 1,2 1 Department of Biomedical Engineering, McArthur Annex, University of Miami, Coral Gables, FL 33124, USA 2 Intelligent Hearing Systems Inc., 6860 SW 81st Street, Miami, FL 33143, USA 3 Department of Otolaryngology, Medical University of Warsaw, Ulica Banacha 1a, 02-097 Warsaw, Poland Correspondence should be addressed to Magdalena Lachowska; [email protected] Received 28 November 2013; Revised 27 February 2014; Accepted 1 March 2014; Published 2 April 2014 Academic Editor: Mu-Kuan Chen Copyright © 2014 Erdem Yavuz et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Objective. To document our experiences using a new skull tapping induced Vestibular Evoked Myogenic Potentials (tap VEMPs) technique combined with standard Auditory Vestibular Evoked Myogenic Potentials (AC VEMPs) for advanced clinical assessment of cerebellopontine angle tumor (CPAT) patients. Design and Study Sample. ree patients were selected in order to highlight observations shown in a larger patient population and to show the variability of the findings. Both tap VEMPs and AC VEMPs were acquired from the sternocleidomastoid muscle (SCM) with EMG-based biofeedback and monitoring. Results. e usefulness of VEMPs was demonstrated, indicating the presence of a tumor and contributing additional information as to the involved nerve bundles in two out of the three cases. Conclusion. Due to the sensory organ dependency and related innervations differences, acquiring both AC VEMPs and tap VEMPs is likely to increase the probability of diagnosing CPATs and provide more information on the involved vestibular nerve bundles. is study demonstrates the feasibility of the possible expansion and combination of tap VEMPs and AC VEMPs techniques into a clinical diagnostic battery for advanced assessment of CPAT patients and its contribution as a guideline for the use of tap VEMPs in general. 1. Introduction Vestibular Evoked Myogenic Potentials (VEMPs) are one of the most recent methods added to the vestibular organ test battery. Although the initial reports of the VEMPs can be dated back to the early 1935 [1], the current highly used method based on the myogenic activity recordings from the sternocleidomastoid (SCM) muscle was introduced by Colebatch et al. [2, 3]. Sound evoked cervical VEMPs rapidly gained the attention of both researchers and clinicians, result- ing in numerous publications describing the clinical and research potential of VEMPs. Additional research extended the VEMP stimulation from auditory to skull tapping [4], bone conduction vibrations [5, 6], and galvanic stimulation [7, 8]. In addition to the SCM muscle, a variety of muscles were also shown to produce VEMPs, such as masseter [9], gastrocnemius, tibialis anterior, biceps femoris, quadriceps [10], and extraocular muscles [11, 12]. Auditory cervical approach is currently the most inves- tigated VEMP acquisition method. e current consensus on the sensory organ responsible for the Auditory Cervi- cal VEMPs (AC VEMPs) is the saccule [13, 14]. Saccular origin suggests that the inferior vestibular nerve functional integrity is essential in the generation of AC VEMPs as the majority of the sacculus innervation is carried by this nerve [1518]. More recently, skull tapping VEMPs (tap VEMPs) have been heavily investigated by various authors. e tap VEMPs are proposed to generate a more complex stimulation paradigm described as containing two different mechanisms, one resulting in an ipsilateral inhibitory activity on the SCM and the second acting bilaterally producing a response with a polarity which is opposite for the two SCM muscles [19]. Although it is still not clear which part of the vestibular organ is responsible for the tap VEMPs, the utricle has been designated to be the origin of the unilateral and bilateral components [1922]. However, the vibrations Hindawi Publishing Corporation BioMed Research International Volume 2014, Article ID 135457, 11 pages http://dx.doi.org/10.1155/2014/135457

Transcript of Research Article Clinical Use of Skull Tap Vestibular...

Page 1: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

Research ArticleClinical Use of Skull Tap Vestibular Evoked Myogenic Potentialsfor the Diagnoses of the Cerebellopontine Angle Tumor Patients

Erdem Yavuz12 Magdalena Lachowska3 Katarzyna PierchaBa3 Krzysztof Morawski3

Kazimierz Niemczyk3 and Rafael E Delgado12

1 Department of Biomedical Engineering McArthur Annex University of Miami Coral Gables FL 33124 USA2 Intelligent Hearing Systems Inc 6860 SW 81st Street Miami FL 33143 USA3Department of Otolaryngology Medical University of Warsaw Ulica Banacha 1a 02-097 Warsaw Poland

Correspondence should be addressed to Magdalena Lachowska mlachowskawumedupl

Received 28 November 2013 Revised 27 February 2014 Accepted 1 March 2014 Published 2 April 2014

Academic Editor Mu-Kuan Chen

Copyright copy 2014 Erdem Yavuz et al This is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Objective To document our experiences using a new skull tapping induced Vestibular Evoked Myogenic Potentials (tap VEMPs)technique combined with standard Auditory Vestibular EvokedMyogenic Potentials (ACVEMPs) for advanced clinical assessmentof cerebellopontine angle tumor (CPAT) patients Design and Study Sample Three patients were selected in order to highlightobservations shown in a larger patient population and to show the variability of the findings Both tap VEMPs and AC VEMPswere acquired from the sternocleidomastoid muscle (SCM) with EMG-based biofeedback and monitoring ResultsThe usefulnessof VEMPs was demonstrated indicating the presence of a tumor and contributing additional information as to the involved nervebundles in two out of the three cases Conclusion Due to the sensory organ dependency and related innervations differencesacquiring both AC VEMPs and tap VEMPs is likely to increase the probability of diagnosing CPATs and provide more informationon the involved vestibular nerve bundles This study demonstrates the feasibility of the possible expansion and combination of tapVEMPs and ACVEMPs techniques into a clinical diagnostic battery for advanced assessment of CPAT patients and its contributionas a guideline for the use of tap VEMPs in general

1 Introduction

Vestibular Evoked Myogenic Potentials (VEMPs) are one ofthe most recent methods added to the vestibular organ testbattery Although the initial reports of the VEMPs can bedated back to the early 1935 [1] the current highly usedmethod based on the myogenic activity recordings fromthe sternocleidomastoid (SCM) muscle was introduced byColebatch et al [2 3] Sound evoked cervical VEMPs rapidlygained the attention of both researchers and clinicians result-ing in numerous publications describing the clinical andresearch potential of VEMPs Additional research extendedthe VEMP stimulation from auditory to skull tapping [4]bone conduction vibrations [5 6] and galvanic stimulation[7 8] In addition to the SCM muscle a variety of muscleswere also shown to produce VEMPs such as masseter [9]gastrocnemius tibialis anterior biceps femoris quadriceps[10] and extraocular muscles [11 12]

Auditory cervical approach is currently the most inves-tigated VEMP acquisition method The current consensuson the sensory organ responsible for the Auditory Cervi-cal VEMPs (AC VEMPs) is the saccule [13 14] Saccularorigin suggests that the inferior vestibular nerve functionalintegrity is essential in the generation of AC VEMPs asthe majority of the sacculus innervation is carried by thisnerve [15ndash18] More recently skull tapping VEMPs (tapVEMPs) have been heavily investigated by various authorsThe tap VEMPs are proposed to generate a more complexstimulation paradigm described as containing two differentmechanisms one resulting in an ipsilateral inhibitory activityon the SCM and the second acting bilaterally producing aresponse with a polarity which is opposite for the two SCMmuscles [19] Although it is still not clear which part ofthe vestibular organ is responsible for the tap VEMPs theutricle has been designated to be the origin of the unilateraland bilateral components [19ndash22] However the vibrations

Hindawi Publishing CorporationBioMed Research InternationalVolume 2014 Article ID 135457 11 pageshttpdxdoiorg1011552014135457

2 BioMed Research International

conducted via bone are propagated to a large region on theskull and may stimulate other parts of the vestibular organTherefore skull tapping is a more complex stimulus typelikely to result in activation of multiple sensors on both sidesof the head bilaterally activating the superior and inferiorvestibular nerves [23 24] Evidence strongly suggests that tapVEMPs to a significant extent are dependent on superiorbundle of vestibular nerve they are more often affected inpatients with vestibular neuritis (which usually affects onlythe superior vestibular nerve) in contrast to AC VEMP [25]It has been also reported that the tap VEMPs can be recordeddespite selective section of the inferior vestibular nerve [26]indicating that tap VEMPs strongly rely on the superiorvestibular nerve [23]

Initial tap VEMP studies were performed by using amanually controlled reflex hammer attached to a triggeringmechanism [4] Skull tapping via reflex hammer is prone todeliver varying amount of momentum with each individualhit to the test subject thus causing variability in the responseLater studies used mechanically controlled vibration andimpact generating devices for skull tapping in order tostandardize the amount of momentum delivered with eachtap [23 27 28] These devices are generally held by handagainst the impact site on the skull The forces delivered bythese devices are also prone to variability as the position onthe head and the hand position are likely to change duringthe recordings The major source of variability in VEMPrecordings is shown to be the contraction level of the musclethat is used as the electromyelography (EMG) source It hasbeen shown that the VEMP amplitude is directly related tothe strength of the background SCM muscle activity and isabsent at rest [3 29 30] In general duringVEMP recordingsthe subject is asked to push the head against a structureto ensure a certain amount of contraction in the cervicalmuscles [3] or asked to lie in supine position lifting theirheads up [4] or asked to turn their heads away from thestimulus [31] Although the abovementioned methods formuscle contraction can help tomaintainmuscle activity nonecan be used to guarantee a constant EMG activity range Toovercome this problem EMG-based biofeedback methodswere developed to increase the cooperation of the subjectsso that the subject can monitor and correct the contractionlevel of the muscle In this approach a muscle activity valueis calculated from the rectified EMG signals and displayed tothe subject as feedback [21 32]

VEMPs stand out as a promising tool in clinical practiceas they are noninvasive and easy to acquire with low time andinstrumentation cost Additionally when acquired togetherAC VEMPs and tap VEMPs may be used as a tool to identifythe functional integrity of inferior and superior vestibularnerves

Despite large amount of research onVEMPs and constantdevelopment of the instrumentation and methods for theclinical usage VEMPs and in particular tap VEMPs are stillnot well established clinically due to a number of issues Someof these issues are lack of a standardized tap VEMP specificdevice limited or no quantification on the delivered forceand instantaneous EMG activity lack of clinical experience

sensitivity specifications and also lack of established clinicalprotocol for the use of tap VEMPs

In this paper our main goal is to establish a clearrepeatable protocol for the clinical assessment of CPATcases geared by the recent developments in the objectivevestibular functional evaluation methods particularly thecomplimentary use of AC VEMPs and tap VEMPs in dailyclinical practice In our department VEMPs are part of aroutine testing on various vestibular problems particularlyon patients with cerebellopontine angle tumors (CPAT) Inthis study we present results of AC VEMP and tap VEMPrecordings acquired with the use of a new prototype auto-mated skull tapping device (Intelligent Hearing System IncMiami FL) that can be stabilized on the skull using a head-band that ensures a fixed placement and contact pressureAdditionally an EMG standardization method integratedinto the acquisition software is used to further minimizethe variability of the AC VEMP and tap VEMP recordingsThis paper describes our findings on 3-case examples froma growing patient data pool which will be presented in thefuture

2 Material and Methods

21 Clinical Investigation Protocol In our department whena patient is identified as a potential CPAT case our generalprotocol is to conduct a diagnostic battery on the patient byfollowing a diagnostic procedure for vestibular or acousticschwannoma [33] using the standard tests with the compli-mentary addition of AC VEMPs and tap VEMPs The orderof the tests in the following list reflects the escalation in thediagnosis towards a CPAT case

(1) Patient history(2) Otoscopy(3) Audiological assessment (particularly for signs of

compression reflecting the involvement of othernerves that share the same trajectory in the auditorycanal [34ndash36]) that involves pure tone audiome-try speech discrimination test impedance audiom-etry with stapedius reflex and auditory brainstemresponse (ABR)

(4) Examination of the patients by acquiring auditoryand skull tapping VEMPs according to the protocolthat will be described in detail below Due to thesensory organ dependency and related innervationsdifferences as mentioned above recording both theAC VEMPs and tap VEMPs further increases thepotential of identification of the affected nerve bun-dles For instance in cases where no or reduced ACVEMPs are observed but tap VEMPs are presenta nonfunctional inferior bundle but a functioningsuperior vestibular nerve can be estimated

(5) Themagnetic resonance imaging (MRI)with gadolin-ium enhancement is currently viewed as the mostaccurate diagnostic tool for VIII nerve schwannomacapable of identifying tumors as small as 3mm insize On the other hand it is quite costly and it is

BioMed Research International 3

not performed at the early stages of the diagnosticsprocedure In many countries where health servicesare rationed a clear indication of tumor presenceis necessary for scheduling an early MRI appoint-ment The MRI is performed if tests described aboveindicate the high suspicion of the CPAT accordingto cross-check rule In MRI tumor size location inthe internal auditory canal (which part of the canal)and brainstem compression if present are describedThis information is very helpful in consideration ofsurgery approach which depends on the size andlocation of the tumor and the degree of hearing loss

(6) Clinical and electrical examination of the facial nerveis performed to test the facial nerve involvement

(7) Surgical referral

While the MRI provides information on tumor presenceand its size and location in the internal auditory canal (whichpart of the canal) that are essential for the surgeon it does notprovide information about which nerve bundles are involvedin the process The information provided by ABR and ACVEMPS and tap VEMPs together is very useful for a surgeondue to the relationship of cochlear and vestibular nervesin the internal auditory canal The vestibulocochlear nervedivides into individual nerves in the lateral aspect of theinternal auditory canal cochlear nerve more anteriorly andboth vestibular nerves superior and inferior more posteriorly[34ndash36]The facial nerve courses anterior like cochlear nervebut remains more superior to it The nerves all togetherrotate 90 degrees in their course from the fundus of theinternal auditory canal to the cerebellopontine angle sothat the cochlear nerve rotates from anterior to posteriorbut stays most inferior [34] As the vestibulocochlear nervedivides into individual nerves the presence of a tumor canbe reflected by malfunctions of these nerves depending onwhich nerve the compression occurs

22 Acquisition of AC VEMPs and tap VEMPs All VEMPrecordings were conducted using surface electrodes placedon the skin above SCM muscle The positive electrodes wereplaced bilaterally on the midpoint of the SCM muscle mea-sured between the points where the muscle was connectedto the mastoid and the sternumThe negative electrodes werepositioned on the sternumand the SCM junctionThegroundelectrode was placed laterally on the zygomatic bone so thatthe placement of the skull tapper on the foreheadwas possiblefor tap VEMP recordings

All VEMPs were acquired using SmartEP evoked poten-tial acquisition system on the IHS USB Box platform(Intelligent Hearing Systems Inc Miami FL) Recordingswere performed with sampling period of 400ms with 5Kamplification filtered using a 6 dB per octave band passfilter with highpass cutoff set at 30Hz and lowpass cutoffset at 1500Hz The AC VEMPs were collected by averaging128 sweeps and tap VEMPs were acquired averaging 64sweeps Less number of sweeps was used for the tap VEMPsas skull tapping was found to generally generate largeramplitude responses compared to the auditory counterpart

For each recording site and type two sets of recordingswere made which were later averaged to increase the signalto noise ratio The two sets of recordings were used tomonitor the repeatability of the recorded signals The ACVEMPs were evoked by 5000ms long 500Hz tone burstsconditioned by an exact Blackman window delivered viaER3a ear insert phones (Etymotic Research Inc Elk GroveVillage IL) at 100 dBnHL The tap VEMPs were evokedby a prototype skull tapping device produced by IntelligentHearing Systems Corp The skull tapper was composedof an electromagnetic push type mechanism automaticallycontrolled by the software to deliver a controlled force witha hit onset detection mechanism The piston of the tapperwas held at the same position for 100ms following the hitat the surface interfacing the skull to ensure a unidirectionalforce delivery The delivered force was measured to be 105Nusing a commercially available artificial mastoid device (type4930) Bruel amp Kjaeligr (Naeligrum Denmark) Details on theskull tapper device will be described in a separate article Astimulation rate of 31s was used for both VEMP recordingtypesThe recording system uses an EMG-based biofeedbackmonitoring method to minimize the variation in the SCMmuscle contractions and thus the variation in the amplitudeof VEMPs This method is based on continuous monitoringof pre- and poststimulus EMG activity In this method twoconditions had to be fulfilled for a window of a recordingcycle to be accepted into the average (a) the root meanssquared (RMS) EMG activity had to fall into a range setby the user (generally minimum at 50120583V and maximum at150 120583V RMS) and (b) the poststimulus activity should notexceed a user set artifact rejection value If both cases weresatisfied an illustration of a smiling face was shown on themonitor to the patient (this would indicate to the patient thatthe SCMmuscle contraction was sufficient for recording andthat heshe should stay in this position to complete the set ofrecordings) In addition a green bar showing the actual EMGRMS levels was also presented When any of the conditionswas notmet the smiling facewas replaced by an upset face andthe EMG bar color was turned to red A secondary feedbackindicator box that contained a red and a green LED light wasalso present Both indicators were used to increase the patientcooperation with the SCMmuscle contraction and minimizethe muscle fatigue

The skull tapper was placed on the skull at three locations(a) at the midline on the forehead (b) behind the left earon the mastoid process and (c) behind the right ear on themastoid process The stabilization of the skull tapper wasensured using an adjustable head band

The recordings were performed with the patients com-fortably resting in a supine position and lifting the head uptowards midline The patients were directed to just lift thehead with no shoulder and abdominal muscle activity ifpossible During all recordings a researcher was present at alltimes directing the patient to increase or decrease the lift ofthe head or the turn movement to stay in the selected RMSEMG levels using the biofeedback monitor for guid ance

Three different types of recordings were conducted withAC VEMPs (two repetitions each)

4 BioMed Research International

AHLB MHLLMHLR

Head lift stimulation sites

Skull tapper side view

Skull tapper front view

Audio stimulus

AHLR AHLL FHL

Figure 1The stimulus presentations sites for the head lift recordingsmade for acoustic and skull tap VEMPs Abbreviations in the illustrationindicate the stimulus type and direction as follows (1) head lift stimulus delivered to the right ear (AHLR) (2) head lift stimulus deliveredto the left ear (AHLL) (3) head lift stimulus delivered to both ears (AHLB) (4) forehead head lift (FHL) (5) mastoid head lift skull tapperlocated at right (MHLR) (6) mastoid head lift skull tapper located at left (MHLL)

(1) head lift stimulus delivered to the left ear (AHLL)(2) head lift stimulus delivered to the right ear (AHLR)(3) head lift stimulus delivered to both ears (AHLB)

Three different types of recordingswere conducted for theskull tapping evokedVEMPs (two repetitions each)with skulltapper located at

(1) forehead head lift both sides recorded (FHLB)(2) mastoid head lift skull tapper located at left (MHLL)(3) mastoid head lift skull tapper located at right

(MHLR)

Therefore a total of 12 recordings were conducted for eachpatient (6 total typeswith two repetitions) before and after thesurgical intervention as shown in Figure 1

The recorded responses were normalized according tothe prestimulus (base) EMG RMS calculations Normalizedvalueswere used to assess the asymmetry ratios (AR) betweenthe left and right side measurements The usefulness of thenormalization of ARmeasurements is still under debate [37]The following equation (1) was used for the asymmetry ratiowhere the 119860

119871is the amplitude measure from the left side

recording between the first positive and first negative peakand similarly 119860

119877is the amplitudemeasured on the right side

Corrected AR of up to 35 is considered normal [38]

Asymmetry Ratio = 100100381610038161003816100381610038161003816100381610038161003816

(119860119871minus 119860119877)

(119860119871+ 119860119877)

100381610038161003816100381610038161003816100381610038161003816

(1)

During the course of this study additional VEMP record-ings were made where the SCM contraction was sustainedvia the head turn to the sides In this paper we only presentthe results and the details of the head lift data as we foundthe head turn method to be unreliable when analyzed via

asymmetry ratio approach We prefer and advocate the headlift approach as it is much easier to control and identify if apatientrsquos head is symmetrically lifted or not For this reasonwe believe that the VEMPs recorded via head lift are lessprone to be affected by the orientation differences of thevestibular organs during the recording sessions compared tohead turnwith the current instrumentation limits Additionalfeedback monitoring of the 3D positioning of the head byusing additionalmeans such as gyroscopes andor accelerom-eters could help to minimize this variability

23 Participating Patients Details

Patient Number 1 Patient number 1 was a 43-year-old manwho suffered from slight tinnitus and slight hearing loss inhis right ear with no vestibular problems prior to admis-sion Audiological tests revealed a small high-frequencysensorineural hearing loss on the right side with pure toneaverage (PTA) for 3 and 4 kHz = 35 dBHL The speech dis-crimination score at 60 dB was almost normal (80 scored100 at 70 dB) Impedance audiometry revealed normalmiddle ear function and normal stapedius reflex thresholdson both sides Normal response to click stimulus at 90 dBnHLwas present on the left side in ABR but on the right sideABR showed retrocochlear abnormality Vestibular calorictest and videonystagmography showed normal responseson both sides with no central vestibular disorders Detailson the VEMP recordings will be described in the Resultssection MRI revealed a tumor in the internal auditory canalthe tumor was 12 times 9mm in size Clinical and electricalexamination (using electromyography) of the right facialnerve revealed its normal function

Middle fossa approach was chosen for the surgeryattempting to preserve the hearing The tumor appeared to

BioMed Research International 5

arise from cochlear nerve and was attached to other nervesin the internal auditory canal

Patient Number 2 Patient number 2was a 51-year-oldwomanPrior to the admission she complained about tinnitus andhearing loss in the right ear with some symptoms of rightfacial nerve paresis Pure tone audiometry revealed sen-sorineural hearing loss on the right side with PTA for 05 and1 kHz = 30 dBHL and for 2 and 4 kHz = 575 dBHL and thespeech discrimination score at 60 dB was 30 for the rightear Normalmiddle ear functionwas provedwith tympanom-etry but stapedius reflexes were missed Normal response toclick stimulus at 90 dBnHLwas present on the left side inABRand no reproducible waves on the right Vestibular calorictest and videonystagmography revealed aflexia on the rightside with no central vestibular abnormalities and normalfunction on the left Clinical and electrical examination(electromyography) of the right facial nerve revealed itsabnormal function Details on the VEMP recordings will bedescribed in the results section MRI showed a 4 times 9mmtumor in the right internal ear canal

Middle fossa approach was selected to increase thepossibility of hearing preservationThe tumor seemed to arisefrom superior vestibular nerve but involved the inferior oneas well

Patient Number 3 Patient number 3 was a 26-year-oldwoman whose main complaint was tinnitus on the left sideAt the admission she stated not having any other hearingor vestibular problems Auditory testing revealed normalhearing in both ears in all audiometric frequencies withthe pure tone average for 05 1 2 and 4 kHz = 25 dB andspeech discrimination score at 60 dB was 100 Impedanceaudiometry revealed normal results Auditory brainstemresponse showed normal reproducible waves on both sidesVestibular caloric test and videonystagmography showednormal responses on both sides with no central vestibulardisorders Left facial nerve function was normal VEMPswill be discussed in the Results section Due to the patientrsquoshistory of asymmetric tinnitus and young age it was decidedto perform MRI The MRI revealed a tumor in the internalauditory canal the tumor was 7 times 5 times 15mm in size

For the surgery middle fossa approach was selected forthe hearing preservation The tumor seemed to arise fromsuperior vestibular nerve

This study is a part of a retrospective-prospective projectthat was approved by the Ethics Committee Review Boardat the Medical University of Warsaw where the VEMPsrecordings have been conducted The project conforms withThe Code of Ethics of the World Medical Association (Dec-laration of Helsinki)

3 Results

Table 1 shows AC VEMP and tap VEMP results with valuesfor P1 latencies and corrected amplitudes of the responsesalong with corrected asymmetry ratios Figure 2 presents theresults of the preoperative (preop) recordings acquired byboth VEMP techniques Figure 3 shows the change observed

between the preop and postoperative (postop) responsesrecorded from the ipsilateral side to the tumor

Patient Number 1 In this patient highly large correctedasymmetry ratio (AR) values for AC VEMPs (AHLB AR =4759 AHLL versus AHLR AR = 4543) were observedValues lower than 35 are considered normal [38] and weused them as referral In close inspection of the waveformsfrom the contralateral side one can easily see that the left sidestimulation producedmuch smaller activity on the right sidewhere the right side stimulation did not produce a similaractivity on the left side (Figure 2)

The tap VEMPs were symmetric for the forehead (FHLBAR = 1915) and for the mastoid skull tapping resultsrecorded from the ipsilateral side SCM (right MHLR versusleft MHLL AR = 1684)

The postop responses were compared with the preop data(Figure 3) The AC VEMPs results showed that P1 and N1disappeared when the ear ipsilateral to the tumor was stim-ulated In the bilaterally stimulated recordings we observedthe preservation of these peaks to an extent Considering thesurgical cut of the ipsilateral inferior bundle the preservationof the peaks suggested the contribution of the contralateralside Forehead placement tapVEMPs showed a reversal in therecorded P1-N1 peak complex In all of the above recordingsthe later waveforms observed between 25 and 60ms rangewhich are generally regarded as cochlear in origin [24 39]did not display a major change

Patient Number 2 Patient number 2 medical history alongwith unilateral sensorineural hearing loss poor speech recog-nition ABR VNG and facial nerve EMG results pointed toimpaired function of VIII and VII nerves on the right side

In AC VEMPs we observed drastic differences betweenleft and right side responses (AHLB AR = 4349) The rightside auditory stimulation failed to generate a response wherethe left side stimulation evoked a robust response (Figure 2)

Skull tapping the forehead and each mastoid resulted inlarge ARs (FHLB AR = 5760 MHLR versus MHLR AR =6132) Upon visual inspection of ipsilateral responses theinitial parts of thewaveformmorphology (P1-N1 region)weredifferent (Figure 2)

In the postop preop comparison (Figure 3) there wereno significant changes in any of the responses recordedipsilateral to the tumor in neither of the VEMP techniquesfor P1 and N1 peaks suggesting that both bundles had totalfunctional loss before the surgery Additionally similar tothe first patient late waveforms did not display a significantchange

Patient Number 3 In patient number 3 all audiologicalVNG and VEMP tests were within normal limits Due topatientrsquos young age and history of tinnitus on the left side thissuggested that there might be a retrocochlear problem

No asymmetry was observed in the AC VEMPs (AHLBAR = 1662 AHLR versus AHLL AR = 1995) and tapVEMPs (FHLB AR = 1718 MHLR versus MHLL AR= 1929) The mastoid ipsilateral tap VEMP recordingsshowed high similarity In this case both AC VEMP and

6 BioMed Research International

Table1Au

ditory

andskulltap

VEM

Phead

liftresults

Patie

ntAnalyzed

parameter

Headlift

Auditory

Tapp

ingforehead

Tapp

ingmastoidsIPS

Irespo

nses

AHLB

AR(

)

AHLL

AHLR

AR(

)

FHLB

AR(

)

MHLL

MHLR

AR(

)Re

spon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

1P1

latency

(ms)

1320

1340

1340

1420

1320

1440

1400

1440

Corram

plitu

de2556

908

4759lowast

2296

862

4543lowast

3624

2459

1915

3367

2397

1684

2P1

latency

(ms)

1400

1360

1460

NR

1440

1520

1720

1560

Corram

plitu

de1314

518

4349lowast

2351

NR

3322

894

5760lowast

3819

916

6132lowast

3P1

latency

(ms)

1260

1280

1280

1300

1400

1360

1440

1320

Corram

plitu

de1019

1414

1626

1962

2940

1995

4488

3172

1718

5823

3940

1929

AHLB

headlift

stimulus

delivered

tobo

thearsA

HLL

headlift

stimulus

delivered

totheleftearAHLR

headlift

stimulus

delivered

totherig

htearFH

LBForeheadHeadLiftskulltapperlocated

atforehead

MHLL

Mastoid

HeadLiftskulltapperlocatedat

Left

MHLR

Mastoid

HeadLiftskulltapperlocatedat

RightP1p

ositive

peakcorram

plitu

decorrected

amplitu

deS

CMsternocleidom

astoid

muscle

AR

Asymmetry

ratio

NR

norespon

seA

bnormalresults

ofcorrectedasym

metry

ratio

s(ARgt35)a

ndno

respon

seresults

(NR)

arem

arkedwithlowast

BioMed Research International 7

AHLR

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

AHLL

(a)

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

AHLR

AHLL

(b)

AHLB

AHLL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

AHLR

(c)

Figure 2 VEMP waveforms recorded from all 3 subjects All the waveforms are normalized according to prestimulus EMG activity In thisfigure left side recordings are plotted as solid lines while right side recordings are plotted as dashed lines Abbreviations are used in thisfigure as follows AHLB auditory head lift both ear stimulation recorded bilaterally AHLL auditory head lift left ear stimulation recordedbilaterally AHLR auditory head lift right ear stimulation recorded bilaterally FHLB head lift recording tapper located at forehead recordedbilaterally MHLL head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at rightmastoid recorded bilaterally

tap VEMP results failed to point to a tumor presence TheMRI showed a tumor in the left internal auditory canal(7 times 5 times 15mm) During the surgical intervention thetumor was identified as arising from the superior vestibularnerve

In the postop versus preop comparison (Figure 3) of thehead lift AC VEMP recordings no significant change onthe tumor side was found when both ears were stimulatedHowever significant difference was shown when the stim-ulation was at the side of pathology For the tap VEMP

8 BioMed Research International

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

(a)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

(b)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

(c)

Figure 3 Preop (solid lines) and postop (dashed lines) VEMP waveforms recorded ipsilateral to the pathology from all 3 subjects Allthe waveforms are normalized according to prestimulus EMG activity Abbreviations are used in this figure as follows where ipsilateralindicates the location in return to the pathology location AHLB ipsilateral auditory head lift recording with both ears stimulated AHLipsilateral auditory head lift recording in return to ipsilateral stimulation FHLB ipsilateral head lift recording tapper located at foreheadMHL ipsilateral head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at ipsilateralmastoid

P1 peak could not be identified in any of the recordingsand N1 peak amplitudes were diminished in all recordingsexcept for the forehead placement where N1 latency andamplitude were preserved In general more variability inlatency and amplitude was also present for the later waves aswell

4 Discussion

In todayrsquos audiovestibular clinical practice a large numberof tests are available to determine the functionality of theaudiovestibular system The selection and the use of thesetests are mostly limited by their selectivity practicality and

BioMed Research International 9

costs The rapid development of VEMP related research andour recent experience with AC VEMPs and tap VEMPs haveled us to use VEMPs as an integral part of our diagnosticbattery In our department we routinely use the cervicalVEMPs due to the longer history thus there is larger amountof accumulated research on cervical VEMPs Currently weare also investigating the use of relatively newer approachof ocular VEMPs and adding it to our collected data setAlthough the recent research on ocular VEMPs has beenencouraging for clinical usage the technique has to still berefined to be used as a routine test The cervical VEMPs areeasy to acquire and can be efficiently used with quantificationmethods for ongoing muscle activity monitoring such asthe one used in this study where acceptance and rejectionmuscle activity regions are used Our near feature planis to include the ocular VEMPs recording in our routinediagnostic tests ensuring that the adaptation of the muscleactivity quantification methods we use is properly utilized

Our results showed that the VEMP recordings werenot only capable of identifying the CPAT but were alsoable to contribute additional information of involved nervebundles in first patient The observed abnormal audiologicalfindings strongly suggested the initial diagnosis of vestibularschwannoma The MRI pointed to the presence of a tumorlocated in the right internal auditory canal VEMP results alsosupported the presence of a tumor additionally pointing tothe inferior vestibular nerve involvementThe surgery reportdescribed the tumor to be arising from cochlear nerve and tobe attached to the other nerves in the internal auditory canalThe cochlear nerve is located closer to the inferior bundle ofthe vestibular nerve [34ndash36] and compression on the inferiornerve therefore was affecting the AC VEMPs results but notaltering the proper function of the superior vestibular nerve(AR in tap VEMPs within normal limits [38])

For the second patient the audiological results alongwith VNG and VEMP results strongly suggested the tumorpresence in the internal auditory canal which was supportedby theMRI findingsThe surgeon described the tumor arisingfrom superior vestibular nerve involving the inferior bundleas well During the surgery the tumor was found to be biggerthan initially described by the MRI which was performed afew months before As routinely done prior to the surgerythe other tests including VEMPs were performed to decideon the surgical approach and determine the possibility forhearing preservation In this case the tumor affected thefunction of all the nerves in the internal auditory canal Ourconclusion from the AC VEMP and tap VEMP findings wasthe involvement of both the inferior and superior nervesThe VEMPs were successful in pointing out both the tumorpresence and the involvement of both of the vestibularnerves An interesting observation was that the left andright responses recorded during both right side and left sideauditory stimulation were highly similar suggesting that thewhole response seen in AHLBmight have been driven by theleft ear

The third patient was a particularly interesting casebecause all tests performed along with AC VEMPs and tapVEMPs proved to be not helpful in the diagnosis of thevestibular schwannoma Although the tumor was arising

from the superior vestibular nerve the tap VEMP failed toindicate presence of the tumor similar to the rest of theclinical tools suggesting a normal function In this case onlythe MRI was sensitive enough to show the tumor The MRIwas performed due to the history of the patient her youngage and our experience in vestibular schwannoma casesThereason why the recorded tap VEMPs were not able to detectthe pathology is a good question to investigate

We observed that the mastoid placement of the skulltapper created additional challenges It was extremely difficultto replicate the same conditions when the skull tapper wasplaced on a surface of the mastoid region Due to the 3-dimensional shape of the mastoid area it was very difficultto maintain a steady 3D relation between the head and theskull tapper hit axis (thus with the vestibule axis) especiallywhen tapper is moved from one side to the other As with thecurrent setup there was no chance of monitoring the relationbetween the skull tapper hit direction and the vestibularorgans and it was not possible to limit the introducedvariability In the light of these observations (although weacquired data with skull tapper positioned at mastoids onboth sides and described the results of the responses acquiredfrom the ipsilateral SMCs) we preferred to relay and advocatethe usage of the forehead stimulation results due to the limitsof currently available instrumentation The directional infor-mation revealed by themastoid placement is complex and hasto be carefully analyzed For general clinical implementationadditional safeguards are required An additional feedbackmechanism describing the orientation relation between thetapper and gravity such as a gyroscope could be helpfulin minimizing the variability and thus could be useful inproducing equivalent directional force delivery to each sidewhen skull tapper is moved from left to right

5 Conclusions

In this paper we introduced our efforts in adding the ACVEMPs and tapVEMPs to expend the clinical diagnostic testsused for advanced assessment in CPAT patients hoping thatit will serve as a guideline for other clinicians interested inutilizing tap VEMPs

The patients presented in this study were selected topoint out different results we observed among a larger patientpopulation The findings from the larger population groupwill be presented in a more detailed follow-up subsequentpaper The main goal of this paper was to focus on theprotocol used and point at the variability in the findings

In two of three presented cases AC VEMPs and tapVEMPs together proved to be helpful in establishing thediagnosis of CPAT providingmore information on the tumoraffected bundle of vestibular nerve (superior or inferior orboth) Performing only AC VEMPs or only tap VEMPswould have provided insufficient information about thetumor and the vestibular nerve bundle involvement Inthe third case VEMPs failed to identify the vestibularschwannoma which was clearly shown in MRI scans Inthis case our medical intuition and expertise with CPATpatients prompted us to perform MRI Due to the high cost

10 BioMed Research International

of MRI it is typically not performed at the early stages ofthe diagnostics procedure in many countries Once othertests indicate the possible presence of the CPAT an MRI isconducted

Providing AC VEMPs and tap VEMPs to the availabletest battery in the assessment of CPAT is likely to improvethe diagnostic process by providing more information onthe involved vestibular nerve bundles In addition thisinformation might be used later during the surgery In manycases theMRI is not performed very short before the surgeryUsually it is performed earlier during the diagnostic processThe surgery takes place sometime after Asmentioned beforethe MRI is quite costly and usually is not performed againif not much time passed However the ABR AC VEMPsand tap VEMP once performed in diagnostic proceedingmight be repeated short before the surgery to clarify thepresence along with possible compression characteristics ofthe tumor on the vestibular andor auditory nerves Thiscombined information from earlier MRI scans and latestelectrophysiological tests serves the surgeons as a guidelinein their surgical approach and during tumor removal Itprovides very useful information for the surgeon in makinga decision about additional intraoperative monitoring ofhearing In our department intraoperative monitoring isroutinely used in every CPAT surgery and many otherear surgeries but intraoperative hearing monitoring is notroutinely performed in most of the other clinics In additionthe details from electrophysiological tests about the involvednerve bundles are useful in patients counseling and informingthem on more realistic possible outcomes of the surgery likehearing preservations possibilities and a risk of hearing lossduring the surgery a risk of facial nerve paresis and vertigosymptoms after the surgery

Abbreviations

ABR Auditory brainstem responseAS Asymmetry ratioCPAT Cerebellopontine angle tumorECochG ElectrocochleographyEEG ElectroencephalographyEMG ElectromiographyMRI Magnetic resonance imagingPTA Pure tone averageRMS Root means squaredSCM SternocleidomastoidVEMP Vestibular Evoked Myogenic PotentialAC VEMP Auditory Vestibular Evoked Myogenic

Potentialtap VEMP Skull tapping induced Vestibular

Evoked Myogenic Potential

AC VEMPsThree Types of Recordings

AHLL Head lift stimulus delivered to the left earAHLR Head lift stimulus delivered to the right earAHLB Head lift stimulus delivered to both ears

tap VEMPs Three Types of Recordings with Skull Tapper

FHLB Forehead head lift both sides recordedMHLL Mastoid head lift skull tapper located at leftMHLR Mastoid head lift skull tapper located at right

Conflict of Interests

The authors declare the following Dr Erdem Yavuz is aResearch Scientist at Research and Development IntelligentHearing Systems Inc andDr Rafael Delgado is the ExecutiveVice President and Director of Research and DevelopmentIntelligent Hearing Systems IncThe authors declare no otherconflict of interests related to this paper

References

[1] G von Bekesy ldquoUber akustische reizung des vestibularappa-ratesrdquo Pflugerrsquos Archiv fur die Gesamte Physiologie des Menschenund der Tiere vol 236 no 1 pp 59ndash76 1935

[2] J G Colebatch and G M Halmagyi ldquoVestibular evokedpotentials in human neck muscles before and after unilateralvestibular deafferentationrdquo Neurology vol 42 no 8 pp 1635ndash1636 1992

[3] J G Colebatch G M Halmagyi and N F Skuse ldquoMyogenicpotentials generated by a click-evoked vestibulocollic reflexrdquoJournal of Neurology Neurosurgery and Psychiatry vol 57 no2 pp 190ndash197 1994

[4] G M Halmagyi R A Yavor and J G Colebatch ldquoTapping thehead activates the vestibular system a new use for the clinicalreflex hammerrdquo Neurology vol 45 no 10 pp 1927ndash1929 1995

[5] K Sheykholeslami T Murofushi M H Kermany and KKaga ldquoBone-conducted evoked myogenic potentials from thesternocleidomastoid musclerdquo Acta Oto-Laryngologica vol 120no 6 pp 731ndash734 2000

[6] K Sheykholeslami M H Kermany and K Kaga ldquoFrequencysensitivity range of the saccule to bone-conducted stimulimeasured by vestibular evoked myogenic potentialsrdquo HearingResearch vol 160 no 1-2 pp 58ndash62 2001

[7] S R D Watson P Fagan and J G Colebatch ldquoGalvanicstimulation evokes short-latency EMG responses in sternoclei-domastoidwhich are abolished by selective vestibular nerve sec-tionrdquo Electroencephalography and Clinical NeurophysiologymdashElectromyography and Motor Control vol 109 no 6 pp 471ndash474 1998

[8] S R D Watson and J G Colebatch ldquoVestibular-evoked elec-tromyographic responses in soleus a comparison between clickand galvanic stimulationrdquo Experimental Brain Research vol 119no 4 pp 504ndash510 1998

[9] F Deriu E Tolu and J C Rothwell ldquoA sound-evoked vestibu-lomasseteric reflex in healthy humansrdquo Journal of Neurophysiol-ogy vol 93 no 5 pp 2739ndash2751 2005

[10] K Botzel P Feise O I Kolev S Krafczyk and T BrandtldquoErratum postural reflexes evoked by tapping forehead andchestrdquo Experimental Brain Research vol 140 no 2 p 251 2001

[11] S M Rosengren N P M Todd and J G ColebatchldquoVestibular-evoked extraocular potentials produced by stimula-tionwith bone-conducted soundrdquoClinical Neurophysiology vol116 no 8 pp 1938ndash1948 2005

[12] N P M Todd S M Rosengren S T Aw and J G ColebatchldquoOcular vestibular evoked myogenic potentials (OVEMPs)

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

Submit your manuscripts athttpwwwhindawicom

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

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Disease Markers

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BioMed Research International

OncologyJournal of

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Oxidative Medicine and Cellular Longevity

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PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Research and TreatmentAIDS

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Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 2: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

2 BioMed Research International

conducted via bone are propagated to a large region on theskull and may stimulate other parts of the vestibular organTherefore skull tapping is a more complex stimulus typelikely to result in activation of multiple sensors on both sidesof the head bilaterally activating the superior and inferiorvestibular nerves [23 24] Evidence strongly suggests that tapVEMPs to a significant extent are dependent on superiorbundle of vestibular nerve they are more often affected inpatients with vestibular neuritis (which usually affects onlythe superior vestibular nerve) in contrast to AC VEMP [25]It has been also reported that the tap VEMPs can be recordeddespite selective section of the inferior vestibular nerve [26]indicating that tap VEMPs strongly rely on the superiorvestibular nerve [23]

Initial tap VEMP studies were performed by using amanually controlled reflex hammer attached to a triggeringmechanism [4] Skull tapping via reflex hammer is prone todeliver varying amount of momentum with each individualhit to the test subject thus causing variability in the responseLater studies used mechanically controlled vibration andimpact generating devices for skull tapping in order tostandardize the amount of momentum delivered with eachtap [23 27 28] These devices are generally held by handagainst the impact site on the skull The forces delivered bythese devices are also prone to variability as the position onthe head and the hand position are likely to change duringthe recordings The major source of variability in VEMPrecordings is shown to be the contraction level of the musclethat is used as the electromyelography (EMG) source It hasbeen shown that the VEMP amplitude is directly related tothe strength of the background SCM muscle activity and isabsent at rest [3 29 30] In general duringVEMP recordingsthe subject is asked to push the head against a structureto ensure a certain amount of contraction in the cervicalmuscles [3] or asked to lie in supine position lifting theirheads up [4] or asked to turn their heads away from thestimulus [31] Although the abovementioned methods formuscle contraction can help tomaintainmuscle activity nonecan be used to guarantee a constant EMG activity range Toovercome this problem EMG-based biofeedback methodswere developed to increase the cooperation of the subjectsso that the subject can monitor and correct the contractionlevel of the muscle In this approach a muscle activity valueis calculated from the rectified EMG signals and displayed tothe subject as feedback [21 32]

VEMPs stand out as a promising tool in clinical practiceas they are noninvasive and easy to acquire with low time andinstrumentation cost Additionally when acquired togetherAC VEMPs and tap VEMPs may be used as a tool to identifythe functional integrity of inferior and superior vestibularnerves

Despite large amount of research onVEMPs and constantdevelopment of the instrumentation and methods for theclinical usage VEMPs and in particular tap VEMPs are stillnot well established clinically due to a number of issues Someof these issues are lack of a standardized tap VEMP specificdevice limited or no quantification on the delivered forceand instantaneous EMG activity lack of clinical experience

sensitivity specifications and also lack of established clinicalprotocol for the use of tap VEMPs

In this paper our main goal is to establish a clearrepeatable protocol for the clinical assessment of CPATcases geared by the recent developments in the objectivevestibular functional evaluation methods particularly thecomplimentary use of AC VEMPs and tap VEMPs in dailyclinical practice In our department VEMPs are part of aroutine testing on various vestibular problems particularlyon patients with cerebellopontine angle tumors (CPAT) Inthis study we present results of AC VEMP and tap VEMPrecordings acquired with the use of a new prototype auto-mated skull tapping device (Intelligent Hearing System IncMiami FL) that can be stabilized on the skull using a head-band that ensures a fixed placement and contact pressureAdditionally an EMG standardization method integratedinto the acquisition software is used to further minimizethe variability of the AC VEMP and tap VEMP recordingsThis paper describes our findings on 3-case examples froma growing patient data pool which will be presented in thefuture

2 Material and Methods

21 Clinical Investigation Protocol In our department whena patient is identified as a potential CPAT case our generalprotocol is to conduct a diagnostic battery on the patient byfollowing a diagnostic procedure for vestibular or acousticschwannoma [33] using the standard tests with the compli-mentary addition of AC VEMPs and tap VEMPs The orderof the tests in the following list reflects the escalation in thediagnosis towards a CPAT case

(1) Patient history(2) Otoscopy(3) Audiological assessment (particularly for signs of

compression reflecting the involvement of othernerves that share the same trajectory in the auditorycanal [34ndash36]) that involves pure tone audiome-try speech discrimination test impedance audiom-etry with stapedius reflex and auditory brainstemresponse (ABR)

(4) Examination of the patients by acquiring auditoryand skull tapping VEMPs according to the protocolthat will be described in detail below Due to thesensory organ dependency and related innervationsdifferences as mentioned above recording both theAC VEMPs and tap VEMPs further increases thepotential of identification of the affected nerve bun-dles For instance in cases where no or reduced ACVEMPs are observed but tap VEMPs are presenta nonfunctional inferior bundle but a functioningsuperior vestibular nerve can be estimated

(5) Themagnetic resonance imaging (MRI)with gadolin-ium enhancement is currently viewed as the mostaccurate diagnostic tool for VIII nerve schwannomacapable of identifying tumors as small as 3mm insize On the other hand it is quite costly and it is

BioMed Research International 3

not performed at the early stages of the diagnosticsprocedure In many countries where health servicesare rationed a clear indication of tumor presenceis necessary for scheduling an early MRI appoint-ment The MRI is performed if tests described aboveindicate the high suspicion of the CPAT accordingto cross-check rule In MRI tumor size location inthe internal auditory canal (which part of the canal)and brainstem compression if present are describedThis information is very helpful in consideration ofsurgery approach which depends on the size andlocation of the tumor and the degree of hearing loss

(6) Clinical and electrical examination of the facial nerveis performed to test the facial nerve involvement

(7) Surgical referral

While the MRI provides information on tumor presenceand its size and location in the internal auditory canal (whichpart of the canal) that are essential for the surgeon it does notprovide information about which nerve bundles are involvedin the process The information provided by ABR and ACVEMPS and tap VEMPs together is very useful for a surgeondue to the relationship of cochlear and vestibular nervesin the internal auditory canal The vestibulocochlear nervedivides into individual nerves in the lateral aspect of theinternal auditory canal cochlear nerve more anteriorly andboth vestibular nerves superior and inferior more posteriorly[34ndash36]The facial nerve courses anterior like cochlear nervebut remains more superior to it The nerves all togetherrotate 90 degrees in their course from the fundus of theinternal auditory canal to the cerebellopontine angle sothat the cochlear nerve rotates from anterior to posteriorbut stays most inferior [34] As the vestibulocochlear nervedivides into individual nerves the presence of a tumor canbe reflected by malfunctions of these nerves depending onwhich nerve the compression occurs

22 Acquisition of AC VEMPs and tap VEMPs All VEMPrecordings were conducted using surface electrodes placedon the skin above SCM muscle The positive electrodes wereplaced bilaterally on the midpoint of the SCM muscle mea-sured between the points where the muscle was connectedto the mastoid and the sternumThe negative electrodes werepositioned on the sternumand the SCM junctionThegroundelectrode was placed laterally on the zygomatic bone so thatthe placement of the skull tapper on the foreheadwas possiblefor tap VEMP recordings

All VEMPs were acquired using SmartEP evoked poten-tial acquisition system on the IHS USB Box platform(Intelligent Hearing Systems Inc Miami FL) Recordingswere performed with sampling period of 400ms with 5Kamplification filtered using a 6 dB per octave band passfilter with highpass cutoff set at 30Hz and lowpass cutoffset at 1500Hz The AC VEMPs were collected by averaging128 sweeps and tap VEMPs were acquired averaging 64sweeps Less number of sweeps was used for the tap VEMPsas skull tapping was found to generally generate largeramplitude responses compared to the auditory counterpart

For each recording site and type two sets of recordingswere made which were later averaged to increase the signalto noise ratio The two sets of recordings were used tomonitor the repeatability of the recorded signals The ACVEMPs were evoked by 5000ms long 500Hz tone burstsconditioned by an exact Blackman window delivered viaER3a ear insert phones (Etymotic Research Inc Elk GroveVillage IL) at 100 dBnHL The tap VEMPs were evokedby a prototype skull tapping device produced by IntelligentHearing Systems Corp The skull tapper was composedof an electromagnetic push type mechanism automaticallycontrolled by the software to deliver a controlled force witha hit onset detection mechanism The piston of the tapperwas held at the same position for 100ms following the hitat the surface interfacing the skull to ensure a unidirectionalforce delivery The delivered force was measured to be 105Nusing a commercially available artificial mastoid device (type4930) Bruel amp Kjaeligr (Naeligrum Denmark) Details on theskull tapper device will be described in a separate article Astimulation rate of 31s was used for both VEMP recordingtypesThe recording system uses an EMG-based biofeedbackmonitoring method to minimize the variation in the SCMmuscle contractions and thus the variation in the amplitudeof VEMPs This method is based on continuous monitoringof pre- and poststimulus EMG activity In this method twoconditions had to be fulfilled for a window of a recordingcycle to be accepted into the average (a) the root meanssquared (RMS) EMG activity had to fall into a range setby the user (generally minimum at 50120583V and maximum at150 120583V RMS) and (b) the poststimulus activity should notexceed a user set artifact rejection value If both cases weresatisfied an illustration of a smiling face was shown on themonitor to the patient (this would indicate to the patient thatthe SCMmuscle contraction was sufficient for recording andthat heshe should stay in this position to complete the set ofrecordings) In addition a green bar showing the actual EMGRMS levels was also presented When any of the conditionswas notmet the smiling facewas replaced by an upset face andthe EMG bar color was turned to red A secondary feedbackindicator box that contained a red and a green LED light wasalso present Both indicators were used to increase the patientcooperation with the SCMmuscle contraction and minimizethe muscle fatigue

The skull tapper was placed on the skull at three locations(a) at the midline on the forehead (b) behind the left earon the mastoid process and (c) behind the right ear on themastoid process The stabilization of the skull tapper wasensured using an adjustable head band

The recordings were performed with the patients com-fortably resting in a supine position and lifting the head uptowards midline The patients were directed to just lift thehead with no shoulder and abdominal muscle activity ifpossible During all recordings a researcher was present at alltimes directing the patient to increase or decrease the lift ofthe head or the turn movement to stay in the selected RMSEMG levels using the biofeedback monitor for guid ance

Three different types of recordings were conducted withAC VEMPs (two repetitions each)

4 BioMed Research International

AHLB MHLLMHLR

Head lift stimulation sites

Skull tapper side view

Skull tapper front view

Audio stimulus

AHLR AHLL FHL

Figure 1The stimulus presentations sites for the head lift recordingsmade for acoustic and skull tap VEMPs Abbreviations in the illustrationindicate the stimulus type and direction as follows (1) head lift stimulus delivered to the right ear (AHLR) (2) head lift stimulus deliveredto the left ear (AHLL) (3) head lift stimulus delivered to both ears (AHLB) (4) forehead head lift (FHL) (5) mastoid head lift skull tapperlocated at right (MHLR) (6) mastoid head lift skull tapper located at left (MHLL)

(1) head lift stimulus delivered to the left ear (AHLL)(2) head lift stimulus delivered to the right ear (AHLR)(3) head lift stimulus delivered to both ears (AHLB)

Three different types of recordingswere conducted for theskull tapping evokedVEMPs (two repetitions each)with skulltapper located at

(1) forehead head lift both sides recorded (FHLB)(2) mastoid head lift skull tapper located at left (MHLL)(3) mastoid head lift skull tapper located at right

(MHLR)

Therefore a total of 12 recordings were conducted for eachpatient (6 total typeswith two repetitions) before and after thesurgical intervention as shown in Figure 1

The recorded responses were normalized according tothe prestimulus (base) EMG RMS calculations Normalizedvalueswere used to assess the asymmetry ratios (AR) betweenthe left and right side measurements The usefulness of thenormalization of ARmeasurements is still under debate [37]The following equation (1) was used for the asymmetry ratiowhere the 119860

119871is the amplitude measure from the left side

recording between the first positive and first negative peakand similarly 119860

119877is the amplitudemeasured on the right side

Corrected AR of up to 35 is considered normal [38]

Asymmetry Ratio = 100100381610038161003816100381610038161003816100381610038161003816

(119860119871minus 119860119877)

(119860119871+ 119860119877)

100381610038161003816100381610038161003816100381610038161003816

(1)

During the course of this study additional VEMP record-ings were made where the SCM contraction was sustainedvia the head turn to the sides In this paper we only presentthe results and the details of the head lift data as we foundthe head turn method to be unreliable when analyzed via

asymmetry ratio approach We prefer and advocate the headlift approach as it is much easier to control and identify if apatientrsquos head is symmetrically lifted or not For this reasonwe believe that the VEMPs recorded via head lift are lessprone to be affected by the orientation differences of thevestibular organs during the recording sessions compared tohead turnwith the current instrumentation limits Additionalfeedback monitoring of the 3D positioning of the head byusing additionalmeans such as gyroscopes andor accelerom-eters could help to minimize this variability

23 Participating Patients Details

Patient Number 1 Patient number 1 was a 43-year-old manwho suffered from slight tinnitus and slight hearing loss inhis right ear with no vestibular problems prior to admis-sion Audiological tests revealed a small high-frequencysensorineural hearing loss on the right side with pure toneaverage (PTA) for 3 and 4 kHz = 35 dBHL The speech dis-crimination score at 60 dB was almost normal (80 scored100 at 70 dB) Impedance audiometry revealed normalmiddle ear function and normal stapedius reflex thresholdson both sides Normal response to click stimulus at 90 dBnHLwas present on the left side in ABR but on the right sideABR showed retrocochlear abnormality Vestibular calorictest and videonystagmography showed normal responseson both sides with no central vestibular disorders Detailson the VEMP recordings will be described in the Resultssection MRI revealed a tumor in the internal auditory canalthe tumor was 12 times 9mm in size Clinical and electricalexamination (using electromyography) of the right facialnerve revealed its normal function

Middle fossa approach was chosen for the surgeryattempting to preserve the hearing The tumor appeared to

BioMed Research International 5

arise from cochlear nerve and was attached to other nervesin the internal auditory canal

Patient Number 2 Patient number 2was a 51-year-oldwomanPrior to the admission she complained about tinnitus andhearing loss in the right ear with some symptoms of rightfacial nerve paresis Pure tone audiometry revealed sen-sorineural hearing loss on the right side with PTA for 05 and1 kHz = 30 dBHL and for 2 and 4 kHz = 575 dBHL and thespeech discrimination score at 60 dB was 30 for the rightear Normalmiddle ear functionwas provedwith tympanom-etry but stapedius reflexes were missed Normal response toclick stimulus at 90 dBnHLwas present on the left side inABRand no reproducible waves on the right Vestibular calorictest and videonystagmography revealed aflexia on the rightside with no central vestibular abnormalities and normalfunction on the left Clinical and electrical examination(electromyography) of the right facial nerve revealed itsabnormal function Details on the VEMP recordings will bedescribed in the results section MRI showed a 4 times 9mmtumor in the right internal ear canal

Middle fossa approach was selected to increase thepossibility of hearing preservationThe tumor seemed to arisefrom superior vestibular nerve but involved the inferior oneas well

Patient Number 3 Patient number 3 was a 26-year-oldwoman whose main complaint was tinnitus on the left sideAt the admission she stated not having any other hearingor vestibular problems Auditory testing revealed normalhearing in both ears in all audiometric frequencies withthe pure tone average for 05 1 2 and 4 kHz = 25 dB andspeech discrimination score at 60 dB was 100 Impedanceaudiometry revealed normal results Auditory brainstemresponse showed normal reproducible waves on both sidesVestibular caloric test and videonystagmography showednormal responses on both sides with no central vestibulardisorders Left facial nerve function was normal VEMPswill be discussed in the Results section Due to the patientrsquoshistory of asymmetric tinnitus and young age it was decidedto perform MRI The MRI revealed a tumor in the internalauditory canal the tumor was 7 times 5 times 15mm in size

For the surgery middle fossa approach was selected forthe hearing preservation The tumor seemed to arise fromsuperior vestibular nerve

This study is a part of a retrospective-prospective projectthat was approved by the Ethics Committee Review Boardat the Medical University of Warsaw where the VEMPsrecordings have been conducted The project conforms withThe Code of Ethics of the World Medical Association (Dec-laration of Helsinki)

3 Results

Table 1 shows AC VEMP and tap VEMP results with valuesfor P1 latencies and corrected amplitudes of the responsesalong with corrected asymmetry ratios Figure 2 presents theresults of the preoperative (preop) recordings acquired byboth VEMP techniques Figure 3 shows the change observed

between the preop and postoperative (postop) responsesrecorded from the ipsilateral side to the tumor

Patient Number 1 In this patient highly large correctedasymmetry ratio (AR) values for AC VEMPs (AHLB AR =4759 AHLL versus AHLR AR = 4543) were observedValues lower than 35 are considered normal [38] and weused them as referral In close inspection of the waveformsfrom the contralateral side one can easily see that the left sidestimulation producedmuch smaller activity on the right sidewhere the right side stimulation did not produce a similaractivity on the left side (Figure 2)

The tap VEMPs were symmetric for the forehead (FHLBAR = 1915) and for the mastoid skull tapping resultsrecorded from the ipsilateral side SCM (right MHLR versusleft MHLL AR = 1684)

The postop responses were compared with the preop data(Figure 3) The AC VEMPs results showed that P1 and N1disappeared when the ear ipsilateral to the tumor was stim-ulated In the bilaterally stimulated recordings we observedthe preservation of these peaks to an extent Considering thesurgical cut of the ipsilateral inferior bundle the preservationof the peaks suggested the contribution of the contralateralside Forehead placement tapVEMPs showed a reversal in therecorded P1-N1 peak complex In all of the above recordingsthe later waveforms observed between 25 and 60ms rangewhich are generally regarded as cochlear in origin [24 39]did not display a major change

Patient Number 2 Patient number 2 medical history alongwith unilateral sensorineural hearing loss poor speech recog-nition ABR VNG and facial nerve EMG results pointed toimpaired function of VIII and VII nerves on the right side

In AC VEMPs we observed drastic differences betweenleft and right side responses (AHLB AR = 4349) The rightside auditory stimulation failed to generate a response wherethe left side stimulation evoked a robust response (Figure 2)

Skull tapping the forehead and each mastoid resulted inlarge ARs (FHLB AR = 5760 MHLR versus MHLR AR =6132) Upon visual inspection of ipsilateral responses theinitial parts of thewaveformmorphology (P1-N1 region)weredifferent (Figure 2)

In the postop preop comparison (Figure 3) there wereno significant changes in any of the responses recordedipsilateral to the tumor in neither of the VEMP techniquesfor P1 and N1 peaks suggesting that both bundles had totalfunctional loss before the surgery Additionally similar tothe first patient late waveforms did not display a significantchange

Patient Number 3 In patient number 3 all audiologicalVNG and VEMP tests were within normal limits Due topatientrsquos young age and history of tinnitus on the left side thissuggested that there might be a retrocochlear problem

No asymmetry was observed in the AC VEMPs (AHLBAR = 1662 AHLR versus AHLL AR = 1995) and tapVEMPs (FHLB AR = 1718 MHLR versus MHLL AR= 1929) The mastoid ipsilateral tap VEMP recordingsshowed high similarity In this case both AC VEMP and

6 BioMed Research International

Table1Au

ditory

andskulltap

VEM

Phead

liftresults

Patie

ntAnalyzed

parameter

Headlift

Auditory

Tapp

ingforehead

Tapp

ingmastoidsIPS

Irespo

nses

AHLB

AR(

)

AHLL

AHLR

AR(

)

FHLB

AR(

)

MHLL

MHLR

AR(

)Re

spon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

1P1

latency

(ms)

1320

1340

1340

1420

1320

1440

1400

1440

Corram

plitu

de2556

908

4759lowast

2296

862

4543lowast

3624

2459

1915

3367

2397

1684

2P1

latency

(ms)

1400

1360

1460

NR

1440

1520

1720

1560

Corram

plitu

de1314

518

4349lowast

2351

NR

3322

894

5760lowast

3819

916

6132lowast

3P1

latency

(ms)

1260

1280

1280

1300

1400

1360

1440

1320

Corram

plitu

de1019

1414

1626

1962

2940

1995

4488

3172

1718

5823

3940

1929

AHLB

headlift

stimulus

delivered

tobo

thearsA

HLL

headlift

stimulus

delivered

totheleftearAHLR

headlift

stimulus

delivered

totherig

htearFH

LBForeheadHeadLiftskulltapperlocated

atforehead

MHLL

Mastoid

HeadLiftskulltapperlocatedat

Left

MHLR

Mastoid

HeadLiftskulltapperlocatedat

RightP1p

ositive

peakcorram

plitu

decorrected

amplitu

deS

CMsternocleidom

astoid

muscle

AR

Asymmetry

ratio

NR

norespon

seA

bnormalresults

ofcorrectedasym

metry

ratio

s(ARgt35)a

ndno

respon

seresults

(NR)

arem

arkedwithlowast

BioMed Research International 7

AHLR

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

AHLL

(a)

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

AHLR

AHLL

(b)

AHLB

AHLL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

AHLR

(c)

Figure 2 VEMP waveforms recorded from all 3 subjects All the waveforms are normalized according to prestimulus EMG activity In thisfigure left side recordings are plotted as solid lines while right side recordings are plotted as dashed lines Abbreviations are used in thisfigure as follows AHLB auditory head lift both ear stimulation recorded bilaterally AHLL auditory head lift left ear stimulation recordedbilaterally AHLR auditory head lift right ear stimulation recorded bilaterally FHLB head lift recording tapper located at forehead recordedbilaterally MHLL head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at rightmastoid recorded bilaterally

tap VEMP results failed to point to a tumor presence TheMRI showed a tumor in the left internal auditory canal(7 times 5 times 15mm) During the surgical intervention thetumor was identified as arising from the superior vestibularnerve

In the postop versus preop comparison (Figure 3) of thehead lift AC VEMP recordings no significant change onthe tumor side was found when both ears were stimulatedHowever significant difference was shown when the stim-ulation was at the side of pathology For the tap VEMP

8 BioMed Research International

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

(a)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

(b)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

(c)

Figure 3 Preop (solid lines) and postop (dashed lines) VEMP waveforms recorded ipsilateral to the pathology from all 3 subjects Allthe waveforms are normalized according to prestimulus EMG activity Abbreviations are used in this figure as follows where ipsilateralindicates the location in return to the pathology location AHLB ipsilateral auditory head lift recording with both ears stimulated AHLipsilateral auditory head lift recording in return to ipsilateral stimulation FHLB ipsilateral head lift recording tapper located at foreheadMHL ipsilateral head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at ipsilateralmastoid

P1 peak could not be identified in any of the recordingsand N1 peak amplitudes were diminished in all recordingsexcept for the forehead placement where N1 latency andamplitude were preserved In general more variability inlatency and amplitude was also present for the later waves aswell

4 Discussion

In todayrsquos audiovestibular clinical practice a large numberof tests are available to determine the functionality of theaudiovestibular system The selection and the use of thesetests are mostly limited by their selectivity practicality and

BioMed Research International 9

costs The rapid development of VEMP related research andour recent experience with AC VEMPs and tap VEMPs haveled us to use VEMPs as an integral part of our diagnosticbattery In our department we routinely use the cervicalVEMPs due to the longer history thus there is larger amountof accumulated research on cervical VEMPs Currently weare also investigating the use of relatively newer approachof ocular VEMPs and adding it to our collected data setAlthough the recent research on ocular VEMPs has beenencouraging for clinical usage the technique has to still berefined to be used as a routine test The cervical VEMPs areeasy to acquire and can be efficiently used with quantificationmethods for ongoing muscle activity monitoring such asthe one used in this study where acceptance and rejectionmuscle activity regions are used Our near feature planis to include the ocular VEMPs recording in our routinediagnostic tests ensuring that the adaptation of the muscleactivity quantification methods we use is properly utilized

Our results showed that the VEMP recordings werenot only capable of identifying the CPAT but were alsoable to contribute additional information of involved nervebundles in first patient The observed abnormal audiologicalfindings strongly suggested the initial diagnosis of vestibularschwannoma The MRI pointed to the presence of a tumorlocated in the right internal auditory canal VEMP results alsosupported the presence of a tumor additionally pointing tothe inferior vestibular nerve involvementThe surgery reportdescribed the tumor to be arising from cochlear nerve and tobe attached to the other nerves in the internal auditory canalThe cochlear nerve is located closer to the inferior bundle ofthe vestibular nerve [34ndash36] and compression on the inferiornerve therefore was affecting the AC VEMPs results but notaltering the proper function of the superior vestibular nerve(AR in tap VEMPs within normal limits [38])

For the second patient the audiological results alongwith VNG and VEMP results strongly suggested the tumorpresence in the internal auditory canal which was supportedby theMRI findingsThe surgeon described the tumor arisingfrom superior vestibular nerve involving the inferior bundleas well During the surgery the tumor was found to be biggerthan initially described by the MRI which was performed afew months before As routinely done prior to the surgerythe other tests including VEMPs were performed to decideon the surgical approach and determine the possibility forhearing preservation In this case the tumor affected thefunction of all the nerves in the internal auditory canal Ourconclusion from the AC VEMP and tap VEMP findings wasthe involvement of both the inferior and superior nervesThe VEMPs were successful in pointing out both the tumorpresence and the involvement of both of the vestibularnerves An interesting observation was that the left andright responses recorded during both right side and left sideauditory stimulation were highly similar suggesting that thewhole response seen in AHLBmight have been driven by theleft ear

The third patient was a particularly interesting casebecause all tests performed along with AC VEMPs and tapVEMPs proved to be not helpful in the diagnosis of thevestibular schwannoma Although the tumor was arising

from the superior vestibular nerve the tap VEMP failed toindicate presence of the tumor similar to the rest of theclinical tools suggesting a normal function In this case onlythe MRI was sensitive enough to show the tumor The MRIwas performed due to the history of the patient her youngage and our experience in vestibular schwannoma casesThereason why the recorded tap VEMPs were not able to detectthe pathology is a good question to investigate

We observed that the mastoid placement of the skulltapper created additional challenges It was extremely difficultto replicate the same conditions when the skull tapper wasplaced on a surface of the mastoid region Due to the 3-dimensional shape of the mastoid area it was very difficultto maintain a steady 3D relation between the head and theskull tapper hit axis (thus with the vestibule axis) especiallywhen tapper is moved from one side to the other As with thecurrent setup there was no chance of monitoring the relationbetween the skull tapper hit direction and the vestibularorgans and it was not possible to limit the introducedvariability In the light of these observations (although weacquired data with skull tapper positioned at mastoids onboth sides and described the results of the responses acquiredfrom the ipsilateral SMCs) we preferred to relay and advocatethe usage of the forehead stimulation results due to the limitsof currently available instrumentation The directional infor-mation revealed by themastoid placement is complex and hasto be carefully analyzed For general clinical implementationadditional safeguards are required An additional feedbackmechanism describing the orientation relation between thetapper and gravity such as a gyroscope could be helpfulin minimizing the variability and thus could be useful inproducing equivalent directional force delivery to each sidewhen skull tapper is moved from left to right

5 Conclusions

In this paper we introduced our efforts in adding the ACVEMPs and tapVEMPs to expend the clinical diagnostic testsused for advanced assessment in CPAT patients hoping thatit will serve as a guideline for other clinicians interested inutilizing tap VEMPs

The patients presented in this study were selected topoint out different results we observed among a larger patientpopulation The findings from the larger population groupwill be presented in a more detailed follow-up subsequentpaper The main goal of this paper was to focus on theprotocol used and point at the variability in the findings

In two of three presented cases AC VEMPs and tapVEMPs together proved to be helpful in establishing thediagnosis of CPAT providingmore information on the tumoraffected bundle of vestibular nerve (superior or inferior orboth) Performing only AC VEMPs or only tap VEMPswould have provided insufficient information about thetumor and the vestibular nerve bundle involvement Inthe third case VEMPs failed to identify the vestibularschwannoma which was clearly shown in MRI scans Inthis case our medical intuition and expertise with CPATpatients prompted us to perform MRI Due to the high cost

10 BioMed Research International

of MRI it is typically not performed at the early stages ofthe diagnostics procedure in many countries Once othertests indicate the possible presence of the CPAT an MRI isconducted

Providing AC VEMPs and tap VEMPs to the availabletest battery in the assessment of CPAT is likely to improvethe diagnostic process by providing more information onthe involved vestibular nerve bundles In addition thisinformation might be used later during the surgery In manycases theMRI is not performed very short before the surgeryUsually it is performed earlier during the diagnostic processThe surgery takes place sometime after Asmentioned beforethe MRI is quite costly and usually is not performed againif not much time passed However the ABR AC VEMPsand tap VEMP once performed in diagnostic proceedingmight be repeated short before the surgery to clarify thepresence along with possible compression characteristics ofthe tumor on the vestibular andor auditory nerves Thiscombined information from earlier MRI scans and latestelectrophysiological tests serves the surgeons as a guidelinein their surgical approach and during tumor removal Itprovides very useful information for the surgeon in makinga decision about additional intraoperative monitoring ofhearing In our department intraoperative monitoring isroutinely used in every CPAT surgery and many otherear surgeries but intraoperative hearing monitoring is notroutinely performed in most of the other clinics In additionthe details from electrophysiological tests about the involvednerve bundles are useful in patients counseling and informingthem on more realistic possible outcomes of the surgery likehearing preservations possibilities and a risk of hearing lossduring the surgery a risk of facial nerve paresis and vertigosymptoms after the surgery

Abbreviations

ABR Auditory brainstem responseAS Asymmetry ratioCPAT Cerebellopontine angle tumorECochG ElectrocochleographyEEG ElectroencephalographyEMG ElectromiographyMRI Magnetic resonance imagingPTA Pure tone averageRMS Root means squaredSCM SternocleidomastoidVEMP Vestibular Evoked Myogenic PotentialAC VEMP Auditory Vestibular Evoked Myogenic

Potentialtap VEMP Skull tapping induced Vestibular

Evoked Myogenic Potential

AC VEMPsThree Types of Recordings

AHLL Head lift stimulus delivered to the left earAHLR Head lift stimulus delivered to the right earAHLB Head lift stimulus delivered to both ears

tap VEMPs Three Types of Recordings with Skull Tapper

FHLB Forehead head lift both sides recordedMHLL Mastoid head lift skull tapper located at leftMHLR Mastoid head lift skull tapper located at right

Conflict of Interests

The authors declare the following Dr Erdem Yavuz is aResearch Scientist at Research and Development IntelligentHearing Systems Inc andDr Rafael Delgado is the ExecutiveVice President and Director of Research and DevelopmentIntelligent Hearing Systems IncThe authors declare no otherconflict of interests related to this paper

References

[1] G von Bekesy ldquoUber akustische reizung des vestibularappa-ratesrdquo Pflugerrsquos Archiv fur die Gesamte Physiologie des Menschenund der Tiere vol 236 no 1 pp 59ndash76 1935

[2] J G Colebatch and G M Halmagyi ldquoVestibular evokedpotentials in human neck muscles before and after unilateralvestibular deafferentationrdquo Neurology vol 42 no 8 pp 1635ndash1636 1992

[3] J G Colebatch G M Halmagyi and N F Skuse ldquoMyogenicpotentials generated by a click-evoked vestibulocollic reflexrdquoJournal of Neurology Neurosurgery and Psychiatry vol 57 no2 pp 190ndash197 1994

[4] G M Halmagyi R A Yavor and J G Colebatch ldquoTapping thehead activates the vestibular system a new use for the clinicalreflex hammerrdquo Neurology vol 45 no 10 pp 1927ndash1929 1995

[5] K Sheykholeslami T Murofushi M H Kermany and KKaga ldquoBone-conducted evoked myogenic potentials from thesternocleidomastoid musclerdquo Acta Oto-Laryngologica vol 120no 6 pp 731ndash734 2000

[6] K Sheykholeslami M H Kermany and K Kaga ldquoFrequencysensitivity range of the saccule to bone-conducted stimulimeasured by vestibular evoked myogenic potentialsrdquo HearingResearch vol 160 no 1-2 pp 58ndash62 2001

[7] S R D Watson P Fagan and J G Colebatch ldquoGalvanicstimulation evokes short-latency EMG responses in sternoclei-domastoidwhich are abolished by selective vestibular nerve sec-tionrdquo Electroencephalography and Clinical NeurophysiologymdashElectromyography and Motor Control vol 109 no 6 pp 471ndash474 1998

[8] S R D Watson and J G Colebatch ldquoVestibular-evoked elec-tromyographic responses in soleus a comparison between clickand galvanic stimulationrdquo Experimental Brain Research vol 119no 4 pp 504ndash510 1998

[9] F Deriu E Tolu and J C Rothwell ldquoA sound-evoked vestibu-lomasseteric reflex in healthy humansrdquo Journal of Neurophysiol-ogy vol 93 no 5 pp 2739ndash2751 2005

[10] K Botzel P Feise O I Kolev S Krafczyk and T BrandtldquoErratum postural reflexes evoked by tapping forehead andchestrdquo Experimental Brain Research vol 140 no 2 p 251 2001

[11] S M Rosengren N P M Todd and J G ColebatchldquoVestibular-evoked extraocular potentials produced by stimula-tionwith bone-conducted soundrdquoClinical Neurophysiology vol116 no 8 pp 1938ndash1948 2005

[12] N P M Todd S M Rosengren S T Aw and J G ColebatchldquoOcular vestibular evoked myogenic potentials (OVEMPs)

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

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Disease Markers

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Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Research and TreatmentAIDS

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 3: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

BioMed Research International 3

not performed at the early stages of the diagnosticsprocedure In many countries where health servicesare rationed a clear indication of tumor presenceis necessary for scheduling an early MRI appoint-ment The MRI is performed if tests described aboveindicate the high suspicion of the CPAT accordingto cross-check rule In MRI tumor size location inthe internal auditory canal (which part of the canal)and brainstem compression if present are describedThis information is very helpful in consideration ofsurgery approach which depends on the size andlocation of the tumor and the degree of hearing loss

(6) Clinical and electrical examination of the facial nerveis performed to test the facial nerve involvement

(7) Surgical referral

While the MRI provides information on tumor presenceand its size and location in the internal auditory canal (whichpart of the canal) that are essential for the surgeon it does notprovide information about which nerve bundles are involvedin the process The information provided by ABR and ACVEMPS and tap VEMPs together is very useful for a surgeondue to the relationship of cochlear and vestibular nervesin the internal auditory canal The vestibulocochlear nervedivides into individual nerves in the lateral aspect of theinternal auditory canal cochlear nerve more anteriorly andboth vestibular nerves superior and inferior more posteriorly[34ndash36]The facial nerve courses anterior like cochlear nervebut remains more superior to it The nerves all togetherrotate 90 degrees in their course from the fundus of theinternal auditory canal to the cerebellopontine angle sothat the cochlear nerve rotates from anterior to posteriorbut stays most inferior [34] As the vestibulocochlear nervedivides into individual nerves the presence of a tumor canbe reflected by malfunctions of these nerves depending onwhich nerve the compression occurs

22 Acquisition of AC VEMPs and tap VEMPs All VEMPrecordings were conducted using surface electrodes placedon the skin above SCM muscle The positive electrodes wereplaced bilaterally on the midpoint of the SCM muscle mea-sured between the points where the muscle was connectedto the mastoid and the sternumThe negative electrodes werepositioned on the sternumand the SCM junctionThegroundelectrode was placed laterally on the zygomatic bone so thatthe placement of the skull tapper on the foreheadwas possiblefor tap VEMP recordings

All VEMPs were acquired using SmartEP evoked poten-tial acquisition system on the IHS USB Box platform(Intelligent Hearing Systems Inc Miami FL) Recordingswere performed with sampling period of 400ms with 5Kamplification filtered using a 6 dB per octave band passfilter with highpass cutoff set at 30Hz and lowpass cutoffset at 1500Hz The AC VEMPs were collected by averaging128 sweeps and tap VEMPs were acquired averaging 64sweeps Less number of sweeps was used for the tap VEMPsas skull tapping was found to generally generate largeramplitude responses compared to the auditory counterpart

For each recording site and type two sets of recordingswere made which were later averaged to increase the signalto noise ratio The two sets of recordings were used tomonitor the repeatability of the recorded signals The ACVEMPs were evoked by 5000ms long 500Hz tone burstsconditioned by an exact Blackman window delivered viaER3a ear insert phones (Etymotic Research Inc Elk GroveVillage IL) at 100 dBnHL The tap VEMPs were evokedby a prototype skull tapping device produced by IntelligentHearing Systems Corp The skull tapper was composedof an electromagnetic push type mechanism automaticallycontrolled by the software to deliver a controlled force witha hit onset detection mechanism The piston of the tapperwas held at the same position for 100ms following the hitat the surface interfacing the skull to ensure a unidirectionalforce delivery The delivered force was measured to be 105Nusing a commercially available artificial mastoid device (type4930) Bruel amp Kjaeligr (Naeligrum Denmark) Details on theskull tapper device will be described in a separate article Astimulation rate of 31s was used for both VEMP recordingtypesThe recording system uses an EMG-based biofeedbackmonitoring method to minimize the variation in the SCMmuscle contractions and thus the variation in the amplitudeof VEMPs This method is based on continuous monitoringof pre- and poststimulus EMG activity In this method twoconditions had to be fulfilled for a window of a recordingcycle to be accepted into the average (a) the root meanssquared (RMS) EMG activity had to fall into a range setby the user (generally minimum at 50120583V and maximum at150 120583V RMS) and (b) the poststimulus activity should notexceed a user set artifact rejection value If both cases weresatisfied an illustration of a smiling face was shown on themonitor to the patient (this would indicate to the patient thatthe SCMmuscle contraction was sufficient for recording andthat heshe should stay in this position to complete the set ofrecordings) In addition a green bar showing the actual EMGRMS levels was also presented When any of the conditionswas notmet the smiling facewas replaced by an upset face andthe EMG bar color was turned to red A secondary feedbackindicator box that contained a red and a green LED light wasalso present Both indicators were used to increase the patientcooperation with the SCMmuscle contraction and minimizethe muscle fatigue

The skull tapper was placed on the skull at three locations(a) at the midline on the forehead (b) behind the left earon the mastoid process and (c) behind the right ear on themastoid process The stabilization of the skull tapper wasensured using an adjustable head band

The recordings were performed with the patients com-fortably resting in a supine position and lifting the head uptowards midline The patients were directed to just lift thehead with no shoulder and abdominal muscle activity ifpossible During all recordings a researcher was present at alltimes directing the patient to increase or decrease the lift ofthe head or the turn movement to stay in the selected RMSEMG levels using the biofeedback monitor for guid ance

Three different types of recordings were conducted withAC VEMPs (two repetitions each)

4 BioMed Research International

AHLB MHLLMHLR

Head lift stimulation sites

Skull tapper side view

Skull tapper front view

Audio stimulus

AHLR AHLL FHL

Figure 1The stimulus presentations sites for the head lift recordingsmade for acoustic and skull tap VEMPs Abbreviations in the illustrationindicate the stimulus type and direction as follows (1) head lift stimulus delivered to the right ear (AHLR) (2) head lift stimulus deliveredto the left ear (AHLL) (3) head lift stimulus delivered to both ears (AHLB) (4) forehead head lift (FHL) (5) mastoid head lift skull tapperlocated at right (MHLR) (6) mastoid head lift skull tapper located at left (MHLL)

(1) head lift stimulus delivered to the left ear (AHLL)(2) head lift stimulus delivered to the right ear (AHLR)(3) head lift stimulus delivered to both ears (AHLB)

Three different types of recordingswere conducted for theskull tapping evokedVEMPs (two repetitions each)with skulltapper located at

(1) forehead head lift both sides recorded (FHLB)(2) mastoid head lift skull tapper located at left (MHLL)(3) mastoid head lift skull tapper located at right

(MHLR)

Therefore a total of 12 recordings were conducted for eachpatient (6 total typeswith two repetitions) before and after thesurgical intervention as shown in Figure 1

The recorded responses were normalized according tothe prestimulus (base) EMG RMS calculations Normalizedvalueswere used to assess the asymmetry ratios (AR) betweenthe left and right side measurements The usefulness of thenormalization of ARmeasurements is still under debate [37]The following equation (1) was used for the asymmetry ratiowhere the 119860

119871is the amplitude measure from the left side

recording between the first positive and first negative peakand similarly 119860

119877is the amplitudemeasured on the right side

Corrected AR of up to 35 is considered normal [38]

Asymmetry Ratio = 100100381610038161003816100381610038161003816100381610038161003816

(119860119871minus 119860119877)

(119860119871+ 119860119877)

100381610038161003816100381610038161003816100381610038161003816

(1)

During the course of this study additional VEMP record-ings were made where the SCM contraction was sustainedvia the head turn to the sides In this paper we only presentthe results and the details of the head lift data as we foundthe head turn method to be unreliable when analyzed via

asymmetry ratio approach We prefer and advocate the headlift approach as it is much easier to control and identify if apatientrsquos head is symmetrically lifted or not For this reasonwe believe that the VEMPs recorded via head lift are lessprone to be affected by the orientation differences of thevestibular organs during the recording sessions compared tohead turnwith the current instrumentation limits Additionalfeedback monitoring of the 3D positioning of the head byusing additionalmeans such as gyroscopes andor accelerom-eters could help to minimize this variability

23 Participating Patients Details

Patient Number 1 Patient number 1 was a 43-year-old manwho suffered from slight tinnitus and slight hearing loss inhis right ear with no vestibular problems prior to admis-sion Audiological tests revealed a small high-frequencysensorineural hearing loss on the right side with pure toneaverage (PTA) for 3 and 4 kHz = 35 dBHL The speech dis-crimination score at 60 dB was almost normal (80 scored100 at 70 dB) Impedance audiometry revealed normalmiddle ear function and normal stapedius reflex thresholdson both sides Normal response to click stimulus at 90 dBnHLwas present on the left side in ABR but on the right sideABR showed retrocochlear abnormality Vestibular calorictest and videonystagmography showed normal responseson both sides with no central vestibular disorders Detailson the VEMP recordings will be described in the Resultssection MRI revealed a tumor in the internal auditory canalthe tumor was 12 times 9mm in size Clinical and electricalexamination (using electromyography) of the right facialnerve revealed its normal function

Middle fossa approach was chosen for the surgeryattempting to preserve the hearing The tumor appeared to

BioMed Research International 5

arise from cochlear nerve and was attached to other nervesin the internal auditory canal

Patient Number 2 Patient number 2was a 51-year-oldwomanPrior to the admission she complained about tinnitus andhearing loss in the right ear with some symptoms of rightfacial nerve paresis Pure tone audiometry revealed sen-sorineural hearing loss on the right side with PTA for 05 and1 kHz = 30 dBHL and for 2 and 4 kHz = 575 dBHL and thespeech discrimination score at 60 dB was 30 for the rightear Normalmiddle ear functionwas provedwith tympanom-etry but stapedius reflexes were missed Normal response toclick stimulus at 90 dBnHLwas present on the left side inABRand no reproducible waves on the right Vestibular calorictest and videonystagmography revealed aflexia on the rightside with no central vestibular abnormalities and normalfunction on the left Clinical and electrical examination(electromyography) of the right facial nerve revealed itsabnormal function Details on the VEMP recordings will bedescribed in the results section MRI showed a 4 times 9mmtumor in the right internal ear canal

Middle fossa approach was selected to increase thepossibility of hearing preservationThe tumor seemed to arisefrom superior vestibular nerve but involved the inferior oneas well

Patient Number 3 Patient number 3 was a 26-year-oldwoman whose main complaint was tinnitus on the left sideAt the admission she stated not having any other hearingor vestibular problems Auditory testing revealed normalhearing in both ears in all audiometric frequencies withthe pure tone average for 05 1 2 and 4 kHz = 25 dB andspeech discrimination score at 60 dB was 100 Impedanceaudiometry revealed normal results Auditory brainstemresponse showed normal reproducible waves on both sidesVestibular caloric test and videonystagmography showednormal responses on both sides with no central vestibulardisorders Left facial nerve function was normal VEMPswill be discussed in the Results section Due to the patientrsquoshistory of asymmetric tinnitus and young age it was decidedto perform MRI The MRI revealed a tumor in the internalauditory canal the tumor was 7 times 5 times 15mm in size

For the surgery middle fossa approach was selected forthe hearing preservation The tumor seemed to arise fromsuperior vestibular nerve

This study is a part of a retrospective-prospective projectthat was approved by the Ethics Committee Review Boardat the Medical University of Warsaw where the VEMPsrecordings have been conducted The project conforms withThe Code of Ethics of the World Medical Association (Dec-laration of Helsinki)

3 Results

Table 1 shows AC VEMP and tap VEMP results with valuesfor P1 latencies and corrected amplitudes of the responsesalong with corrected asymmetry ratios Figure 2 presents theresults of the preoperative (preop) recordings acquired byboth VEMP techniques Figure 3 shows the change observed

between the preop and postoperative (postop) responsesrecorded from the ipsilateral side to the tumor

Patient Number 1 In this patient highly large correctedasymmetry ratio (AR) values for AC VEMPs (AHLB AR =4759 AHLL versus AHLR AR = 4543) were observedValues lower than 35 are considered normal [38] and weused them as referral In close inspection of the waveformsfrom the contralateral side one can easily see that the left sidestimulation producedmuch smaller activity on the right sidewhere the right side stimulation did not produce a similaractivity on the left side (Figure 2)

The tap VEMPs were symmetric for the forehead (FHLBAR = 1915) and for the mastoid skull tapping resultsrecorded from the ipsilateral side SCM (right MHLR versusleft MHLL AR = 1684)

The postop responses were compared with the preop data(Figure 3) The AC VEMPs results showed that P1 and N1disappeared when the ear ipsilateral to the tumor was stim-ulated In the bilaterally stimulated recordings we observedthe preservation of these peaks to an extent Considering thesurgical cut of the ipsilateral inferior bundle the preservationof the peaks suggested the contribution of the contralateralside Forehead placement tapVEMPs showed a reversal in therecorded P1-N1 peak complex In all of the above recordingsthe later waveforms observed between 25 and 60ms rangewhich are generally regarded as cochlear in origin [24 39]did not display a major change

Patient Number 2 Patient number 2 medical history alongwith unilateral sensorineural hearing loss poor speech recog-nition ABR VNG and facial nerve EMG results pointed toimpaired function of VIII and VII nerves on the right side

In AC VEMPs we observed drastic differences betweenleft and right side responses (AHLB AR = 4349) The rightside auditory stimulation failed to generate a response wherethe left side stimulation evoked a robust response (Figure 2)

Skull tapping the forehead and each mastoid resulted inlarge ARs (FHLB AR = 5760 MHLR versus MHLR AR =6132) Upon visual inspection of ipsilateral responses theinitial parts of thewaveformmorphology (P1-N1 region)weredifferent (Figure 2)

In the postop preop comparison (Figure 3) there wereno significant changes in any of the responses recordedipsilateral to the tumor in neither of the VEMP techniquesfor P1 and N1 peaks suggesting that both bundles had totalfunctional loss before the surgery Additionally similar tothe first patient late waveforms did not display a significantchange

Patient Number 3 In patient number 3 all audiologicalVNG and VEMP tests were within normal limits Due topatientrsquos young age and history of tinnitus on the left side thissuggested that there might be a retrocochlear problem

No asymmetry was observed in the AC VEMPs (AHLBAR = 1662 AHLR versus AHLL AR = 1995) and tapVEMPs (FHLB AR = 1718 MHLR versus MHLL AR= 1929) The mastoid ipsilateral tap VEMP recordingsshowed high similarity In this case both AC VEMP and

6 BioMed Research International

Table1Au

ditory

andskulltap

VEM

Phead

liftresults

Patie

ntAnalyzed

parameter

Headlift

Auditory

Tapp

ingforehead

Tapp

ingmastoidsIPS

Irespo

nses

AHLB

AR(

)

AHLL

AHLR

AR(

)

FHLB

AR(

)

MHLL

MHLR

AR(

)Re

spon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

1P1

latency

(ms)

1320

1340

1340

1420

1320

1440

1400

1440

Corram

plitu

de2556

908

4759lowast

2296

862

4543lowast

3624

2459

1915

3367

2397

1684

2P1

latency

(ms)

1400

1360

1460

NR

1440

1520

1720

1560

Corram

plitu

de1314

518

4349lowast

2351

NR

3322

894

5760lowast

3819

916

6132lowast

3P1

latency

(ms)

1260

1280

1280

1300

1400

1360

1440

1320

Corram

plitu

de1019

1414

1626

1962

2940

1995

4488

3172

1718

5823

3940

1929

AHLB

headlift

stimulus

delivered

tobo

thearsA

HLL

headlift

stimulus

delivered

totheleftearAHLR

headlift

stimulus

delivered

totherig

htearFH

LBForeheadHeadLiftskulltapperlocated

atforehead

MHLL

Mastoid

HeadLiftskulltapperlocatedat

Left

MHLR

Mastoid

HeadLiftskulltapperlocatedat

RightP1p

ositive

peakcorram

plitu

decorrected

amplitu

deS

CMsternocleidom

astoid

muscle

AR

Asymmetry

ratio

NR

norespon

seA

bnormalresults

ofcorrectedasym

metry

ratio

s(ARgt35)a

ndno

respon

seresults

(NR)

arem

arkedwithlowast

BioMed Research International 7

AHLR

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

AHLL

(a)

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

AHLR

AHLL

(b)

AHLB

AHLL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

AHLR

(c)

Figure 2 VEMP waveforms recorded from all 3 subjects All the waveforms are normalized according to prestimulus EMG activity In thisfigure left side recordings are plotted as solid lines while right side recordings are plotted as dashed lines Abbreviations are used in thisfigure as follows AHLB auditory head lift both ear stimulation recorded bilaterally AHLL auditory head lift left ear stimulation recordedbilaterally AHLR auditory head lift right ear stimulation recorded bilaterally FHLB head lift recording tapper located at forehead recordedbilaterally MHLL head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at rightmastoid recorded bilaterally

tap VEMP results failed to point to a tumor presence TheMRI showed a tumor in the left internal auditory canal(7 times 5 times 15mm) During the surgical intervention thetumor was identified as arising from the superior vestibularnerve

In the postop versus preop comparison (Figure 3) of thehead lift AC VEMP recordings no significant change onthe tumor side was found when both ears were stimulatedHowever significant difference was shown when the stim-ulation was at the side of pathology For the tap VEMP

8 BioMed Research International

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

(a)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

(b)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

(c)

Figure 3 Preop (solid lines) and postop (dashed lines) VEMP waveforms recorded ipsilateral to the pathology from all 3 subjects Allthe waveforms are normalized according to prestimulus EMG activity Abbreviations are used in this figure as follows where ipsilateralindicates the location in return to the pathology location AHLB ipsilateral auditory head lift recording with both ears stimulated AHLipsilateral auditory head lift recording in return to ipsilateral stimulation FHLB ipsilateral head lift recording tapper located at foreheadMHL ipsilateral head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at ipsilateralmastoid

P1 peak could not be identified in any of the recordingsand N1 peak amplitudes were diminished in all recordingsexcept for the forehead placement where N1 latency andamplitude were preserved In general more variability inlatency and amplitude was also present for the later waves aswell

4 Discussion

In todayrsquos audiovestibular clinical practice a large numberof tests are available to determine the functionality of theaudiovestibular system The selection and the use of thesetests are mostly limited by their selectivity practicality and

BioMed Research International 9

costs The rapid development of VEMP related research andour recent experience with AC VEMPs and tap VEMPs haveled us to use VEMPs as an integral part of our diagnosticbattery In our department we routinely use the cervicalVEMPs due to the longer history thus there is larger amountof accumulated research on cervical VEMPs Currently weare also investigating the use of relatively newer approachof ocular VEMPs and adding it to our collected data setAlthough the recent research on ocular VEMPs has beenencouraging for clinical usage the technique has to still berefined to be used as a routine test The cervical VEMPs areeasy to acquire and can be efficiently used with quantificationmethods for ongoing muscle activity monitoring such asthe one used in this study where acceptance and rejectionmuscle activity regions are used Our near feature planis to include the ocular VEMPs recording in our routinediagnostic tests ensuring that the adaptation of the muscleactivity quantification methods we use is properly utilized

Our results showed that the VEMP recordings werenot only capable of identifying the CPAT but were alsoable to contribute additional information of involved nervebundles in first patient The observed abnormal audiologicalfindings strongly suggested the initial diagnosis of vestibularschwannoma The MRI pointed to the presence of a tumorlocated in the right internal auditory canal VEMP results alsosupported the presence of a tumor additionally pointing tothe inferior vestibular nerve involvementThe surgery reportdescribed the tumor to be arising from cochlear nerve and tobe attached to the other nerves in the internal auditory canalThe cochlear nerve is located closer to the inferior bundle ofthe vestibular nerve [34ndash36] and compression on the inferiornerve therefore was affecting the AC VEMPs results but notaltering the proper function of the superior vestibular nerve(AR in tap VEMPs within normal limits [38])

For the second patient the audiological results alongwith VNG and VEMP results strongly suggested the tumorpresence in the internal auditory canal which was supportedby theMRI findingsThe surgeon described the tumor arisingfrom superior vestibular nerve involving the inferior bundleas well During the surgery the tumor was found to be biggerthan initially described by the MRI which was performed afew months before As routinely done prior to the surgerythe other tests including VEMPs were performed to decideon the surgical approach and determine the possibility forhearing preservation In this case the tumor affected thefunction of all the nerves in the internal auditory canal Ourconclusion from the AC VEMP and tap VEMP findings wasthe involvement of both the inferior and superior nervesThe VEMPs were successful in pointing out both the tumorpresence and the involvement of both of the vestibularnerves An interesting observation was that the left andright responses recorded during both right side and left sideauditory stimulation were highly similar suggesting that thewhole response seen in AHLBmight have been driven by theleft ear

The third patient was a particularly interesting casebecause all tests performed along with AC VEMPs and tapVEMPs proved to be not helpful in the diagnosis of thevestibular schwannoma Although the tumor was arising

from the superior vestibular nerve the tap VEMP failed toindicate presence of the tumor similar to the rest of theclinical tools suggesting a normal function In this case onlythe MRI was sensitive enough to show the tumor The MRIwas performed due to the history of the patient her youngage and our experience in vestibular schwannoma casesThereason why the recorded tap VEMPs were not able to detectthe pathology is a good question to investigate

We observed that the mastoid placement of the skulltapper created additional challenges It was extremely difficultto replicate the same conditions when the skull tapper wasplaced on a surface of the mastoid region Due to the 3-dimensional shape of the mastoid area it was very difficultto maintain a steady 3D relation between the head and theskull tapper hit axis (thus with the vestibule axis) especiallywhen tapper is moved from one side to the other As with thecurrent setup there was no chance of monitoring the relationbetween the skull tapper hit direction and the vestibularorgans and it was not possible to limit the introducedvariability In the light of these observations (although weacquired data with skull tapper positioned at mastoids onboth sides and described the results of the responses acquiredfrom the ipsilateral SMCs) we preferred to relay and advocatethe usage of the forehead stimulation results due to the limitsof currently available instrumentation The directional infor-mation revealed by themastoid placement is complex and hasto be carefully analyzed For general clinical implementationadditional safeguards are required An additional feedbackmechanism describing the orientation relation between thetapper and gravity such as a gyroscope could be helpfulin minimizing the variability and thus could be useful inproducing equivalent directional force delivery to each sidewhen skull tapper is moved from left to right

5 Conclusions

In this paper we introduced our efforts in adding the ACVEMPs and tapVEMPs to expend the clinical diagnostic testsused for advanced assessment in CPAT patients hoping thatit will serve as a guideline for other clinicians interested inutilizing tap VEMPs

The patients presented in this study were selected topoint out different results we observed among a larger patientpopulation The findings from the larger population groupwill be presented in a more detailed follow-up subsequentpaper The main goal of this paper was to focus on theprotocol used and point at the variability in the findings

In two of three presented cases AC VEMPs and tapVEMPs together proved to be helpful in establishing thediagnosis of CPAT providingmore information on the tumoraffected bundle of vestibular nerve (superior or inferior orboth) Performing only AC VEMPs or only tap VEMPswould have provided insufficient information about thetumor and the vestibular nerve bundle involvement Inthe third case VEMPs failed to identify the vestibularschwannoma which was clearly shown in MRI scans Inthis case our medical intuition and expertise with CPATpatients prompted us to perform MRI Due to the high cost

10 BioMed Research International

of MRI it is typically not performed at the early stages ofthe diagnostics procedure in many countries Once othertests indicate the possible presence of the CPAT an MRI isconducted

Providing AC VEMPs and tap VEMPs to the availabletest battery in the assessment of CPAT is likely to improvethe diagnostic process by providing more information onthe involved vestibular nerve bundles In addition thisinformation might be used later during the surgery In manycases theMRI is not performed very short before the surgeryUsually it is performed earlier during the diagnostic processThe surgery takes place sometime after Asmentioned beforethe MRI is quite costly and usually is not performed againif not much time passed However the ABR AC VEMPsand tap VEMP once performed in diagnostic proceedingmight be repeated short before the surgery to clarify thepresence along with possible compression characteristics ofthe tumor on the vestibular andor auditory nerves Thiscombined information from earlier MRI scans and latestelectrophysiological tests serves the surgeons as a guidelinein their surgical approach and during tumor removal Itprovides very useful information for the surgeon in makinga decision about additional intraoperative monitoring ofhearing In our department intraoperative monitoring isroutinely used in every CPAT surgery and many otherear surgeries but intraoperative hearing monitoring is notroutinely performed in most of the other clinics In additionthe details from electrophysiological tests about the involvednerve bundles are useful in patients counseling and informingthem on more realistic possible outcomes of the surgery likehearing preservations possibilities and a risk of hearing lossduring the surgery a risk of facial nerve paresis and vertigosymptoms after the surgery

Abbreviations

ABR Auditory brainstem responseAS Asymmetry ratioCPAT Cerebellopontine angle tumorECochG ElectrocochleographyEEG ElectroencephalographyEMG ElectromiographyMRI Magnetic resonance imagingPTA Pure tone averageRMS Root means squaredSCM SternocleidomastoidVEMP Vestibular Evoked Myogenic PotentialAC VEMP Auditory Vestibular Evoked Myogenic

Potentialtap VEMP Skull tapping induced Vestibular

Evoked Myogenic Potential

AC VEMPsThree Types of Recordings

AHLL Head lift stimulus delivered to the left earAHLR Head lift stimulus delivered to the right earAHLB Head lift stimulus delivered to both ears

tap VEMPs Three Types of Recordings with Skull Tapper

FHLB Forehead head lift both sides recordedMHLL Mastoid head lift skull tapper located at leftMHLR Mastoid head lift skull tapper located at right

Conflict of Interests

The authors declare the following Dr Erdem Yavuz is aResearch Scientist at Research and Development IntelligentHearing Systems Inc andDr Rafael Delgado is the ExecutiveVice President and Director of Research and DevelopmentIntelligent Hearing Systems IncThe authors declare no otherconflict of interests related to this paper

References

[1] G von Bekesy ldquoUber akustische reizung des vestibularappa-ratesrdquo Pflugerrsquos Archiv fur die Gesamte Physiologie des Menschenund der Tiere vol 236 no 1 pp 59ndash76 1935

[2] J G Colebatch and G M Halmagyi ldquoVestibular evokedpotentials in human neck muscles before and after unilateralvestibular deafferentationrdquo Neurology vol 42 no 8 pp 1635ndash1636 1992

[3] J G Colebatch G M Halmagyi and N F Skuse ldquoMyogenicpotentials generated by a click-evoked vestibulocollic reflexrdquoJournal of Neurology Neurosurgery and Psychiatry vol 57 no2 pp 190ndash197 1994

[4] G M Halmagyi R A Yavor and J G Colebatch ldquoTapping thehead activates the vestibular system a new use for the clinicalreflex hammerrdquo Neurology vol 45 no 10 pp 1927ndash1929 1995

[5] K Sheykholeslami T Murofushi M H Kermany and KKaga ldquoBone-conducted evoked myogenic potentials from thesternocleidomastoid musclerdquo Acta Oto-Laryngologica vol 120no 6 pp 731ndash734 2000

[6] K Sheykholeslami M H Kermany and K Kaga ldquoFrequencysensitivity range of the saccule to bone-conducted stimulimeasured by vestibular evoked myogenic potentialsrdquo HearingResearch vol 160 no 1-2 pp 58ndash62 2001

[7] S R D Watson P Fagan and J G Colebatch ldquoGalvanicstimulation evokes short-latency EMG responses in sternoclei-domastoidwhich are abolished by selective vestibular nerve sec-tionrdquo Electroencephalography and Clinical NeurophysiologymdashElectromyography and Motor Control vol 109 no 6 pp 471ndash474 1998

[8] S R D Watson and J G Colebatch ldquoVestibular-evoked elec-tromyographic responses in soleus a comparison between clickand galvanic stimulationrdquo Experimental Brain Research vol 119no 4 pp 504ndash510 1998

[9] F Deriu E Tolu and J C Rothwell ldquoA sound-evoked vestibu-lomasseteric reflex in healthy humansrdquo Journal of Neurophysiol-ogy vol 93 no 5 pp 2739ndash2751 2005

[10] K Botzel P Feise O I Kolev S Krafczyk and T BrandtldquoErratum postural reflexes evoked by tapping forehead andchestrdquo Experimental Brain Research vol 140 no 2 p 251 2001

[11] S M Rosengren N P M Todd and J G ColebatchldquoVestibular-evoked extraocular potentials produced by stimula-tionwith bone-conducted soundrdquoClinical Neurophysiology vol116 no 8 pp 1938ndash1948 2005

[12] N P M Todd S M Rosengren S T Aw and J G ColebatchldquoOcular vestibular evoked myogenic potentials (OVEMPs)

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

Submit your manuscripts athttpwwwhindawicom

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Page 4: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

4 BioMed Research International

AHLB MHLLMHLR

Head lift stimulation sites

Skull tapper side view

Skull tapper front view

Audio stimulus

AHLR AHLL FHL

Figure 1The stimulus presentations sites for the head lift recordingsmade for acoustic and skull tap VEMPs Abbreviations in the illustrationindicate the stimulus type and direction as follows (1) head lift stimulus delivered to the right ear (AHLR) (2) head lift stimulus deliveredto the left ear (AHLL) (3) head lift stimulus delivered to both ears (AHLB) (4) forehead head lift (FHL) (5) mastoid head lift skull tapperlocated at right (MHLR) (6) mastoid head lift skull tapper located at left (MHLL)

(1) head lift stimulus delivered to the left ear (AHLL)(2) head lift stimulus delivered to the right ear (AHLR)(3) head lift stimulus delivered to both ears (AHLB)

Three different types of recordingswere conducted for theskull tapping evokedVEMPs (two repetitions each)with skulltapper located at

(1) forehead head lift both sides recorded (FHLB)(2) mastoid head lift skull tapper located at left (MHLL)(3) mastoid head lift skull tapper located at right

(MHLR)

Therefore a total of 12 recordings were conducted for eachpatient (6 total typeswith two repetitions) before and after thesurgical intervention as shown in Figure 1

The recorded responses were normalized according tothe prestimulus (base) EMG RMS calculations Normalizedvalueswere used to assess the asymmetry ratios (AR) betweenthe left and right side measurements The usefulness of thenormalization of ARmeasurements is still under debate [37]The following equation (1) was used for the asymmetry ratiowhere the 119860

119871is the amplitude measure from the left side

recording between the first positive and first negative peakand similarly 119860

119877is the amplitudemeasured on the right side

Corrected AR of up to 35 is considered normal [38]

Asymmetry Ratio = 100100381610038161003816100381610038161003816100381610038161003816

(119860119871minus 119860119877)

(119860119871+ 119860119877)

100381610038161003816100381610038161003816100381610038161003816

(1)

During the course of this study additional VEMP record-ings were made where the SCM contraction was sustainedvia the head turn to the sides In this paper we only presentthe results and the details of the head lift data as we foundthe head turn method to be unreliable when analyzed via

asymmetry ratio approach We prefer and advocate the headlift approach as it is much easier to control and identify if apatientrsquos head is symmetrically lifted or not For this reasonwe believe that the VEMPs recorded via head lift are lessprone to be affected by the orientation differences of thevestibular organs during the recording sessions compared tohead turnwith the current instrumentation limits Additionalfeedback monitoring of the 3D positioning of the head byusing additionalmeans such as gyroscopes andor accelerom-eters could help to minimize this variability

23 Participating Patients Details

Patient Number 1 Patient number 1 was a 43-year-old manwho suffered from slight tinnitus and slight hearing loss inhis right ear with no vestibular problems prior to admis-sion Audiological tests revealed a small high-frequencysensorineural hearing loss on the right side with pure toneaverage (PTA) for 3 and 4 kHz = 35 dBHL The speech dis-crimination score at 60 dB was almost normal (80 scored100 at 70 dB) Impedance audiometry revealed normalmiddle ear function and normal stapedius reflex thresholdson both sides Normal response to click stimulus at 90 dBnHLwas present on the left side in ABR but on the right sideABR showed retrocochlear abnormality Vestibular calorictest and videonystagmography showed normal responseson both sides with no central vestibular disorders Detailson the VEMP recordings will be described in the Resultssection MRI revealed a tumor in the internal auditory canalthe tumor was 12 times 9mm in size Clinical and electricalexamination (using electromyography) of the right facialnerve revealed its normal function

Middle fossa approach was chosen for the surgeryattempting to preserve the hearing The tumor appeared to

BioMed Research International 5

arise from cochlear nerve and was attached to other nervesin the internal auditory canal

Patient Number 2 Patient number 2was a 51-year-oldwomanPrior to the admission she complained about tinnitus andhearing loss in the right ear with some symptoms of rightfacial nerve paresis Pure tone audiometry revealed sen-sorineural hearing loss on the right side with PTA for 05 and1 kHz = 30 dBHL and for 2 and 4 kHz = 575 dBHL and thespeech discrimination score at 60 dB was 30 for the rightear Normalmiddle ear functionwas provedwith tympanom-etry but stapedius reflexes were missed Normal response toclick stimulus at 90 dBnHLwas present on the left side inABRand no reproducible waves on the right Vestibular calorictest and videonystagmography revealed aflexia on the rightside with no central vestibular abnormalities and normalfunction on the left Clinical and electrical examination(electromyography) of the right facial nerve revealed itsabnormal function Details on the VEMP recordings will bedescribed in the results section MRI showed a 4 times 9mmtumor in the right internal ear canal

Middle fossa approach was selected to increase thepossibility of hearing preservationThe tumor seemed to arisefrom superior vestibular nerve but involved the inferior oneas well

Patient Number 3 Patient number 3 was a 26-year-oldwoman whose main complaint was tinnitus on the left sideAt the admission she stated not having any other hearingor vestibular problems Auditory testing revealed normalhearing in both ears in all audiometric frequencies withthe pure tone average for 05 1 2 and 4 kHz = 25 dB andspeech discrimination score at 60 dB was 100 Impedanceaudiometry revealed normal results Auditory brainstemresponse showed normal reproducible waves on both sidesVestibular caloric test and videonystagmography showednormal responses on both sides with no central vestibulardisorders Left facial nerve function was normal VEMPswill be discussed in the Results section Due to the patientrsquoshistory of asymmetric tinnitus and young age it was decidedto perform MRI The MRI revealed a tumor in the internalauditory canal the tumor was 7 times 5 times 15mm in size

For the surgery middle fossa approach was selected forthe hearing preservation The tumor seemed to arise fromsuperior vestibular nerve

This study is a part of a retrospective-prospective projectthat was approved by the Ethics Committee Review Boardat the Medical University of Warsaw where the VEMPsrecordings have been conducted The project conforms withThe Code of Ethics of the World Medical Association (Dec-laration of Helsinki)

3 Results

Table 1 shows AC VEMP and tap VEMP results with valuesfor P1 latencies and corrected amplitudes of the responsesalong with corrected asymmetry ratios Figure 2 presents theresults of the preoperative (preop) recordings acquired byboth VEMP techniques Figure 3 shows the change observed

between the preop and postoperative (postop) responsesrecorded from the ipsilateral side to the tumor

Patient Number 1 In this patient highly large correctedasymmetry ratio (AR) values for AC VEMPs (AHLB AR =4759 AHLL versus AHLR AR = 4543) were observedValues lower than 35 are considered normal [38] and weused them as referral In close inspection of the waveformsfrom the contralateral side one can easily see that the left sidestimulation producedmuch smaller activity on the right sidewhere the right side stimulation did not produce a similaractivity on the left side (Figure 2)

The tap VEMPs were symmetric for the forehead (FHLBAR = 1915) and for the mastoid skull tapping resultsrecorded from the ipsilateral side SCM (right MHLR versusleft MHLL AR = 1684)

The postop responses were compared with the preop data(Figure 3) The AC VEMPs results showed that P1 and N1disappeared when the ear ipsilateral to the tumor was stim-ulated In the bilaterally stimulated recordings we observedthe preservation of these peaks to an extent Considering thesurgical cut of the ipsilateral inferior bundle the preservationof the peaks suggested the contribution of the contralateralside Forehead placement tapVEMPs showed a reversal in therecorded P1-N1 peak complex In all of the above recordingsthe later waveforms observed between 25 and 60ms rangewhich are generally regarded as cochlear in origin [24 39]did not display a major change

Patient Number 2 Patient number 2 medical history alongwith unilateral sensorineural hearing loss poor speech recog-nition ABR VNG and facial nerve EMG results pointed toimpaired function of VIII and VII nerves on the right side

In AC VEMPs we observed drastic differences betweenleft and right side responses (AHLB AR = 4349) The rightside auditory stimulation failed to generate a response wherethe left side stimulation evoked a robust response (Figure 2)

Skull tapping the forehead and each mastoid resulted inlarge ARs (FHLB AR = 5760 MHLR versus MHLR AR =6132) Upon visual inspection of ipsilateral responses theinitial parts of thewaveformmorphology (P1-N1 region)weredifferent (Figure 2)

In the postop preop comparison (Figure 3) there wereno significant changes in any of the responses recordedipsilateral to the tumor in neither of the VEMP techniquesfor P1 and N1 peaks suggesting that both bundles had totalfunctional loss before the surgery Additionally similar tothe first patient late waveforms did not display a significantchange

Patient Number 3 In patient number 3 all audiologicalVNG and VEMP tests were within normal limits Due topatientrsquos young age and history of tinnitus on the left side thissuggested that there might be a retrocochlear problem

No asymmetry was observed in the AC VEMPs (AHLBAR = 1662 AHLR versus AHLL AR = 1995) and tapVEMPs (FHLB AR = 1718 MHLR versus MHLL AR= 1929) The mastoid ipsilateral tap VEMP recordingsshowed high similarity In this case both AC VEMP and

6 BioMed Research International

Table1Au

ditory

andskulltap

VEM

Phead

liftresults

Patie

ntAnalyzed

parameter

Headlift

Auditory

Tapp

ingforehead

Tapp

ingmastoidsIPS

Irespo

nses

AHLB

AR(

)

AHLL

AHLR

AR(

)

FHLB

AR(

)

MHLL

MHLR

AR(

)Re

spon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

1P1

latency

(ms)

1320

1340

1340

1420

1320

1440

1400

1440

Corram

plitu

de2556

908

4759lowast

2296

862

4543lowast

3624

2459

1915

3367

2397

1684

2P1

latency

(ms)

1400

1360

1460

NR

1440

1520

1720

1560

Corram

plitu

de1314

518

4349lowast

2351

NR

3322

894

5760lowast

3819

916

6132lowast

3P1

latency

(ms)

1260

1280

1280

1300

1400

1360

1440

1320

Corram

plitu

de1019

1414

1626

1962

2940

1995

4488

3172

1718

5823

3940

1929

AHLB

headlift

stimulus

delivered

tobo

thearsA

HLL

headlift

stimulus

delivered

totheleftearAHLR

headlift

stimulus

delivered

totherig

htearFH

LBForeheadHeadLiftskulltapperlocated

atforehead

MHLL

Mastoid

HeadLiftskulltapperlocatedat

Left

MHLR

Mastoid

HeadLiftskulltapperlocatedat

RightP1p

ositive

peakcorram

plitu

decorrected

amplitu

deS

CMsternocleidom

astoid

muscle

AR

Asymmetry

ratio

NR

norespon

seA

bnormalresults

ofcorrectedasym

metry

ratio

s(ARgt35)a

ndno

respon

seresults

(NR)

arem

arkedwithlowast

BioMed Research International 7

AHLR

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

AHLL

(a)

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

AHLR

AHLL

(b)

AHLB

AHLL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

AHLR

(c)

Figure 2 VEMP waveforms recorded from all 3 subjects All the waveforms are normalized according to prestimulus EMG activity In thisfigure left side recordings are plotted as solid lines while right side recordings are plotted as dashed lines Abbreviations are used in thisfigure as follows AHLB auditory head lift both ear stimulation recorded bilaterally AHLL auditory head lift left ear stimulation recordedbilaterally AHLR auditory head lift right ear stimulation recorded bilaterally FHLB head lift recording tapper located at forehead recordedbilaterally MHLL head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at rightmastoid recorded bilaterally

tap VEMP results failed to point to a tumor presence TheMRI showed a tumor in the left internal auditory canal(7 times 5 times 15mm) During the surgical intervention thetumor was identified as arising from the superior vestibularnerve

In the postop versus preop comparison (Figure 3) of thehead lift AC VEMP recordings no significant change onthe tumor side was found when both ears were stimulatedHowever significant difference was shown when the stim-ulation was at the side of pathology For the tap VEMP

8 BioMed Research International

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

(a)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

(b)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

(c)

Figure 3 Preop (solid lines) and postop (dashed lines) VEMP waveforms recorded ipsilateral to the pathology from all 3 subjects Allthe waveforms are normalized according to prestimulus EMG activity Abbreviations are used in this figure as follows where ipsilateralindicates the location in return to the pathology location AHLB ipsilateral auditory head lift recording with both ears stimulated AHLipsilateral auditory head lift recording in return to ipsilateral stimulation FHLB ipsilateral head lift recording tapper located at foreheadMHL ipsilateral head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at ipsilateralmastoid

P1 peak could not be identified in any of the recordingsand N1 peak amplitudes were diminished in all recordingsexcept for the forehead placement where N1 latency andamplitude were preserved In general more variability inlatency and amplitude was also present for the later waves aswell

4 Discussion

In todayrsquos audiovestibular clinical practice a large numberof tests are available to determine the functionality of theaudiovestibular system The selection and the use of thesetests are mostly limited by their selectivity practicality and

BioMed Research International 9

costs The rapid development of VEMP related research andour recent experience with AC VEMPs and tap VEMPs haveled us to use VEMPs as an integral part of our diagnosticbattery In our department we routinely use the cervicalVEMPs due to the longer history thus there is larger amountof accumulated research on cervical VEMPs Currently weare also investigating the use of relatively newer approachof ocular VEMPs and adding it to our collected data setAlthough the recent research on ocular VEMPs has beenencouraging for clinical usage the technique has to still berefined to be used as a routine test The cervical VEMPs areeasy to acquire and can be efficiently used with quantificationmethods for ongoing muscle activity monitoring such asthe one used in this study where acceptance and rejectionmuscle activity regions are used Our near feature planis to include the ocular VEMPs recording in our routinediagnostic tests ensuring that the adaptation of the muscleactivity quantification methods we use is properly utilized

Our results showed that the VEMP recordings werenot only capable of identifying the CPAT but were alsoable to contribute additional information of involved nervebundles in first patient The observed abnormal audiologicalfindings strongly suggested the initial diagnosis of vestibularschwannoma The MRI pointed to the presence of a tumorlocated in the right internal auditory canal VEMP results alsosupported the presence of a tumor additionally pointing tothe inferior vestibular nerve involvementThe surgery reportdescribed the tumor to be arising from cochlear nerve and tobe attached to the other nerves in the internal auditory canalThe cochlear nerve is located closer to the inferior bundle ofthe vestibular nerve [34ndash36] and compression on the inferiornerve therefore was affecting the AC VEMPs results but notaltering the proper function of the superior vestibular nerve(AR in tap VEMPs within normal limits [38])

For the second patient the audiological results alongwith VNG and VEMP results strongly suggested the tumorpresence in the internal auditory canal which was supportedby theMRI findingsThe surgeon described the tumor arisingfrom superior vestibular nerve involving the inferior bundleas well During the surgery the tumor was found to be biggerthan initially described by the MRI which was performed afew months before As routinely done prior to the surgerythe other tests including VEMPs were performed to decideon the surgical approach and determine the possibility forhearing preservation In this case the tumor affected thefunction of all the nerves in the internal auditory canal Ourconclusion from the AC VEMP and tap VEMP findings wasthe involvement of both the inferior and superior nervesThe VEMPs were successful in pointing out both the tumorpresence and the involvement of both of the vestibularnerves An interesting observation was that the left andright responses recorded during both right side and left sideauditory stimulation were highly similar suggesting that thewhole response seen in AHLBmight have been driven by theleft ear

The third patient was a particularly interesting casebecause all tests performed along with AC VEMPs and tapVEMPs proved to be not helpful in the diagnosis of thevestibular schwannoma Although the tumor was arising

from the superior vestibular nerve the tap VEMP failed toindicate presence of the tumor similar to the rest of theclinical tools suggesting a normal function In this case onlythe MRI was sensitive enough to show the tumor The MRIwas performed due to the history of the patient her youngage and our experience in vestibular schwannoma casesThereason why the recorded tap VEMPs were not able to detectthe pathology is a good question to investigate

We observed that the mastoid placement of the skulltapper created additional challenges It was extremely difficultto replicate the same conditions when the skull tapper wasplaced on a surface of the mastoid region Due to the 3-dimensional shape of the mastoid area it was very difficultto maintain a steady 3D relation between the head and theskull tapper hit axis (thus with the vestibule axis) especiallywhen tapper is moved from one side to the other As with thecurrent setup there was no chance of monitoring the relationbetween the skull tapper hit direction and the vestibularorgans and it was not possible to limit the introducedvariability In the light of these observations (although weacquired data with skull tapper positioned at mastoids onboth sides and described the results of the responses acquiredfrom the ipsilateral SMCs) we preferred to relay and advocatethe usage of the forehead stimulation results due to the limitsof currently available instrumentation The directional infor-mation revealed by themastoid placement is complex and hasto be carefully analyzed For general clinical implementationadditional safeguards are required An additional feedbackmechanism describing the orientation relation between thetapper and gravity such as a gyroscope could be helpfulin minimizing the variability and thus could be useful inproducing equivalent directional force delivery to each sidewhen skull tapper is moved from left to right

5 Conclusions

In this paper we introduced our efforts in adding the ACVEMPs and tapVEMPs to expend the clinical diagnostic testsused for advanced assessment in CPAT patients hoping thatit will serve as a guideline for other clinicians interested inutilizing tap VEMPs

The patients presented in this study were selected topoint out different results we observed among a larger patientpopulation The findings from the larger population groupwill be presented in a more detailed follow-up subsequentpaper The main goal of this paper was to focus on theprotocol used and point at the variability in the findings

In two of three presented cases AC VEMPs and tapVEMPs together proved to be helpful in establishing thediagnosis of CPAT providingmore information on the tumoraffected bundle of vestibular nerve (superior or inferior orboth) Performing only AC VEMPs or only tap VEMPswould have provided insufficient information about thetumor and the vestibular nerve bundle involvement Inthe third case VEMPs failed to identify the vestibularschwannoma which was clearly shown in MRI scans Inthis case our medical intuition and expertise with CPATpatients prompted us to perform MRI Due to the high cost

10 BioMed Research International

of MRI it is typically not performed at the early stages ofthe diagnostics procedure in many countries Once othertests indicate the possible presence of the CPAT an MRI isconducted

Providing AC VEMPs and tap VEMPs to the availabletest battery in the assessment of CPAT is likely to improvethe diagnostic process by providing more information onthe involved vestibular nerve bundles In addition thisinformation might be used later during the surgery In manycases theMRI is not performed very short before the surgeryUsually it is performed earlier during the diagnostic processThe surgery takes place sometime after Asmentioned beforethe MRI is quite costly and usually is not performed againif not much time passed However the ABR AC VEMPsand tap VEMP once performed in diagnostic proceedingmight be repeated short before the surgery to clarify thepresence along with possible compression characteristics ofthe tumor on the vestibular andor auditory nerves Thiscombined information from earlier MRI scans and latestelectrophysiological tests serves the surgeons as a guidelinein their surgical approach and during tumor removal Itprovides very useful information for the surgeon in makinga decision about additional intraoperative monitoring ofhearing In our department intraoperative monitoring isroutinely used in every CPAT surgery and many otherear surgeries but intraoperative hearing monitoring is notroutinely performed in most of the other clinics In additionthe details from electrophysiological tests about the involvednerve bundles are useful in patients counseling and informingthem on more realistic possible outcomes of the surgery likehearing preservations possibilities and a risk of hearing lossduring the surgery a risk of facial nerve paresis and vertigosymptoms after the surgery

Abbreviations

ABR Auditory brainstem responseAS Asymmetry ratioCPAT Cerebellopontine angle tumorECochG ElectrocochleographyEEG ElectroencephalographyEMG ElectromiographyMRI Magnetic resonance imagingPTA Pure tone averageRMS Root means squaredSCM SternocleidomastoidVEMP Vestibular Evoked Myogenic PotentialAC VEMP Auditory Vestibular Evoked Myogenic

Potentialtap VEMP Skull tapping induced Vestibular

Evoked Myogenic Potential

AC VEMPsThree Types of Recordings

AHLL Head lift stimulus delivered to the left earAHLR Head lift stimulus delivered to the right earAHLB Head lift stimulus delivered to both ears

tap VEMPs Three Types of Recordings with Skull Tapper

FHLB Forehead head lift both sides recordedMHLL Mastoid head lift skull tapper located at leftMHLR Mastoid head lift skull tapper located at right

Conflict of Interests

The authors declare the following Dr Erdem Yavuz is aResearch Scientist at Research and Development IntelligentHearing Systems Inc andDr Rafael Delgado is the ExecutiveVice President and Director of Research and DevelopmentIntelligent Hearing Systems IncThe authors declare no otherconflict of interests related to this paper

References

[1] G von Bekesy ldquoUber akustische reizung des vestibularappa-ratesrdquo Pflugerrsquos Archiv fur die Gesamte Physiologie des Menschenund der Tiere vol 236 no 1 pp 59ndash76 1935

[2] J G Colebatch and G M Halmagyi ldquoVestibular evokedpotentials in human neck muscles before and after unilateralvestibular deafferentationrdquo Neurology vol 42 no 8 pp 1635ndash1636 1992

[3] J G Colebatch G M Halmagyi and N F Skuse ldquoMyogenicpotentials generated by a click-evoked vestibulocollic reflexrdquoJournal of Neurology Neurosurgery and Psychiatry vol 57 no2 pp 190ndash197 1994

[4] G M Halmagyi R A Yavor and J G Colebatch ldquoTapping thehead activates the vestibular system a new use for the clinicalreflex hammerrdquo Neurology vol 45 no 10 pp 1927ndash1929 1995

[5] K Sheykholeslami T Murofushi M H Kermany and KKaga ldquoBone-conducted evoked myogenic potentials from thesternocleidomastoid musclerdquo Acta Oto-Laryngologica vol 120no 6 pp 731ndash734 2000

[6] K Sheykholeslami M H Kermany and K Kaga ldquoFrequencysensitivity range of the saccule to bone-conducted stimulimeasured by vestibular evoked myogenic potentialsrdquo HearingResearch vol 160 no 1-2 pp 58ndash62 2001

[7] S R D Watson P Fagan and J G Colebatch ldquoGalvanicstimulation evokes short-latency EMG responses in sternoclei-domastoidwhich are abolished by selective vestibular nerve sec-tionrdquo Electroencephalography and Clinical NeurophysiologymdashElectromyography and Motor Control vol 109 no 6 pp 471ndash474 1998

[8] S R D Watson and J G Colebatch ldquoVestibular-evoked elec-tromyographic responses in soleus a comparison between clickand galvanic stimulationrdquo Experimental Brain Research vol 119no 4 pp 504ndash510 1998

[9] F Deriu E Tolu and J C Rothwell ldquoA sound-evoked vestibu-lomasseteric reflex in healthy humansrdquo Journal of Neurophysiol-ogy vol 93 no 5 pp 2739ndash2751 2005

[10] K Botzel P Feise O I Kolev S Krafczyk and T BrandtldquoErratum postural reflexes evoked by tapping forehead andchestrdquo Experimental Brain Research vol 140 no 2 p 251 2001

[11] S M Rosengren N P M Todd and J G ColebatchldquoVestibular-evoked extraocular potentials produced by stimula-tionwith bone-conducted soundrdquoClinical Neurophysiology vol116 no 8 pp 1938ndash1948 2005

[12] N P M Todd S M Rosengren S T Aw and J G ColebatchldquoOcular vestibular evoked myogenic potentials (OVEMPs)

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

Submit your manuscripts athttpwwwhindawicom

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Behavioural Neurology

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Disease Markers

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PPAR Research

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Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 5: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

BioMed Research International 5

arise from cochlear nerve and was attached to other nervesin the internal auditory canal

Patient Number 2 Patient number 2was a 51-year-oldwomanPrior to the admission she complained about tinnitus andhearing loss in the right ear with some symptoms of rightfacial nerve paresis Pure tone audiometry revealed sen-sorineural hearing loss on the right side with PTA for 05 and1 kHz = 30 dBHL and for 2 and 4 kHz = 575 dBHL and thespeech discrimination score at 60 dB was 30 for the rightear Normalmiddle ear functionwas provedwith tympanom-etry but stapedius reflexes were missed Normal response toclick stimulus at 90 dBnHLwas present on the left side inABRand no reproducible waves on the right Vestibular calorictest and videonystagmography revealed aflexia on the rightside with no central vestibular abnormalities and normalfunction on the left Clinical and electrical examination(electromyography) of the right facial nerve revealed itsabnormal function Details on the VEMP recordings will bedescribed in the results section MRI showed a 4 times 9mmtumor in the right internal ear canal

Middle fossa approach was selected to increase thepossibility of hearing preservationThe tumor seemed to arisefrom superior vestibular nerve but involved the inferior oneas well

Patient Number 3 Patient number 3 was a 26-year-oldwoman whose main complaint was tinnitus on the left sideAt the admission she stated not having any other hearingor vestibular problems Auditory testing revealed normalhearing in both ears in all audiometric frequencies withthe pure tone average for 05 1 2 and 4 kHz = 25 dB andspeech discrimination score at 60 dB was 100 Impedanceaudiometry revealed normal results Auditory brainstemresponse showed normal reproducible waves on both sidesVestibular caloric test and videonystagmography showednormal responses on both sides with no central vestibulardisorders Left facial nerve function was normal VEMPswill be discussed in the Results section Due to the patientrsquoshistory of asymmetric tinnitus and young age it was decidedto perform MRI The MRI revealed a tumor in the internalauditory canal the tumor was 7 times 5 times 15mm in size

For the surgery middle fossa approach was selected forthe hearing preservation The tumor seemed to arise fromsuperior vestibular nerve

This study is a part of a retrospective-prospective projectthat was approved by the Ethics Committee Review Boardat the Medical University of Warsaw where the VEMPsrecordings have been conducted The project conforms withThe Code of Ethics of the World Medical Association (Dec-laration of Helsinki)

3 Results

Table 1 shows AC VEMP and tap VEMP results with valuesfor P1 latencies and corrected amplitudes of the responsesalong with corrected asymmetry ratios Figure 2 presents theresults of the preoperative (preop) recordings acquired byboth VEMP techniques Figure 3 shows the change observed

between the preop and postoperative (postop) responsesrecorded from the ipsilateral side to the tumor

Patient Number 1 In this patient highly large correctedasymmetry ratio (AR) values for AC VEMPs (AHLB AR =4759 AHLL versus AHLR AR = 4543) were observedValues lower than 35 are considered normal [38] and weused them as referral In close inspection of the waveformsfrom the contralateral side one can easily see that the left sidestimulation producedmuch smaller activity on the right sidewhere the right side stimulation did not produce a similaractivity on the left side (Figure 2)

The tap VEMPs were symmetric for the forehead (FHLBAR = 1915) and for the mastoid skull tapping resultsrecorded from the ipsilateral side SCM (right MHLR versusleft MHLL AR = 1684)

The postop responses were compared with the preop data(Figure 3) The AC VEMPs results showed that P1 and N1disappeared when the ear ipsilateral to the tumor was stim-ulated In the bilaterally stimulated recordings we observedthe preservation of these peaks to an extent Considering thesurgical cut of the ipsilateral inferior bundle the preservationof the peaks suggested the contribution of the contralateralside Forehead placement tapVEMPs showed a reversal in therecorded P1-N1 peak complex In all of the above recordingsthe later waveforms observed between 25 and 60ms rangewhich are generally regarded as cochlear in origin [24 39]did not display a major change

Patient Number 2 Patient number 2 medical history alongwith unilateral sensorineural hearing loss poor speech recog-nition ABR VNG and facial nerve EMG results pointed toimpaired function of VIII and VII nerves on the right side

In AC VEMPs we observed drastic differences betweenleft and right side responses (AHLB AR = 4349) The rightside auditory stimulation failed to generate a response wherethe left side stimulation evoked a robust response (Figure 2)

Skull tapping the forehead and each mastoid resulted inlarge ARs (FHLB AR = 5760 MHLR versus MHLR AR =6132) Upon visual inspection of ipsilateral responses theinitial parts of thewaveformmorphology (P1-N1 region)weredifferent (Figure 2)

In the postop preop comparison (Figure 3) there wereno significant changes in any of the responses recordedipsilateral to the tumor in neither of the VEMP techniquesfor P1 and N1 peaks suggesting that both bundles had totalfunctional loss before the surgery Additionally similar tothe first patient late waveforms did not display a significantchange

Patient Number 3 In patient number 3 all audiologicalVNG and VEMP tests were within normal limits Due topatientrsquos young age and history of tinnitus on the left side thissuggested that there might be a retrocochlear problem

No asymmetry was observed in the AC VEMPs (AHLBAR = 1662 AHLR versus AHLL AR = 1995) and tapVEMPs (FHLB AR = 1718 MHLR versus MHLL AR= 1929) The mastoid ipsilateral tap VEMP recordingsshowed high similarity In this case both AC VEMP and

6 BioMed Research International

Table1Au

ditory

andskulltap

VEM

Phead

liftresults

Patie

ntAnalyzed

parameter

Headlift

Auditory

Tapp

ingforehead

Tapp

ingmastoidsIPS

Irespo

nses

AHLB

AR(

)

AHLL

AHLR

AR(

)

FHLB

AR(

)

MHLL

MHLR

AR(

)Re

spon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

1P1

latency

(ms)

1320

1340

1340

1420

1320

1440

1400

1440

Corram

plitu

de2556

908

4759lowast

2296

862

4543lowast

3624

2459

1915

3367

2397

1684

2P1

latency

(ms)

1400

1360

1460

NR

1440

1520

1720

1560

Corram

plitu

de1314

518

4349lowast

2351

NR

3322

894

5760lowast

3819

916

6132lowast

3P1

latency

(ms)

1260

1280

1280

1300

1400

1360

1440

1320

Corram

plitu

de1019

1414

1626

1962

2940

1995

4488

3172

1718

5823

3940

1929

AHLB

headlift

stimulus

delivered

tobo

thearsA

HLL

headlift

stimulus

delivered

totheleftearAHLR

headlift

stimulus

delivered

totherig

htearFH

LBForeheadHeadLiftskulltapperlocated

atforehead

MHLL

Mastoid

HeadLiftskulltapperlocatedat

Left

MHLR

Mastoid

HeadLiftskulltapperlocatedat

RightP1p

ositive

peakcorram

plitu

decorrected

amplitu

deS

CMsternocleidom

astoid

muscle

AR

Asymmetry

ratio

NR

norespon

seA

bnormalresults

ofcorrectedasym

metry

ratio

s(ARgt35)a

ndno

respon

seresults

(NR)

arem

arkedwithlowast

BioMed Research International 7

AHLR

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

AHLL

(a)

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

AHLR

AHLL

(b)

AHLB

AHLL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

AHLR

(c)

Figure 2 VEMP waveforms recorded from all 3 subjects All the waveforms are normalized according to prestimulus EMG activity In thisfigure left side recordings are plotted as solid lines while right side recordings are plotted as dashed lines Abbreviations are used in thisfigure as follows AHLB auditory head lift both ear stimulation recorded bilaterally AHLL auditory head lift left ear stimulation recordedbilaterally AHLR auditory head lift right ear stimulation recorded bilaterally FHLB head lift recording tapper located at forehead recordedbilaterally MHLL head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at rightmastoid recorded bilaterally

tap VEMP results failed to point to a tumor presence TheMRI showed a tumor in the left internal auditory canal(7 times 5 times 15mm) During the surgical intervention thetumor was identified as arising from the superior vestibularnerve

In the postop versus preop comparison (Figure 3) of thehead lift AC VEMP recordings no significant change onthe tumor side was found when both ears were stimulatedHowever significant difference was shown when the stim-ulation was at the side of pathology For the tap VEMP

8 BioMed Research International

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

(a)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

(b)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

(c)

Figure 3 Preop (solid lines) and postop (dashed lines) VEMP waveforms recorded ipsilateral to the pathology from all 3 subjects Allthe waveforms are normalized according to prestimulus EMG activity Abbreviations are used in this figure as follows where ipsilateralindicates the location in return to the pathology location AHLB ipsilateral auditory head lift recording with both ears stimulated AHLipsilateral auditory head lift recording in return to ipsilateral stimulation FHLB ipsilateral head lift recording tapper located at foreheadMHL ipsilateral head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at ipsilateralmastoid

P1 peak could not be identified in any of the recordingsand N1 peak amplitudes were diminished in all recordingsexcept for the forehead placement where N1 latency andamplitude were preserved In general more variability inlatency and amplitude was also present for the later waves aswell

4 Discussion

In todayrsquos audiovestibular clinical practice a large numberof tests are available to determine the functionality of theaudiovestibular system The selection and the use of thesetests are mostly limited by their selectivity practicality and

BioMed Research International 9

costs The rapid development of VEMP related research andour recent experience with AC VEMPs and tap VEMPs haveled us to use VEMPs as an integral part of our diagnosticbattery In our department we routinely use the cervicalVEMPs due to the longer history thus there is larger amountof accumulated research on cervical VEMPs Currently weare also investigating the use of relatively newer approachof ocular VEMPs and adding it to our collected data setAlthough the recent research on ocular VEMPs has beenencouraging for clinical usage the technique has to still berefined to be used as a routine test The cervical VEMPs areeasy to acquire and can be efficiently used with quantificationmethods for ongoing muscle activity monitoring such asthe one used in this study where acceptance and rejectionmuscle activity regions are used Our near feature planis to include the ocular VEMPs recording in our routinediagnostic tests ensuring that the adaptation of the muscleactivity quantification methods we use is properly utilized

Our results showed that the VEMP recordings werenot only capable of identifying the CPAT but were alsoable to contribute additional information of involved nervebundles in first patient The observed abnormal audiologicalfindings strongly suggested the initial diagnosis of vestibularschwannoma The MRI pointed to the presence of a tumorlocated in the right internal auditory canal VEMP results alsosupported the presence of a tumor additionally pointing tothe inferior vestibular nerve involvementThe surgery reportdescribed the tumor to be arising from cochlear nerve and tobe attached to the other nerves in the internal auditory canalThe cochlear nerve is located closer to the inferior bundle ofthe vestibular nerve [34ndash36] and compression on the inferiornerve therefore was affecting the AC VEMPs results but notaltering the proper function of the superior vestibular nerve(AR in tap VEMPs within normal limits [38])

For the second patient the audiological results alongwith VNG and VEMP results strongly suggested the tumorpresence in the internal auditory canal which was supportedby theMRI findingsThe surgeon described the tumor arisingfrom superior vestibular nerve involving the inferior bundleas well During the surgery the tumor was found to be biggerthan initially described by the MRI which was performed afew months before As routinely done prior to the surgerythe other tests including VEMPs were performed to decideon the surgical approach and determine the possibility forhearing preservation In this case the tumor affected thefunction of all the nerves in the internal auditory canal Ourconclusion from the AC VEMP and tap VEMP findings wasthe involvement of both the inferior and superior nervesThe VEMPs were successful in pointing out both the tumorpresence and the involvement of both of the vestibularnerves An interesting observation was that the left andright responses recorded during both right side and left sideauditory stimulation were highly similar suggesting that thewhole response seen in AHLBmight have been driven by theleft ear

The third patient was a particularly interesting casebecause all tests performed along with AC VEMPs and tapVEMPs proved to be not helpful in the diagnosis of thevestibular schwannoma Although the tumor was arising

from the superior vestibular nerve the tap VEMP failed toindicate presence of the tumor similar to the rest of theclinical tools suggesting a normal function In this case onlythe MRI was sensitive enough to show the tumor The MRIwas performed due to the history of the patient her youngage and our experience in vestibular schwannoma casesThereason why the recorded tap VEMPs were not able to detectthe pathology is a good question to investigate

We observed that the mastoid placement of the skulltapper created additional challenges It was extremely difficultto replicate the same conditions when the skull tapper wasplaced on a surface of the mastoid region Due to the 3-dimensional shape of the mastoid area it was very difficultto maintain a steady 3D relation between the head and theskull tapper hit axis (thus with the vestibule axis) especiallywhen tapper is moved from one side to the other As with thecurrent setup there was no chance of monitoring the relationbetween the skull tapper hit direction and the vestibularorgans and it was not possible to limit the introducedvariability In the light of these observations (although weacquired data with skull tapper positioned at mastoids onboth sides and described the results of the responses acquiredfrom the ipsilateral SMCs) we preferred to relay and advocatethe usage of the forehead stimulation results due to the limitsof currently available instrumentation The directional infor-mation revealed by themastoid placement is complex and hasto be carefully analyzed For general clinical implementationadditional safeguards are required An additional feedbackmechanism describing the orientation relation between thetapper and gravity such as a gyroscope could be helpfulin minimizing the variability and thus could be useful inproducing equivalent directional force delivery to each sidewhen skull tapper is moved from left to right

5 Conclusions

In this paper we introduced our efforts in adding the ACVEMPs and tapVEMPs to expend the clinical diagnostic testsused for advanced assessment in CPAT patients hoping thatit will serve as a guideline for other clinicians interested inutilizing tap VEMPs

The patients presented in this study were selected topoint out different results we observed among a larger patientpopulation The findings from the larger population groupwill be presented in a more detailed follow-up subsequentpaper The main goal of this paper was to focus on theprotocol used and point at the variability in the findings

In two of three presented cases AC VEMPs and tapVEMPs together proved to be helpful in establishing thediagnosis of CPAT providingmore information on the tumoraffected bundle of vestibular nerve (superior or inferior orboth) Performing only AC VEMPs or only tap VEMPswould have provided insufficient information about thetumor and the vestibular nerve bundle involvement Inthe third case VEMPs failed to identify the vestibularschwannoma which was clearly shown in MRI scans Inthis case our medical intuition and expertise with CPATpatients prompted us to perform MRI Due to the high cost

10 BioMed Research International

of MRI it is typically not performed at the early stages ofthe diagnostics procedure in many countries Once othertests indicate the possible presence of the CPAT an MRI isconducted

Providing AC VEMPs and tap VEMPs to the availabletest battery in the assessment of CPAT is likely to improvethe diagnostic process by providing more information onthe involved vestibular nerve bundles In addition thisinformation might be used later during the surgery In manycases theMRI is not performed very short before the surgeryUsually it is performed earlier during the diagnostic processThe surgery takes place sometime after Asmentioned beforethe MRI is quite costly and usually is not performed againif not much time passed However the ABR AC VEMPsand tap VEMP once performed in diagnostic proceedingmight be repeated short before the surgery to clarify thepresence along with possible compression characteristics ofthe tumor on the vestibular andor auditory nerves Thiscombined information from earlier MRI scans and latestelectrophysiological tests serves the surgeons as a guidelinein their surgical approach and during tumor removal Itprovides very useful information for the surgeon in makinga decision about additional intraoperative monitoring ofhearing In our department intraoperative monitoring isroutinely used in every CPAT surgery and many otherear surgeries but intraoperative hearing monitoring is notroutinely performed in most of the other clinics In additionthe details from electrophysiological tests about the involvednerve bundles are useful in patients counseling and informingthem on more realistic possible outcomes of the surgery likehearing preservations possibilities and a risk of hearing lossduring the surgery a risk of facial nerve paresis and vertigosymptoms after the surgery

Abbreviations

ABR Auditory brainstem responseAS Asymmetry ratioCPAT Cerebellopontine angle tumorECochG ElectrocochleographyEEG ElectroencephalographyEMG ElectromiographyMRI Magnetic resonance imagingPTA Pure tone averageRMS Root means squaredSCM SternocleidomastoidVEMP Vestibular Evoked Myogenic PotentialAC VEMP Auditory Vestibular Evoked Myogenic

Potentialtap VEMP Skull tapping induced Vestibular

Evoked Myogenic Potential

AC VEMPsThree Types of Recordings

AHLL Head lift stimulus delivered to the left earAHLR Head lift stimulus delivered to the right earAHLB Head lift stimulus delivered to both ears

tap VEMPs Three Types of Recordings with Skull Tapper

FHLB Forehead head lift both sides recordedMHLL Mastoid head lift skull tapper located at leftMHLR Mastoid head lift skull tapper located at right

Conflict of Interests

The authors declare the following Dr Erdem Yavuz is aResearch Scientist at Research and Development IntelligentHearing Systems Inc andDr Rafael Delgado is the ExecutiveVice President and Director of Research and DevelopmentIntelligent Hearing Systems IncThe authors declare no otherconflict of interests related to this paper

References

[1] G von Bekesy ldquoUber akustische reizung des vestibularappa-ratesrdquo Pflugerrsquos Archiv fur die Gesamte Physiologie des Menschenund der Tiere vol 236 no 1 pp 59ndash76 1935

[2] J G Colebatch and G M Halmagyi ldquoVestibular evokedpotentials in human neck muscles before and after unilateralvestibular deafferentationrdquo Neurology vol 42 no 8 pp 1635ndash1636 1992

[3] J G Colebatch G M Halmagyi and N F Skuse ldquoMyogenicpotentials generated by a click-evoked vestibulocollic reflexrdquoJournal of Neurology Neurosurgery and Psychiatry vol 57 no2 pp 190ndash197 1994

[4] G M Halmagyi R A Yavor and J G Colebatch ldquoTapping thehead activates the vestibular system a new use for the clinicalreflex hammerrdquo Neurology vol 45 no 10 pp 1927ndash1929 1995

[5] K Sheykholeslami T Murofushi M H Kermany and KKaga ldquoBone-conducted evoked myogenic potentials from thesternocleidomastoid musclerdquo Acta Oto-Laryngologica vol 120no 6 pp 731ndash734 2000

[6] K Sheykholeslami M H Kermany and K Kaga ldquoFrequencysensitivity range of the saccule to bone-conducted stimulimeasured by vestibular evoked myogenic potentialsrdquo HearingResearch vol 160 no 1-2 pp 58ndash62 2001

[7] S R D Watson P Fagan and J G Colebatch ldquoGalvanicstimulation evokes short-latency EMG responses in sternoclei-domastoidwhich are abolished by selective vestibular nerve sec-tionrdquo Electroencephalography and Clinical NeurophysiologymdashElectromyography and Motor Control vol 109 no 6 pp 471ndash474 1998

[8] S R D Watson and J G Colebatch ldquoVestibular-evoked elec-tromyographic responses in soleus a comparison between clickand galvanic stimulationrdquo Experimental Brain Research vol 119no 4 pp 504ndash510 1998

[9] F Deriu E Tolu and J C Rothwell ldquoA sound-evoked vestibu-lomasseteric reflex in healthy humansrdquo Journal of Neurophysiol-ogy vol 93 no 5 pp 2739ndash2751 2005

[10] K Botzel P Feise O I Kolev S Krafczyk and T BrandtldquoErratum postural reflexes evoked by tapping forehead andchestrdquo Experimental Brain Research vol 140 no 2 p 251 2001

[11] S M Rosengren N P M Todd and J G ColebatchldquoVestibular-evoked extraocular potentials produced by stimula-tionwith bone-conducted soundrdquoClinical Neurophysiology vol116 no 8 pp 1938ndash1948 2005

[12] N P M Todd S M Rosengren S T Aw and J G ColebatchldquoOcular vestibular evoked myogenic potentials (OVEMPs)

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

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Oxidative Medicine and Cellular Longevity

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PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

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Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 6: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

6 BioMed Research International

Table1Au

ditory

andskulltap

VEM

Phead

liftresults

Patie

ntAnalyzed

parameter

Headlift

Auditory

Tapp

ingforehead

Tapp

ingmastoidsIPS

Irespo

nses

AHLB

AR(

)

AHLL

AHLR

AR(

)

FHLB

AR(

)

MHLL

MHLR

AR(

)Re

spon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

Respon

sefro

mleft

SCM

Respon

sefro

mrig

htSC

M

1P1

latency

(ms)

1320

1340

1340

1420

1320

1440

1400

1440

Corram

plitu

de2556

908

4759lowast

2296

862

4543lowast

3624

2459

1915

3367

2397

1684

2P1

latency

(ms)

1400

1360

1460

NR

1440

1520

1720

1560

Corram

plitu

de1314

518

4349lowast

2351

NR

3322

894

5760lowast

3819

916

6132lowast

3P1

latency

(ms)

1260

1280

1280

1300

1400

1360

1440

1320

Corram

plitu

de1019

1414

1626

1962

2940

1995

4488

3172

1718

5823

3940

1929

AHLB

headlift

stimulus

delivered

tobo

thearsA

HLL

headlift

stimulus

delivered

totheleftearAHLR

headlift

stimulus

delivered

totherig

htearFH

LBForeheadHeadLiftskulltapperlocated

atforehead

MHLL

Mastoid

HeadLiftskulltapperlocatedat

Left

MHLR

Mastoid

HeadLiftskulltapperlocatedat

RightP1p

ositive

peakcorram

plitu

decorrected

amplitu

deS

CMsternocleidom

astoid

muscle

AR

Asymmetry

ratio

NR

norespon

seA

bnormalresults

ofcorrectedasym

metry

ratio

s(ARgt35)a

ndno

respon

seresults

(NR)

arem

arkedwithlowast

BioMed Research International 7

AHLR

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

AHLL

(a)

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

AHLR

AHLL

(b)

AHLB

AHLL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

AHLR

(c)

Figure 2 VEMP waveforms recorded from all 3 subjects All the waveforms are normalized according to prestimulus EMG activity In thisfigure left side recordings are plotted as solid lines while right side recordings are plotted as dashed lines Abbreviations are used in thisfigure as follows AHLB auditory head lift both ear stimulation recorded bilaterally AHLL auditory head lift left ear stimulation recordedbilaterally AHLR auditory head lift right ear stimulation recorded bilaterally FHLB head lift recording tapper located at forehead recordedbilaterally MHLL head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at rightmastoid recorded bilaterally

tap VEMP results failed to point to a tumor presence TheMRI showed a tumor in the left internal auditory canal(7 times 5 times 15mm) During the surgical intervention thetumor was identified as arising from the superior vestibularnerve

In the postop versus preop comparison (Figure 3) of thehead lift AC VEMP recordings no significant change onthe tumor side was found when both ears were stimulatedHowever significant difference was shown when the stim-ulation was at the side of pathology For the tap VEMP

8 BioMed Research International

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

(a)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

(b)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

(c)

Figure 3 Preop (solid lines) and postop (dashed lines) VEMP waveforms recorded ipsilateral to the pathology from all 3 subjects Allthe waveforms are normalized according to prestimulus EMG activity Abbreviations are used in this figure as follows where ipsilateralindicates the location in return to the pathology location AHLB ipsilateral auditory head lift recording with both ears stimulated AHLipsilateral auditory head lift recording in return to ipsilateral stimulation FHLB ipsilateral head lift recording tapper located at foreheadMHL ipsilateral head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at ipsilateralmastoid

P1 peak could not be identified in any of the recordingsand N1 peak amplitudes were diminished in all recordingsexcept for the forehead placement where N1 latency andamplitude were preserved In general more variability inlatency and amplitude was also present for the later waves aswell

4 Discussion

In todayrsquos audiovestibular clinical practice a large numberof tests are available to determine the functionality of theaudiovestibular system The selection and the use of thesetests are mostly limited by their selectivity practicality and

BioMed Research International 9

costs The rapid development of VEMP related research andour recent experience with AC VEMPs and tap VEMPs haveled us to use VEMPs as an integral part of our diagnosticbattery In our department we routinely use the cervicalVEMPs due to the longer history thus there is larger amountof accumulated research on cervical VEMPs Currently weare also investigating the use of relatively newer approachof ocular VEMPs and adding it to our collected data setAlthough the recent research on ocular VEMPs has beenencouraging for clinical usage the technique has to still berefined to be used as a routine test The cervical VEMPs areeasy to acquire and can be efficiently used with quantificationmethods for ongoing muscle activity monitoring such asthe one used in this study where acceptance and rejectionmuscle activity regions are used Our near feature planis to include the ocular VEMPs recording in our routinediagnostic tests ensuring that the adaptation of the muscleactivity quantification methods we use is properly utilized

Our results showed that the VEMP recordings werenot only capable of identifying the CPAT but were alsoable to contribute additional information of involved nervebundles in first patient The observed abnormal audiologicalfindings strongly suggested the initial diagnosis of vestibularschwannoma The MRI pointed to the presence of a tumorlocated in the right internal auditory canal VEMP results alsosupported the presence of a tumor additionally pointing tothe inferior vestibular nerve involvementThe surgery reportdescribed the tumor to be arising from cochlear nerve and tobe attached to the other nerves in the internal auditory canalThe cochlear nerve is located closer to the inferior bundle ofthe vestibular nerve [34ndash36] and compression on the inferiornerve therefore was affecting the AC VEMPs results but notaltering the proper function of the superior vestibular nerve(AR in tap VEMPs within normal limits [38])

For the second patient the audiological results alongwith VNG and VEMP results strongly suggested the tumorpresence in the internal auditory canal which was supportedby theMRI findingsThe surgeon described the tumor arisingfrom superior vestibular nerve involving the inferior bundleas well During the surgery the tumor was found to be biggerthan initially described by the MRI which was performed afew months before As routinely done prior to the surgerythe other tests including VEMPs were performed to decideon the surgical approach and determine the possibility forhearing preservation In this case the tumor affected thefunction of all the nerves in the internal auditory canal Ourconclusion from the AC VEMP and tap VEMP findings wasthe involvement of both the inferior and superior nervesThe VEMPs were successful in pointing out both the tumorpresence and the involvement of both of the vestibularnerves An interesting observation was that the left andright responses recorded during both right side and left sideauditory stimulation were highly similar suggesting that thewhole response seen in AHLBmight have been driven by theleft ear

The third patient was a particularly interesting casebecause all tests performed along with AC VEMPs and tapVEMPs proved to be not helpful in the diagnosis of thevestibular schwannoma Although the tumor was arising

from the superior vestibular nerve the tap VEMP failed toindicate presence of the tumor similar to the rest of theclinical tools suggesting a normal function In this case onlythe MRI was sensitive enough to show the tumor The MRIwas performed due to the history of the patient her youngage and our experience in vestibular schwannoma casesThereason why the recorded tap VEMPs were not able to detectthe pathology is a good question to investigate

We observed that the mastoid placement of the skulltapper created additional challenges It was extremely difficultto replicate the same conditions when the skull tapper wasplaced on a surface of the mastoid region Due to the 3-dimensional shape of the mastoid area it was very difficultto maintain a steady 3D relation between the head and theskull tapper hit axis (thus with the vestibule axis) especiallywhen tapper is moved from one side to the other As with thecurrent setup there was no chance of monitoring the relationbetween the skull tapper hit direction and the vestibularorgans and it was not possible to limit the introducedvariability In the light of these observations (although weacquired data with skull tapper positioned at mastoids onboth sides and described the results of the responses acquiredfrom the ipsilateral SMCs) we preferred to relay and advocatethe usage of the forehead stimulation results due to the limitsof currently available instrumentation The directional infor-mation revealed by themastoid placement is complex and hasto be carefully analyzed For general clinical implementationadditional safeguards are required An additional feedbackmechanism describing the orientation relation between thetapper and gravity such as a gyroscope could be helpfulin minimizing the variability and thus could be useful inproducing equivalent directional force delivery to each sidewhen skull tapper is moved from left to right

5 Conclusions

In this paper we introduced our efforts in adding the ACVEMPs and tapVEMPs to expend the clinical diagnostic testsused for advanced assessment in CPAT patients hoping thatit will serve as a guideline for other clinicians interested inutilizing tap VEMPs

The patients presented in this study were selected topoint out different results we observed among a larger patientpopulation The findings from the larger population groupwill be presented in a more detailed follow-up subsequentpaper The main goal of this paper was to focus on theprotocol used and point at the variability in the findings

In two of three presented cases AC VEMPs and tapVEMPs together proved to be helpful in establishing thediagnosis of CPAT providingmore information on the tumoraffected bundle of vestibular nerve (superior or inferior orboth) Performing only AC VEMPs or only tap VEMPswould have provided insufficient information about thetumor and the vestibular nerve bundle involvement Inthe third case VEMPs failed to identify the vestibularschwannoma which was clearly shown in MRI scans Inthis case our medical intuition and expertise with CPATpatients prompted us to perform MRI Due to the high cost

10 BioMed Research International

of MRI it is typically not performed at the early stages ofthe diagnostics procedure in many countries Once othertests indicate the possible presence of the CPAT an MRI isconducted

Providing AC VEMPs and tap VEMPs to the availabletest battery in the assessment of CPAT is likely to improvethe diagnostic process by providing more information onthe involved vestibular nerve bundles In addition thisinformation might be used later during the surgery In manycases theMRI is not performed very short before the surgeryUsually it is performed earlier during the diagnostic processThe surgery takes place sometime after Asmentioned beforethe MRI is quite costly and usually is not performed againif not much time passed However the ABR AC VEMPsand tap VEMP once performed in diagnostic proceedingmight be repeated short before the surgery to clarify thepresence along with possible compression characteristics ofthe tumor on the vestibular andor auditory nerves Thiscombined information from earlier MRI scans and latestelectrophysiological tests serves the surgeons as a guidelinein their surgical approach and during tumor removal Itprovides very useful information for the surgeon in makinga decision about additional intraoperative monitoring ofhearing In our department intraoperative monitoring isroutinely used in every CPAT surgery and many otherear surgeries but intraoperative hearing monitoring is notroutinely performed in most of the other clinics In additionthe details from electrophysiological tests about the involvednerve bundles are useful in patients counseling and informingthem on more realistic possible outcomes of the surgery likehearing preservations possibilities and a risk of hearing lossduring the surgery a risk of facial nerve paresis and vertigosymptoms after the surgery

Abbreviations

ABR Auditory brainstem responseAS Asymmetry ratioCPAT Cerebellopontine angle tumorECochG ElectrocochleographyEEG ElectroencephalographyEMG ElectromiographyMRI Magnetic resonance imagingPTA Pure tone averageRMS Root means squaredSCM SternocleidomastoidVEMP Vestibular Evoked Myogenic PotentialAC VEMP Auditory Vestibular Evoked Myogenic

Potentialtap VEMP Skull tapping induced Vestibular

Evoked Myogenic Potential

AC VEMPsThree Types of Recordings

AHLL Head lift stimulus delivered to the left earAHLR Head lift stimulus delivered to the right earAHLB Head lift stimulus delivered to both ears

tap VEMPs Three Types of Recordings with Skull Tapper

FHLB Forehead head lift both sides recordedMHLL Mastoid head lift skull tapper located at leftMHLR Mastoid head lift skull tapper located at right

Conflict of Interests

The authors declare the following Dr Erdem Yavuz is aResearch Scientist at Research and Development IntelligentHearing Systems Inc andDr Rafael Delgado is the ExecutiveVice President and Director of Research and DevelopmentIntelligent Hearing Systems IncThe authors declare no otherconflict of interests related to this paper

References

[1] G von Bekesy ldquoUber akustische reizung des vestibularappa-ratesrdquo Pflugerrsquos Archiv fur die Gesamte Physiologie des Menschenund der Tiere vol 236 no 1 pp 59ndash76 1935

[2] J G Colebatch and G M Halmagyi ldquoVestibular evokedpotentials in human neck muscles before and after unilateralvestibular deafferentationrdquo Neurology vol 42 no 8 pp 1635ndash1636 1992

[3] J G Colebatch G M Halmagyi and N F Skuse ldquoMyogenicpotentials generated by a click-evoked vestibulocollic reflexrdquoJournal of Neurology Neurosurgery and Psychiatry vol 57 no2 pp 190ndash197 1994

[4] G M Halmagyi R A Yavor and J G Colebatch ldquoTapping thehead activates the vestibular system a new use for the clinicalreflex hammerrdquo Neurology vol 45 no 10 pp 1927ndash1929 1995

[5] K Sheykholeslami T Murofushi M H Kermany and KKaga ldquoBone-conducted evoked myogenic potentials from thesternocleidomastoid musclerdquo Acta Oto-Laryngologica vol 120no 6 pp 731ndash734 2000

[6] K Sheykholeslami M H Kermany and K Kaga ldquoFrequencysensitivity range of the saccule to bone-conducted stimulimeasured by vestibular evoked myogenic potentialsrdquo HearingResearch vol 160 no 1-2 pp 58ndash62 2001

[7] S R D Watson P Fagan and J G Colebatch ldquoGalvanicstimulation evokes short-latency EMG responses in sternoclei-domastoidwhich are abolished by selective vestibular nerve sec-tionrdquo Electroencephalography and Clinical NeurophysiologymdashElectromyography and Motor Control vol 109 no 6 pp 471ndash474 1998

[8] S R D Watson and J G Colebatch ldquoVestibular-evoked elec-tromyographic responses in soleus a comparison between clickand galvanic stimulationrdquo Experimental Brain Research vol 119no 4 pp 504ndash510 1998

[9] F Deriu E Tolu and J C Rothwell ldquoA sound-evoked vestibu-lomasseteric reflex in healthy humansrdquo Journal of Neurophysiol-ogy vol 93 no 5 pp 2739ndash2751 2005

[10] K Botzel P Feise O I Kolev S Krafczyk and T BrandtldquoErratum postural reflexes evoked by tapping forehead andchestrdquo Experimental Brain Research vol 140 no 2 p 251 2001

[11] S M Rosengren N P M Todd and J G ColebatchldquoVestibular-evoked extraocular potentials produced by stimula-tionwith bone-conducted soundrdquoClinical Neurophysiology vol116 no 8 pp 1938ndash1948 2005

[12] N P M Todd S M Rosengren S T Aw and J G ColebatchldquoOcular vestibular evoked myogenic potentials (OVEMPs)

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 7: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

BioMed Research International 7

AHLR

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

AHLL

(a)

AHLB

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

AHLR

AHLL

(b)

AHLB

AHLL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

AHLR

(c)

Figure 2 VEMP waveforms recorded from all 3 subjects All the waveforms are normalized according to prestimulus EMG activity In thisfigure left side recordings are plotted as solid lines while right side recordings are plotted as dashed lines Abbreviations are used in thisfigure as follows AHLB auditory head lift both ear stimulation recorded bilaterally AHLL auditory head lift left ear stimulation recordedbilaterally AHLR auditory head lift right ear stimulation recorded bilaterally FHLB head lift recording tapper located at forehead recordedbilaterally MHLL head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at rightmastoid recorded bilaterally

tap VEMP results failed to point to a tumor presence TheMRI showed a tumor in the left internal auditory canal(7 times 5 times 15mm) During the surgical intervention thetumor was identified as arising from the superior vestibularnerve

In the postop versus preop comparison (Figure 3) of thehead lift AC VEMP recordings no significant change onthe tumor side was found when both ears were stimulatedHowever significant difference was shown when the stim-ulation was at the side of pathology For the tap VEMP

8 BioMed Research International

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

(a)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

(b)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

(c)

Figure 3 Preop (solid lines) and postop (dashed lines) VEMP waveforms recorded ipsilateral to the pathology from all 3 subjects Allthe waveforms are normalized according to prestimulus EMG activity Abbreviations are used in this figure as follows where ipsilateralindicates the location in return to the pathology location AHLB ipsilateral auditory head lift recording with both ears stimulated AHLipsilateral auditory head lift recording in return to ipsilateral stimulation FHLB ipsilateral head lift recording tapper located at foreheadMHL ipsilateral head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at ipsilateralmastoid

P1 peak could not be identified in any of the recordingsand N1 peak amplitudes were diminished in all recordingsexcept for the forehead placement where N1 latency andamplitude were preserved In general more variability inlatency and amplitude was also present for the later waves aswell

4 Discussion

In todayrsquos audiovestibular clinical practice a large numberof tests are available to determine the functionality of theaudiovestibular system The selection and the use of thesetests are mostly limited by their selectivity practicality and

BioMed Research International 9

costs The rapid development of VEMP related research andour recent experience with AC VEMPs and tap VEMPs haveled us to use VEMPs as an integral part of our diagnosticbattery In our department we routinely use the cervicalVEMPs due to the longer history thus there is larger amountof accumulated research on cervical VEMPs Currently weare also investigating the use of relatively newer approachof ocular VEMPs and adding it to our collected data setAlthough the recent research on ocular VEMPs has beenencouraging for clinical usage the technique has to still berefined to be used as a routine test The cervical VEMPs areeasy to acquire and can be efficiently used with quantificationmethods for ongoing muscle activity monitoring such asthe one used in this study where acceptance and rejectionmuscle activity regions are used Our near feature planis to include the ocular VEMPs recording in our routinediagnostic tests ensuring that the adaptation of the muscleactivity quantification methods we use is properly utilized

Our results showed that the VEMP recordings werenot only capable of identifying the CPAT but were alsoable to contribute additional information of involved nervebundles in first patient The observed abnormal audiologicalfindings strongly suggested the initial diagnosis of vestibularschwannoma The MRI pointed to the presence of a tumorlocated in the right internal auditory canal VEMP results alsosupported the presence of a tumor additionally pointing tothe inferior vestibular nerve involvementThe surgery reportdescribed the tumor to be arising from cochlear nerve and tobe attached to the other nerves in the internal auditory canalThe cochlear nerve is located closer to the inferior bundle ofthe vestibular nerve [34ndash36] and compression on the inferiornerve therefore was affecting the AC VEMPs results but notaltering the proper function of the superior vestibular nerve(AR in tap VEMPs within normal limits [38])

For the second patient the audiological results alongwith VNG and VEMP results strongly suggested the tumorpresence in the internal auditory canal which was supportedby theMRI findingsThe surgeon described the tumor arisingfrom superior vestibular nerve involving the inferior bundleas well During the surgery the tumor was found to be biggerthan initially described by the MRI which was performed afew months before As routinely done prior to the surgerythe other tests including VEMPs were performed to decideon the surgical approach and determine the possibility forhearing preservation In this case the tumor affected thefunction of all the nerves in the internal auditory canal Ourconclusion from the AC VEMP and tap VEMP findings wasthe involvement of both the inferior and superior nervesThe VEMPs were successful in pointing out both the tumorpresence and the involvement of both of the vestibularnerves An interesting observation was that the left andright responses recorded during both right side and left sideauditory stimulation were highly similar suggesting that thewhole response seen in AHLBmight have been driven by theleft ear

The third patient was a particularly interesting casebecause all tests performed along with AC VEMPs and tapVEMPs proved to be not helpful in the diagnosis of thevestibular schwannoma Although the tumor was arising

from the superior vestibular nerve the tap VEMP failed toindicate presence of the tumor similar to the rest of theclinical tools suggesting a normal function In this case onlythe MRI was sensitive enough to show the tumor The MRIwas performed due to the history of the patient her youngage and our experience in vestibular schwannoma casesThereason why the recorded tap VEMPs were not able to detectthe pathology is a good question to investigate

We observed that the mastoid placement of the skulltapper created additional challenges It was extremely difficultto replicate the same conditions when the skull tapper wasplaced on a surface of the mastoid region Due to the 3-dimensional shape of the mastoid area it was very difficultto maintain a steady 3D relation between the head and theskull tapper hit axis (thus with the vestibule axis) especiallywhen tapper is moved from one side to the other As with thecurrent setup there was no chance of monitoring the relationbetween the skull tapper hit direction and the vestibularorgans and it was not possible to limit the introducedvariability In the light of these observations (although weacquired data with skull tapper positioned at mastoids onboth sides and described the results of the responses acquiredfrom the ipsilateral SMCs) we preferred to relay and advocatethe usage of the forehead stimulation results due to the limitsof currently available instrumentation The directional infor-mation revealed by themastoid placement is complex and hasto be carefully analyzed For general clinical implementationadditional safeguards are required An additional feedbackmechanism describing the orientation relation between thetapper and gravity such as a gyroscope could be helpfulin minimizing the variability and thus could be useful inproducing equivalent directional force delivery to each sidewhen skull tapper is moved from left to right

5 Conclusions

In this paper we introduced our efforts in adding the ACVEMPs and tapVEMPs to expend the clinical diagnostic testsused for advanced assessment in CPAT patients hoping thatit will serve as a guideline for other clinicians interested inutilizing tap VEMPs

The patients presented in this study were selected topoint out different results we observed among a larger patientpopulation The findings from the larger population groupwill be presented in a more detailed follow-up subsequentpaper The main goal of this paper was to focus on theprotocol used and point at the variability in the findings

In two of three presented cases AC VEMPs and tapVEMPs together proved to be helpful in establishing thediagnosis of CPAT providingmore information on the tumoraffected bundle of vestibular nerve (superior or inferior orboth) Performing only AC VEMPs or only tap VEMPswould have provided insufficient information about thetumor and the vestibular nerve bundle involvement Inthe third case VEMPs failed to identify the vestibularschwannoma which was clearly shown in MRI scans Inthis case our medical intuition and expertise with CPATpatients prompted us to perform MRI Due to the high cost

10 BioMed Research International

of MRI it is typically not performed at the early stages ofthe diagnostics procedure in many countries Once othertests indicate the possible presence of the CPAT an MRI isconducted

Providing AC VEMPs and tap VEMPs to the availabletest battery in the assessment of CPAT is likely to improvethe diagnostic process by providing more information onthe involved vestibular nerve bundles In addition thisinformation might be used later during the surgery In manycases theMRI is not performed very short before the surgeryUsually it is performed earlier during the diagnostic processThe surgery takes place sometime after Asmentioned beforethe MRI is quite costly and usually is not performed againif not much time passed However the ABR AC VEMPsand tap VEMP once performed in diagnostic proceedingmight be repeated short before the surgery to clarify thepresence along with possible compression characteristics ofthe tumor on the vestibular andor auditory nerves Thiscombined information from earlier MRI scans and latestelectrophysiological tests serves the surgeons as a guidelinein their surgical approach and during tumor removal Itprovides very useful information for the surgeon in makinga decision about additional intraoperative monitoring ofhearing In our department intraoperative monitoring isroutinely used in every CPAT surgery and many otherear surgeries but intraoperative hearing monitoring is notroutinely performed in most of the other clinics In additionthe details from electrophysiological tests about the involvednerve bundles are useful in patients counseling and informingthem on more realistic possible outcomes of the surgery likehearing preservations possibilities and a risk of hearing lossduring the surgery a risk of facial nerve paresis and vertigosymptoms after the surgery

Abbreviations

ABR Auditory brainstem responseAS Asymmetry ratioCPAT Cerebellopontine angle tumorECochG ElectrocochleographyEEG ElectroencephalographyEMG ElectromiographyMRI Magnetic resonance imagingPTA Pure tone averageRMS Root means squaredSCM SternocleidomastoidVEMP Vestibular Evoked Myogenic PotentialAC VEMP Auditory Vestibular Evoked Myogenic

Potentialtap VEMP Skull tapping induced Vestibular

Evoked Myogenic Potential

AC VEMPsThree Types of Recordings

AHLL Head lift stimulus delivered to the left earAHLR Head lift stimulus delivered to the right earAHLB Head lift stimulus delivered to both ears

tap VEMPs Three Types of Recordings with Skull Tapper

FHLB Forehead head lift both sides recordedMHLL Mastoid head lift skull tapper located at leftMHLR Mastoid head lift skull tapper located at right

Conflict of Interests

The authors declare the following Dr Erdem Yavuz is aResearch Scientist at Research and Development IntelligentHearing Systems Inc andDr Rafael Delgado is the ExecutiveVice President and Director of Research and DevelopmentIntelligent Hearing Systems IncThe authors declare no otherconflict of interests related to this paper

References

[1] G von Bekesy ldquoUber akustische reizung des vestibularappa-ratesrdquo Pflugerrsquos Archiv fur die Gesamte Physiologie des Menschenund der Tiere vol 236 no 1 pp 59ndash76 1935

[2] J G Colebatch and G M Halmagyi ldquoVestibular evokedpotentials in human neck muscles before and after unilateralvestibular deafferentationrdquo Neurology vol 42 no 8 pp 1635ndash1636 1992

[3] J G Colebatch G M Halmagyi and N F Skuse ldquoMyogenicpotentials generated by a click-evoked vestibulocollic reflexrdquoJournal of Neurology Neurosurgery and Psychiatry vol 57 no2 pp 190ndash197 1994

[4] G M Halmagyi R A Yavor and J G Colebatch ldquoTapping thehead activates the vestibular system a new use for the clinicalreflex hammerrdquo Neurology vol 45 no 10 pp 1927ndash1929 1995

[5] K Sheykholeslami T Murofushi M H Kermany and KKaga ldquoBone-conducted evoked myogenic potentials from thesternocleidomastoid musclerdquo Acta Oto-Laryngologica vol 120no 6 pp 731ndash734 2000

[6] K Sheykholeslami M H Kermany and K Kaga ldquoFrequencysensitivity range of the saccule to bone-conducted stimulimeasured by vestibular evoked myogenic potentialsrdquo HearingResearch vol 160 no 1-2 pp 58ndash62 2001

[7] S R D Watson P Fagan and J G Colebatch ldquoGalvanicstimulation evokes short-latency EMG responses in sternoclei-domastoidwhich are abolished by selective vestibular nerve sec-tionrdquo Electroencephalography and Clinical NeurophysiologymdashElectromyography and Motor Control vol 109 no 6 pp 471ndash474 1998

[8] S R D Watson and J G Colebatch ldquoVestibular-evoked elec-tromyographic responses in soleus a comparison between clickand galvanic stimulationrdquo Experimental Brain Research vol 119no 4 pp 504ndash510 1998

[9] F Deriu E Tolu and J C Rothwell ldquoA sound-evoked vestibu-lomasseteric reflex in healthy humansrdquo Journal of Neurophysiol-ogy vol 93 no 5 pp 2739ndash2751 2005

[10] K Botzel P Feise O I Kolev S Krafczyk and T BrandtldquoErratum postural reflexes evoked by tapping forehead andchestrdquo Experimental Brain Research vol 140 no 2 p 251 2001

[11] S M Rosengren N P M Todd and J G ColebatchldquoVestibular-evoked extraocular potentials produced by stimula-tionwith bone-conducted soundrdquoClinical Neurophysiology vol116 no 8 pp 1938ndash1948 2005

[12] N P M Todd S M Rosengren S T Aw and J G ColebatchldquoOcular vestibular evoked myogenic potentials (OVEMPs)

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 8: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

8 BioMed Research International

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 1

(ms)

(a)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 2

(ms)

(b)

IPSI

AHLB

AHL

FHLB

MHLL

MHLR

0 20 40 60 80

Subject 3

(ms)

(c)

Figure 3 Preop (solid lines) and postop (dashed lines) VEMP waveforms recorded ipsilateral to the pathology from all 3 subjects Allthe waveforms are normalized according to prestimulus EMG activity Abbreviations are used in this figure as follows where ipsilateralindicates the location in return to the pathology location AHLB ipsilateral auditory head lift recording with both ears stimulated AHLipsilateral auditory head lift recording in return to ipsilateral stimulation FHLB ipsilateral head lift recording tapper located at foreheadMHL ipsilateral head lift recording tapper located at left mastoid recorded bilaterally MHLR head lift recording tapper located at ipsilateralmastoid

P1 peak could not be identified in any of the recordingsand N1 peak amplitudes were diminished in all recordingsexcept for the forehead placement where N1 latency andamplitude were preserved In general more variability inlatency and amplitude was also present for the later waves aswell

4 Discussion

In todayrsquos audiovestibular clinical practice a large numberof tests are available to determine the functionality of theaudiovestibular system The selection and the use of thesetests are mostly limited by their selectivity practicality and

BioMed Research International 9

costs The rapid development of VEMP related research andour recent experience with AC VEMPs and tap VEMPs haveled us to use VEMPs as an integral part of our diagnosticbattery In our department we routinely use the cervicalVEMPs due to the longer history thus there is larger amountof accumulated research on cervical VEMPs Currently weare also investigating the use of relatively newer approachof ocular VEMPs and adding it to our collected data setAlthough the recent research on ocular VEMPs has beenencouraging for clinical usage the technique has to still berefined to be used as a routine test The cervical VEMPs areeasy to acquire and can be efficiently used with quantificationmethods for ongoing muscle activity monitoring such asthe one used in this study where acceptance and rejectionmuscle activity regions are used Our near feature planis to include the ocular VEMPs recording in our routinediagnostic tests ensuring that the adaptation of the muscleactivity quantification methods we use is properly utilized

Our results showed that the VEMP recordings werenot only capable of identifying the CPAT but were alsoable to contribute additional information of involved nervebundles in first patient The observed abnormal audiologicalfindings strongly suggested the initial diagnosis of vestibularschwannoma The MRI pointed to the presence of a tumorlocated in the right internal auditory canal VEMP results alsosupported the presence of a tumor additionally pointing tothe inferior vestibular nerve involvementThe surgery reportdescribed the tumor to be arising from cochlear nerve and tobe attached to the other nerves in the internal auditory canalThe cochlear nerve is located closer to the inferior bundle ofthe vestibular nerve [34ndash36] and compression on the inferiornerve therefore was affecting the AC VEMPs results but notaltering the proper function of the superior vestibular nerve(AR in tap VEMPs within normal limits [38])

For the second patient the audiological results alongwith VNG and VEMP results strongly suggested the tumorpresence in the internal auditory canal which was supportedby theMRI findingsThe surgeon described the tumor arisingfrom superior vestibular nerve involving the inferior bundleas well During the surgery the tumor was found to be biggerthan initially described by the MRI which was performed afew months before As routinely done prior to the surgerythe other tests including VEMPs were performed to decideon the surgical approach and determine the possibility forhearing preservation In this case the tumor affected thefunction of all the nerves in the internal auditory canal Ourconclusion from the AC VEMP and tap VEMP findings wasthe involvement of both the inferior and superior nervesThe VEMPs were successful in pointing out both the tumorpresence and the involvement of both of the vestibularnerves An interesting observation was that the left andright responses recorded during both right side and left sideauditory stimulation were highly similar suggesting that thewhole response seen in AHLBmight have been driven by theleft ear

The third patient was a particularly interesting casebecause all tests performed along with AC VEMPs and tapVEMPs proved to be not helpful in the diagnosis of thevestibular schwannoma Although the tumor was arising

from the superior vestibular nerve the tap VEMP failed toindicate presence of the tumor similar to the rest of theclinical tools suggesting a normal function In this case onlythe MRI was sensitive enough to show the tumor The MRIwas performed due to the history of the patient her youngage and our experience in vestibular schwannoma casesThereason why the recorded tap VEMPs were not able to detectthe pathology is a good question to investigate

We observed that the mastoid placement of the skulltapper created additional challenges It was extremely difficultto replicate the same conditions when the skull tapper wasplaced on a surface of the mastoid region Due to the 3-dimensional shape of the mastoid area it was very difficultto maintain a steady 3D relation between the head and theskull tapper hit axis (thus with the vestibule axis) especiallywhen tapper is moved from one side to the other As with thecurrent setup there was no chance of monitoring the relationbetween the skull tapper hit direction and the vestibularorgans and it was not possible to limit the introducedvariability In the light of these observations (although weacquired data with skull tapper positioned at mastoids onboth sides and described the results of the responses acquiredfrom the ipsilateral SMCs) we preferred to relay and advocatethe usage of the forehead stimulation results due to the limitsof currently available instrumentation The directional infor-mation revealed by themastoid placement is complex and hasto be carefully analyzed For general clinical implementationadditional safeguards are required An additional feedbackmechanism describing the orientation relation between thetapper and gravity such as a gyroscope could be helpfulin minimizing the variability and thus could be useful inproducing equivalent directional force delivery to each sidewhen skull tapper is moved from left to right

5 Conclusions

In this paper we introduced our efforts in adding the ACVEMPs and tapVEMPs to expend the clinical diagnostic testsused for advanced assessment in CPAT patients hoping thatit will serve as a guideline for other clinicians interested inutilizing tap VEMPs

The patients presented in this study were selected topoint out different results we observed among a larger patientpopulation The findings from the larger population groupwill be presented in a more detailed follow-up subsequentpaper The main goal of this paper was to focus on theprotocol used and point at the variability in the findings

In two of three presented cases AC VEMPs and tapVEMPs together proved to be helpful in establishing thediagnosis of CPAT providingmore information on the tumoraffected bundle of vestibular nerve (superior or inferior orboth) Performing only AC VEMPs or only tap VEMPswould have provided insufficient information about thetumor and the vestibular nerve bundle involvement Inthe third case VEMPs failed to identify the vestibularschwannoma which was clearly shown in MRI scans Inthis case our medical intuition and expertise with CPATpatients prompted us to perform MRI Due to the high cost

10 BioMed Research International

of MRI it is typically not performed at the early stages ofthe diagnostics procedure in many countries Once othertests indicate the possible presence of the CPAT an MRI isconducted

Providing AC VEMPs and tap VEMPs to the availabletest battery in the assessment of CPAT is likely to improvethe diagnostic process by providing more information onthe involved vestibular nerve bundles In addition thisinformation might be used later during the surgery In manycases theMRI is not performed very short before the surgeryUsually it is performed earlier during the diagnostic processThe surgery takes place sometime after Asmentioned beforethe MRI is quite costly and usually is not performed againif not much time passed However the ABR AC VEMPsand tap VEMP once performed in diagnostic proceedingmight be repeated short before the surgery to clarify thepresence along with possible compression characteristics ofthe tumor on the vestibular andor auditory nerves Thiscombined information from earlier MRI scans and latestelectrophysiological tests serves the surgeons as a guidelinein their surgical approach and during tumor removal Itprovides very useful information for the surgeon in makinga decision about additional intraoperative monitoring ofhearing In our department intraoperative monitoring isroutinely used in every CPAT surgery and many otherear surgeries but intraoperative hearing monitoring is notroutinely performed in most of the other clinics In additionthe details from electrophysiological tests about the involvednerve bundles are useful in patients counseling and informingthem on more realistic possible outcomes of the surgery likehearing preservations possibilities and a risk of hearing lossduring the surgery a risk of facial nerve paresis and vertigosymptoms after the surgery

Abbreviations

ABR Auditory brainstem responseAS Asymmetry ratioCPAT Cerebellopontine angle tumorECochG ElectrocochleographyEEG ElectroencephalographyEMG ElectromiographyMRI Magnetic resonance imagingPTA Pure tone averageRMS Root means squaredSCM SternocleidomastoidVEMP Vestibular Evoked Myogenic PotentialAC VEMP Auditory Vestibular Evoked Myogenic

Potentialtap VEMP Skull tapping induced Vestibular

Evoked Myogenic Potential

AC VEMPsThree Types of Recordings

AHLL Head lift stimulus delivered to the left earAHLR Head lift stimulus delivered to the right earAHLB Head lift stimulus delivered to both ears

tap VEMPs Three Types of Recordings with Skull Tapper

FHLB Forehead head lift both sides recordedMHLL Mastoid head lift skull tapper located at leftMHLR Mastoid head lift skull tapper located at right

Conflict of Interests

The authors declare the following Dr Erdem Yavuz is aResearch Scientist at Research and Development IntelligentHearing Systems Inc andDr Rafael Delgado is the ExecutiveVice President and Director of Research and DevelopmentIntelligent Hearing Systems IncThe authors declare no otherconflict of interests related to this paper

References

[1] G von Bekesy ldquoUber akustische reizung des vestibularappa-ratesrdquo Pflugerrsquos Archiv fur die Gesamte Physiologie des Menschenund der Tiere vol 236 no 1 pp 59ndash76 1935

[2] J G Colebatch and G M Halmagyi ldquoVestibular evokedpotentials in human neck muscles before and after unilateralvestibular deafferentationrdquo Neurology vol 42 no 8 pp 1635ndash1636 1992

[3] J G Colebatch G M Halmagyi and N F Skuse ldquoMyogenicpotentials generated by a click-evoked vestibulocollic reflexrdquoJournal of Neurology Neurosurgery and Psychiatry vol 57 no2 pp 190ndash197 1994

[4] G M Halmagyi R A Yavor and J G Colebatch ldquoTapping thehead activates the vestibular system a new use for the clinicalreflex hammerrdquo Neurology vol 45 no 10 pp 1927ndash1929 1995

[5] K Sheykholeslami T Murofushi M H Kermany and KKaga ldquoBone-conducted evoked myogenic potentials from thesternocleidomastoid musclerdquo Acta Oto-Laryngologica vol 120no 6 pp 731ndash734 2000

[6] K Sheykholeslami M H Kermany and K Kaga ldquoFrequencysensitivity range of the saccule to bone-conducted stimulimeasured by vestibular evoked myogenic potentialsrdquo HearingResearch vol 160 no 1-2 pp 58ndash62 2001

[7] S R D Watson P Fagan and J G Colebatch ldquoGalvanicstimulation evokes short-latency EMG responses in sternoclei-domastoidwhich are abolished by selective vestibular nerve sec-tionrdquo Electroencephalography and Clinical NeurophysiologymdashElectromyography and Motor Control vol 109 no 6 pp 471ndash474 1998

[8] S R D Watson and J G Colebatch ldquoVestibular-evoked elec-tromyographic responses in soleus a comparison between clickand galvanic stimulationrdquo Experimental Brain Research vol 119no 4 pp 504ndash510 1998

[9] F Deriu E Tolu and J C Rothwell ldquoA sound-evoked vestibu-lomasseteric reflex in healthy humansrdquo Journal of Neurophysiol-ogy vol 93 no 5 pp 2739ndash2751 2005

[10] K Botzel P Feise O I Kolev S Krafczyk and T BrandtldquoErratum postural reflexes evoked by tapping forehead andchestrdquo Experimental Brain Research vol 140 no 2 p 251 2001

[11] S M Rosengren N P M Todd and J G ColebatchldquoVestibular-evoked extraocular potentials produced by stimula-tionwith bone-conducted soundrdquoClinical Neurophysiology vol116 no 8 pp 1938ndash1948 2005

[12] N P M Todd S M Rosengren S T Aw and J G ColebatchldquoOcular vestibular evoked myogenic potentials (OVEMPs)

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 9: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

BioMed Research International 9

costs The rapid development of VEMP related research andour recent experience with AC VEMPs and tap VEMPs haveled us to use VEMPs as an integral part of our diagnosticbattery In our department we routinely use the cervicalVEMPs due to the longer history thus there is larger amountof accumulated research on cervical VEMPs Currently weare also investigating the use of relatively newer approachof ocular VEMPs and adding it to our collected data setAlthough the recent research on ocular VEMPs has beenencouraging for clinical usage the technique has to still berefined to be used as a routine test The cervical VEMPs areeasy to acquire and can be efficiently used with quantificationmethods for ongoing muscle activity monitoring such asthe one used in this study where acceptance and rejectionmuscle activity regions are used Our near feature planis to include the ocular VEMPs recording in our routinediagnostic tests ensuring that the adaptation of the muscleactivity quantification methods we use is properly utilized

Our results showed that the VEMP recordings werenot only capable of identifying the CPAT but were alsoable to contribute additional information of involved nervebundles in first patient The observed abnormal audiologicalfindings strongly suggested the initial diagnosis of vestibularschwannoma The MRI pointed to the presence of a tumorlocated in the right internal auditory canal VEMP results alsosupported the presence of a tumor additionally pointing tothe inferior vestibular nerve involvementThe surgery reportdescribed the tumor to be arising from cochlear nerve and tobe attached to the other nerves in the internal auditory canalThe cochlear nerve is located closer to the inferior bundle ofthe vestibular nerve [34ndash36] and compression on the inferiornerve therefore was affecting the AC VEMPs results but notaltering the proper function of the superior vestibular nerve(AR in tap VEMPs within normal limits [38])

For the second patient the audiological results alongwith VNG and VEMP results strongly suggested the tumorpresence in the internal auditory canal which was supportedby theMRI findingsThe surgeon described the tumor arisingfrom superior vestibular nerve involving the inferior bundleas well During the surgery the tumor was found to be biggerthan initially described by the MRI which was performed afew months before As routinely done prior to the surgerythe other tests including VEMPs were performed to decideon the surgical approach and determine the possibility forhearing preservation In this case the tumor affected thefunction of all the nerves in the internal auditory canal Ourconclusion from the AC VEMP and tap VEMP findings wasthe involvement of both the inferior and superior nervesThe VEMPs were successful in pointing out both the tumorpresence and the involvement of both of the vestibularnerves An interesting observation was that the left andright responses recorded during both right side and left sideauditory stimulation were highly similar suggesting that thewhole response seen in AHLBmight have been driven by theleft ear

The third patient was a particularly interesting casebecause all tests performed along with AC VEMPs and tapVEMPs proved to be not helpful in the diagnosis of thevestibular schwannoma Although the tumor was arising

from the superior vestibular nerve the tap VEMP failed toindicate presence of the tumor similar to the rest of theclinical tools suggesting a normal function In this case onlythe MRI was sensitive enough to show the tumor The MRIwas performed due to the history of the patient her youngage and our experience in vestibular schwannoma casesThereason why the recorded tap VEMPs were not able to detectthe pathology is a good question to investigate

We observed that the mastoid placement of the skulltapper created additional challenges It was extremely difficultto replicate the same conditions when the skull tapper wasplaced on a surface of the mastoid region Due to the 3-dimensional shape of the mastoid area it was very difficultto maintain a steady 3D relation between the head and theskull tapper hit axis (thus with the vestibule axis) especiallywhen tapper is moved from one side to the other As with thecurrent setup there was no chance of monitoring the relationbetween the skull tapper hit direction and the vestibularorgans and it was not possible to limit the introducedvariability In the light of these observations (although weacquired data with skull tapper positioned at mastoids onboth sides and described the results of the responses acquiredfrom the ipsilateral SMCs) we preferred to relay and advocatethe usage of the forehead stimulation results due to the limitsof currently available instrumentation The directional infor-mation revealed by themastoid placement is complex and hasto be carefully analyzed For general clinical implementationadditional safeguards are required An additional feedbackmechanism describing the orientation relation between thetapper and gravity such as a gyroscope could be helpfulin minimizing the variability and thus could be useful inproducing equivalent directional force delivery to each sidewhen skull tapper is moved from left to right

5 Conclusions

In this paper we introduced our efforts in adding the ACVEMPs and tapVEMPs to expend the clinical diagnostic testsused for advanced assessment in CPAT patients hoping thatit will serve as a guideline for other clinicians interested inutilizing tap VEMPs

The patients presented in this study were selected topoint out different results we observed among a larger patientpopulation The findings from the larger population groupwill be presented in a more detailed follow-up subsequentpaper The main goal of this paper was to focus on theprotocol used and point at the variability in the findings

In two of three presented cases AC VEMPs and tapVEMPs together proved to be helpful in establishing thediagnosis of CPAT providingmore information on the tumoraffected bundle of vestibular nerve (superior or inferior orboth) Performing only AC VEMPs or only tap VEMPswould have provided insufficient information about thetumor and the vestibular nerve bundle involvement Inthe third case VEMPs failed to identify the vestibularschwannoma which was clearly shown in MRI scans Inthis case our medical intuition and expertise with CPATpatients prompted us to perform MRI Due to the high cost

10 BioMed Research International

of MRI it is typically not performed at the early stages ofthe diagnostics procedure in many countries Once othertests indicate the possible presence of the CPAT an MRI isconducted

Providing AC VEMPs and tap VEMPs to the availabletest battery in the assessment of CPAT is likely to improvethe diagnostic process by providing more information onthe involved vestibular nerve bundles In addition thisinformation might be used later during the surgery In manycases theMRI is not performed very short before the surgeryUsually it is performed earlier during the diagnostic processThe surgery takes place sometime after Asmentioned beforethe MRI is quite costly and usually is not performed againif not much time passed However the ABR AC VEMPsand tap VEMP once performed in diagnostic proceedingmight be repeated short before the surgery to clarify thepresence along with possible compression characteristics ofthe tumor on the vestibular andor auditory nerves Thiscombined information from earlier MRI scans and latestelectrophysiological tests serves the surgeons as a guidelinein their surgical approach and during tumor removal Itprovides very useful information for the surgeon in makinga decision about additional intraoperative monitoring ofhearing In our department intraoperative monitoring isroutinely used in every CPAT surgery and many otherear surgeries but intraoperative hearing monitoring is notroutinely performed in most of the other clinics In additionthe details from electrophysiological tests about the involvednerve bundles are useful in patients counseling and informingthem on more realistic possible outcomes of the surgery likehearing preservations possibilities and a risk of hearing lossduring the surgery a risk of facial nerve paresis and vertigosymptoms after the surgery

Abbreviations

ABR Auditory brainstem responseAS Asymmetry ratioCPAT Cerebellopontine angle tumorECochG ElectrocochleographyEEG ElectroencephalographyEMG ElectromiographyMRI Magnetic resonance imagingPTA Pure tone averageRMS Root means squaredSCM SternocleidomastoidVEMP Vestibular Evoked Myogenic PotentialAC VEMP Auditory Vestibular Evoked Myogenic

Potentialtap VEMP Skull tapping induced Vestibular

Evoked Myogenic Potential

AC VEMPsThree Types of Recordings

AHLL Head lift stimulus delivered to the left earAHLR Head lift stimulus delivered to the right earAHLB Head lift stimulus delivered to both ears

tap VEMPs Three Types of Recordings with Skull Tapper

FHLB Forehead head lift both sides recordedMHLL Mastoid head lift skull tapper located at leftMHLR Mastoid head lift skull tapper located at right

Conflict of Interests

The authors declare the following Dr Erdem Yavuz is aResearch Scientist at Research and Development IntelligentHearing Systems Inc andDr Rafael Delgado is the ExecutiveVice President and Director of Research and DevelopmentIntelligent Hearing Systems IncThe authors declare no otherconflict of interests related to this paper

References

[1] G von Bekesy ldquoUber akustische reizung des vestibularappa-ratesrdquo Pflugerrsquos Archiv fur die Gesamte Physiologie des Menschenund der Tiere vol 236 no 1 pp 59ndash76 1935

[2] J G Colebatch and G M Halmagyi ldquoVestibular evokedpotentials in human neck muscles before and after unilateralvestibular deafferentationrdquo Neurology vol 42 no 8 pp 1635ndash1636 1992

[3] J G Colebatch G M Halmagyi and N F Skuse ldquoMyogenicpotentials generated by a click-evoked vestibulocollic reflexrdquoJournal of Neurology Neurosurgery and Psychiatry vol 57 no2 pp 190ndash197 1994

[4] G M Halmagyi R A Yavor and J G Colebatch ldquoTapping thehead activates the vestibular system a new use for the clinicalreflex hammerrdquo Neurology vol 45 no 10 pp 1927ndash1929 1995

[5] K Sheykholeslami T Murofushi M H Kermany and KKaga ldquoBone-conducted evoked myogenic potentials from thesternocleidomastoid musclerdquo Acta Oto-Laryngologica vol 120no 6 pp 731ndash734 2000

[6] K Sheykholeslami M H Kermany and K Kaga ldquoFrequencysensitivity range of the saccule to bone-conducted stimulimeasured by vestibular evoked myogenic potentialsrdquo HearingResearch vol 160 no 1-2 pp 58ndash62 2001

[7] S R D Watson P Fagan and J G Colebatch ldquoGalvanicstimulation evokes short-latency EMG responses in sternoclei-domastoidwhich are abolished by selective vestibular nerve sec-tionrdquo Electroencephalography and Clinical NeurophysiologymdashElectromyography and Motor Control vol 109 no 6 pp 471ndash474 1998

[8] S R D Watson and J G Colebatch ldquoVestibular-evoked elec-tromyographic responses in soleus a comparison between clickand galvanic stimulationrdquo Experimental Brain Research vol 119no 4 pp 504ndash510 1998

[9] F Deriu E Tolu and J C Rothwell ldquoA sound-evoked vestibu-lomasseteric reflex in healthy humansrdquo Journal of Neurophysiol-ogy vol 93 no 5 pp 2739ndash2751 2005

[10] K Botzel P Feise O I Kolev S Krafczyk and T BrandtldquoErratum postural reflexes evoked by tapping forehead andchestrdquo Experimental Brain Research vol 140 no 2 p 251 2001

[11] S M Rosengren N P M Todd and J G ColebatchldquoVestibular-evoked extraocular potentials produced by stimula-tionwith bone-conducted soundrdquoClinical Neurophysiology vol116 no 8 pp 1938ndash1948 2005

[12] N P M Todd S M Rosengren S T Aw and J G ColebatchldquoOcular vestibular evoked myogenic potentials (OVEMPs)

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 10: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

10 BioMed Research International

of MRI it is typically not performed at the early stages ofthe diagnostics procedure in many countries Once othertests indicate the possible presence of the CPAT an MRI isconducted

Providing AC VEMPs and tap VEMPs to the availabletest battery in the assessment of CPAT is likely to improvethe diagnostic process by providing more information onthe involved vestibular nerve bundles In addition thisinformation might be used later during the surgery In manycases theMRI is not performed very short before the surgeryUsually it is performed earlier during the diagnostic processThe surgery takes place sometime after Asmentioned beforethe MRI is quite costly and usually is not performed againif not much time passed However the ABR AC VEMPsand tap VEMP once performed in diagnostic proceedingmight be repeated short before the surgery to clarify thepresence along with possible compression characteristics ofthe tumor on the vestibular andor auditory nerves Thiscombined information from earlier MRI scans and latestelectrophysiological tests serves the surgeons as a guidelinein their surgical approach and during tumor removal Itprovides very useful information for the surgeon in makinga decision about additional intraoperative monitoring ofhearing In our department intraoperative monitoring isroutinely used in every CPAT surgery and many otherear surgeries but intraoperative hearing monitoring is notroutinely performed in most of the other clinics In additionthe details from electrophysiological tests about the involvednerve bundles are useful in patients counseling and informingthem on more realistic possible outcomes of the surgery likehearing preservations possibilities and a risk of hearing lossduring the surgery a risk of facial nerve paresis and vertigosymptoms after the surgery

Abbreviations

ABR Auditory brainstem responseAS Asymmetry ratioCPAT Cerebellopontine angle tumorECochG ElectrocochleographyEEG ElectroencephalographyEMG ElectromiographyMRI Magnetic resonance imagingPTA Pure tone averageRMS Root means squaredSCM SternocleidomastoidVEMP Vestibular Evoked Myogenic PotentialAC VEMP Auditory Vestibular Evoked Myogenic

Potentialtap VEMP Skull tapping induced Vestibular

Evoked Myogenic Potential

AC VEMPsThree Types of Recordings

AHLL Head lift stimulus delivered to the left earAHLR Head lift stimulus delivered to the right earAHLB Head lift stimulus delivered to both ears

tap VEMPs Three Types of Recordings with Skull Tapper

FHLB Forehead head lift both sides recordedMHLL Mastoid head lift skull tapper located at leftMHLR Mastoid head lift skull tapper located at right

Conflict of Interests

The authors declare the following Dr Erdem Yavuz is aResearch Scientist at Research and Development IntelligentHearing Systems Inc andDr Rafael Delgado is the ExecutiveVice President and Director of Research and DevelopmentIntelligent Hearing Systems IncThe authors declare no otherconflict of interests related to this paper

References

[1] G von Bekesy ldquoUber akustische reizung des vestibularappa-ratesrdquo Pflugerrsquos Archiv fur die Gesamte Physiologie des Menschenund der Tiere vol 236 no 1 pp 59ndash76 1935

[2] J G Colebatch and G M Halmagyi ldquoVestibular evokedpotentials in human neck muscles before and after unilateralvestibular deafferentationrdquo Neurology vol 42 no 8 pp 1635ndash1636 1992

[3] J G Colebatch G M Halmagyi and N F Skuse ldquoMyogenicpotentials generated by a click-evoked vestibulocollic reflexrdquoJournal of Neurology Neurosurgery and Psychiatry vol 57 no2 pp 190ndash197 1994

[4] G M Halmagyi R A Yavor and J G Colebatch ldquoTapping thehead activates the vestibular system a new use for the clinicalreflex hammerrdquo Neurology vol 45 no 10 pp 1927ndash1929 1995

[5] K Sheykholeslami T Murofushi M H Kermany and KKaga ldquoBone-conducted evoked myogenic potentials from thesternocleidomastoid musclerdquo Acta Oto-Laryngologica vol 120no 6 pp 731ndash734 2000

[6] K Sheykholeslami M H Kermany and K Kaga ldquoFrequencysensitivity range of the saccule to bone-conducted stimulimeasured by vestibular evoked myogenic potentialsrdquo HearingResearch vol 160 no 1-2 pp 58ndash62 2001

[7] S R D Watson P Fagan and J G Colebatch ldquoGalvanicstimulation evokes short-latency EMG responses in sternoclei-domastoidwhich are abolished by selective vestibular nerve sec-tionrdquo Electroencephalography and Clinical NeurophysiologymdashElectromyography and Motor Control vol 109 no 6 pp 471ndash474 1998

[8] S R D Watson and J G Colebatch ldquoVestibular-evoked elec-tromyographic responses in soleus a comparison between clickand galvanic stimulationrdquo Experimental Brain Research vol 119no 4 pp 504ndash510 1998

[9] F Deriu E Tolu and J C Rothwell ldquoA sound-evoked vestibu-lomasseteric reflex in healthy humansrdquo Journal of Neurophysiol-ogy vol 93 no 5 pp 2739ndash2751 2005

[10] K Botzel P Feise O I Kolev S Krafczyk and T BrandtldquoErratum postural reflexes evoked by tapping forehead andchestrdquo Experimental Brain Research vol 140 no 2 p 251 2001

[11] S M Rosengren N P M Todd and J G ColebatchldquoVestibular-evoked extraocular potentials produced by stimula-tionwith bone-conducted soundrdquoClinical Neurophysiology vol116 no 8 pp 1938ndash1948 2005

[12] N P M Todd S M Rosengren S T Aw and J G ColebatchldquoOcular vestibular evoked myogenic potentials (OVEMPs)

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 11: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

BioMed Research International 11

produced by air- and bone-conducted soundrdquo Clinical Neuro-physiology vol 118 no 2 pp 381ndash390 2007

[13] E D Young C Fernandez and J M Goldberg ldquoResponses ofsquirrel monkey vestibular neurons to audio-frequency soundand head vibrationrdquo Acta Oto-Laryngologica vol 84 no 5-6pp 352ndash360 1977

[14] T Murofushi and I S Curthoys ldquoPhysiological and anatomicalstudy of click-sensitive primary vestibular afferents in theguinea pigrdquo Acta Oto-Laryngologica vol 117 no 1 pp 66ndash721997

[15] G L Townsend and D T Cody ldquoThe averaged inion responseevoked by acoustic stimulation its relation to the sacculerdquoAnnals of Otology Rhinology and Laryngology vol 80 no 1 pp121ndash131 1971

[16] T Murofushi G M Halmagyi R A Yavor and J G ColebatchldquoAbsent vestibular evoked myogenic potentials in vestibularneurolabyrinthitis an indicator of inferior vestibular nerveinvolvementrdquo Archives of OtolaryngologymdashHead and NeckSurgery vol 122 no 8 pp 845ndash848 1996

[17] T Murofushi M Matsuzaki and M Mizuno ldquoVestibularevoked myogenic potentials in patients with acoustic neuro-masrdquo Archives of OtolaryngologymdashHead and Neck Surgery vol124 no 5 pp 509ndash512 1998

[18] T Tsutsumi A Tsunoda Y Noguchi and A KomatsuzakildquoPrediction of the nerves of origin of vestibular schwannomaswith vestibular evoked myogenic potentialsrdquo American Journalof Otology vol 21 no 5 pp 712ndash715 2000

[19] K Brantberg M Westin L Lofqvist L Verrecchia and ATribukait ldquoVestibular evoked myogenic potentials in responseto lateral skull taps are dependent on two different mecha-nismsrdquo Clinical Neurophysiology vol 120 no 5 pp 974ndash9792009

[20] K Kushiro M Zakir Y Ogawa H Sato and Y Uchino ldquoSac-cular and utricular inputs to sternocleidomastoid motoneuronsof decerebrate catsrdquo Experimental Brain Research vol 126 no3 pp 410ndash416 1999

[21] K Brantberg and A Tribukait ldquoVestibular evoked myogenicpotentials in response to laterally directed skull tapsrdquo Journalof Vestibular Research Equilibrium and Orientation vol 12 no1 pp 35ndash45 2002

[22] N P M Todd S M Rosengren and J G Colebatch ldquoA sourceanalysis of short-latency vestibular evoked potentials producedby air- and bone-conducted soundrdquo Clinical Neurophysiologyvol 119 no 8 pp 1881ndash1894 2008

[23] K Brantberg L LofqvistMWestin andATribukait ldquoSkull tapinduced vestibular evoked myogenic potentials an ipsilateralvibration response and a bilateral head acceleration responserdquoClinical Neurophysiology vol 119 no 10 pp 2363ndash2369 2008

[24] S M Rosengren M S Welgampola and J G ColebatchldquoVestibular evoked myogenic potentials past present andfuturerdquo Clinical Neurophysiology vol 121 no 5 pp 636ndash6512010

[25] K Brantberg A Tribukait and P-A Fransson ldquoVestibularevoked myogenic potentials in response to skull taps forpatients with vestibular neuritisrdquo Journal of Vestibular ResearchEquilibrium and Orientation vol 13 no 2-3 pp 121ndash130 2003

[26] K Brantberg and T Mathiesen ldquoPreservation of tap vestibularevoked myogenic potentials despite resection of the inferiorvestibular nerverdquo Journal of Vestibular Research Equilibriumand Orientation vol 14 no 4 pp 347ndash351 2004

[27] S Iwasaki L A McGarvie G M Halmagyi et al ldquoHead tapsevoke a crossed vestibulo-ocular reflexrdquo Neurology vol 68 no15 pp 1227ndash1229 2007

[28] Y Chihara S Iwasaki M Ushio et al ldquoOcular vestibular-evoked myogenic potentials (oVEMPs) require extraocularmuscles but not facial or cochlear nerve activityrdquo ClinicalNeurophysiology vol 120 no 3 pp 581ndash587 2009

[29] A P Bath N Harris and M P Yardley ldquoThe vestibulo-collicreflexrdquo Clinical Otolaryngology and Allied Sciences vol 23 no5 pp 462ndash466 1998

[30] F W Akin O D Murnane P C Panus S K Caruthers AE Wilkinson and T M Proffitt ldquoThe influence of voluntarytonic EMG level on the vestibular-evoked myogenic potentialrdquoJournal of Rehabilitation Research and Development vol 41 no3 pp 473ndash480 2004

[31] J S Sandhu and S L Bell ldquoEffects of eye position on thevestibular evokedmyogenic potentialrdquo Acta Oto-Laryngologicavol 129 no 2 pp 175ndash178 2009

[32] K Brantberg and P-A Fransson ldquoSymmetry measures ofvestibular evokedmyogenic potentials using objective detectioncriteriardquo Scandinavian Audiology vol 30 no 3 pp 189ndash1962001

[33] O Sterkers C Martin and W Arnold ldquoVestibularschwannomardquo in Otorhinolaryngology Head and NeckSurgerymdashEuropean Manual of Medicine M Anniko MBernal-Sprekelsen V Bonkowsky P Bradley and S IuratoEds pp 92ndash97 Springer Berlin Germany 2010

[34] H Silverstein ldquoCochlear and vestibular gross andhistologic anatomy (as seen from postauricular approach)rdquoOtolaryngologymdashHead and Neck Surgery vol 92 no 2 pp207ndash211 1984

[35] R P Schefter and S G Harner ldquoHistologic study of thevestibulocochlear nerverdquo Annals of Otology Rhinology andLaryngology vol 95 no 2 part 1 pp 146ndash150 1986

[36] D Rubinstein E J Sandberg and A G Cajade-Law ldquoAnatomyof the facial and vestibulocochlear nerves in the internalauditory canalrdquo American Journal of Neuroradiology vol 17 no6 pp 1099ndash1105 1996

[37] J M Bogle D A Zapala R Criter and R Burkard ldquoTheeffect of muscle contraction level on the cervical vestibularevoked myogenic potential (cVEMP) usefulness of amplitudenormalizationrdquo Journal of the American Academy of Audiologyvol 24 no 2 pp 77ndash88 2013

[38] M SWelgampola and J G Colebatch ldquoVestibulocollic reflexesnormal values and the effect of agerdquo Clinical Neurophysiologyvol 112 no 11 pp 1971ndash1979 2001

[39] M S Welgampola and J G Colebatch ldquoCharacteristics andclinical applications of vestibular-evoked myogenic potentialsrdquoNeurology vol 64 no 10 pp 1682ndash1688 2005

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 12: Research Article Clinical Use of Skull Tap Vestibular …downloads.hindawi.com/journals/bmri/2014/135457.pdfResearch Article Clinical Use of Skull Tap Vestibular Evoked Myogenic Potentials

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom