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470 Jae-Seung Baek, et al. Usefulness of the Facial Motor Evoked Potential during Cerebello-pontine Angle Tumor Surgery ORIGINAL ARTICLE Korean J Clin Lab Sci. 2018;50(4):470-476 https://doi.org/10.15324/kjcls.2018.50.4.470 pissn 1738-3544 eissn 2288-1662 Facial Motor Evoked Potential Techniques and Functional Prediction during Cerebello-pontine Angle Surgery Jae-Seung Baek 1, Sang-Ku Park 1, Dong-Jun Kim 1, Chan-Woo Park 1, Sung-Hyuk Lim 1, Jang Ho Lee 2, Young-Kuk Cho 3 1 Department of Neurology, Samsung Medical Center, Seoul, Korea 2 Department of Clinical Laboratory Science, Semyung University, Jecheon, Korea 3 Department of Medical Laboratory Science, Seoyeong University, Gwangju, Korea 소뇌교각수술중에안면운동유발전위의검사방법과기능적예측인자 백재승 1, 박상구 1, 김동준 1, 박찬우 1, 임성혁 1, 이장호 2, 조영국 3 1 삼성서울병원신경과, 2 세명대학교임상병리학과, 3 서영대학교임상병리과 Facial motor evoked potential (FMEP) by multi-pulse transcranial electrical stimulation (mptes) can complement free-running electromyography (EMG) and direct facial nerve stimulation to predict the functional integrity of the facial nerve during cerebello-pontine angle (CPA) tumor surgery. The purpose of this paper is to examine the standardized test methods and the usefulness of FMEP as a predictor of facial nerve function and to minimize the incidence of facial paralysis as an aftereffect of surgery. TES was delivered through electrode Mz (cathode) - M3/M4 (anode), and extracranially direct distal facial muscle excitation was excluded by the absence of single pulse response (SPR) and by longer onset latency (more than 10 ms). FMEP from the orbicularis oris (o.oris) and the mentalis muscle simultaneously can improve the accuracy and success rate compared with FMEP from the o.oris alone. Using the methods described, we can effectively predict facial nerve outcomes immediately after surgery with a reduction of more than 50% of FMEP amplitude as a warning criterion. In conclusion, along with free-running EMG and direct facial nerve stimulation, FMEP is a useful method to reduce the incidence of facial paralysis as a sequela during CPA tumor surgery. Key words: Cerebellopontine angle, Facial nerve, Intraoperative monitoring, Motor evoked potential, Transcranial electrical stimulation Corresponding author: Jae-Seung Baek Department of Neurology, Samsung Medical Center, 81 Irwon-ro, Gangnam-gu, Seoul 06351, Korea Tel: 82-2-3410-2737 Fax: 82-2-3410-2759 E-mail: jslove.back@samsung.com This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Copyright 2018 The Korean Society for Clinical Laboratory Science. All rights reserved. Received: September 13, 2018 Revised 1 st : October 12, 2018 Revised 2 nd : October 22, 2018 Accepted: October 22, 2018 서론수술중신경감시는현대신경외과수술에서사망률은줄이고운동신경과감각신경그리고뇌신경기능보존등의수술결과를향상시킬수있는방법중하나이다 [1]. 그중자유진행근전도 (free-running EMG) 와직접적인안면신경전기자극법 (direct facial nerve electrical stimulation) 의도입은소뇌교각종양수술중에안면신경손상으로발생하는후유증인안면마비발생률을감소시켰다 [2-5]. 첫번째검사인자유진행근전도는안면근육에기록전극을부착하고실시간으로안면신경이자극될때발생하는신경긴장성의발산 (neurotonic discharge) 즉, 근전도반응을보는것

Korean J Clin Lab Sci. Vol. 50, No. 4, December 2018 471 이다. 이런반응은리트랙터 (retractor) 로인한신경당김, 종양절제중에근접한신경손상과같은의도하지않은손상성안면신경이자극될때발생하고이때집도의에게알린다. 그러나, 수술중식염수세척, 지혈솜압박등의안면신경에손상을가하지는않지만간접적인자극도생기기때문에근전도반응이많이있었다고해서꼭안면신경의손상을나타내지는않는다 [6]. 게다가수술초기큰종양으로인해안면신경이식별되기도전에수술가위, 메스, 바이폴라포셉등의날카로운도구에 0.7 mm 이하의작은안면신경이집도의도모르게순식간에절단되면근전도반응은유발되지않을수있기때문에그들의부재가안면신경의기능적인완전성 (integrity) 을보장하지못한다 [3, 7]. 즉, 근전도반응은신경손상정도의정확한기능평가는할수없는단점이있다. 하지만이러한단점에도불구하고수술중집도의에게실시간으로안면신경의자극여부을제공하는목적만으로근전도반응검사를시행해오고있다 [3]. 두번째검사인직접적인안면신경전기자극에반응하는안면근육에서의복합근육활동전위 (compound muscle action potentials, CMAPs) 는신경의기능평가를하는검사로서자유진행근전도를보완한다. 소뇌교각종양을기준으로안면신경의근위부인근기시부 (root exit zone) 및원위부인내이도 (internal auditory canal, IAC) 에서최대상 (supramaximal) 자극에대한안면근육의복합근육활동전위비율이 30% 이상일때와, 근기시부자극임계치 (threshold) 가 0.3 ma보다같거나작을때가만족스러운수술후안면기능을예측한다 [2, 8, 9]. 그러나이검사는근기시부안면신경이식별된후에집도의가수술을잠시멈추고단극성신경자극기 (monopolar nerve stimulator) (Figure 1) 로직접자극을해야하기때문에간헐적으로진행이되고수술절차를지연시킬수있다. 이러한이유로인하여집도의들이자주시행하지않는다 [10]. 그리고수술중에안면신경식별이매우어려운큰종양의경우는뇌간의해부학적변형과대부분의수술중에종양에안면신경이가려져있 어직접적인안면신경전기자극시행가능성여부가집도의의안면신경근기시부위치를정확하게알아내는능력에높게의존한다 [5, 11, 12]. 앞에서언급한자유진행근전도의부정확한안면신경의기능예측과직접적인안면신경전기자극의간헐적이고큰종양수술일경우에는시행조차못할수있는단점들때문에여전히안면마비는환자가소뇌교각종양수술을받을때주로걱정되는후유증이다 [11, 13]. 그래서이런단점들을보완한근기시부안면신경을직접확인할필요없고직접적인안면신경전기자극을위해수술을중간에중단하지않아도되고안면신경을집도의가원할때마다검사할수있는다중펄스경두개전기자극 (multi-pulse transcranial electrical stimulation, mptes) 에의한안면운동유발전위 (facial motor evoked potential, FMEP) 가도입이되었다. 다중펄스경두개전기자극에의한운동유발전위는대뇌운동피질시스템의평가를위한방법이다 [14-16]. 안면신경감시를위한피질연수로 (corticobulbar tract) 로이기술을적용하면안면신경의기능을예측할수있다 [11, 18]. 그러나이검사는자극전극과측정되는안면근육이근접해있어자극이강하면피질연수로뿐만아니라두개외로전파되어직접적으로말초안면근육을자극시켜검사의정확도가떨어질수있다 [18]. 그리고자극잡파혼입도많아서안면운동유발전위결과분석이어려워국내에서는거의시행되고있지않다. 본원에서도수술중에자유진행근전도와직접적인안면신경전기자극법만으로최근까지감시를했었고수술중에안면신경손상없이끝났다고생각했지만수술직후안면마비가발생한환자들이발생하고있는실정이다. 따라서안면운동유발전위를통하여안면마비의발생률의유의미한감소효과를관찰해보고자하였다. 본논문에서는소뇌교각종양수술중에다중펄스경두개전기자극에의한안면운동유발전위의직접적인말초안면근육자극없이정확하게검사하는방법들과수술직후안면신경결과예측인자로서의유용성을알아보고수술후중대한후유증인안면마비의발생률을최소화하는것을목적으로하였다. 재료및방법 1. 검사장비 Figure 1. Monopolar stimulator. 수술장에서사용하는수술중신경계추적감시 (intraoperative neuro-monitoring, INM) 장비는 Xltek Protektor (Natus Medical Incor.) 를사용하였다. 안면운동유발전위를위한세팅은 Range ±1 10 mv, Reject Threshold ±1 10 mv,

472 Jae-Seung Baek, et al. Usefulness of the Facial Motor Evoked Potential during Cerebello-pontine Angle Tumor Surgery LFF/HFF: 100 150 Hz/3 5 KHz, Timebase 5 ms/div, Amplitude 100 V로설정하여검사를하였다. 2. 검사방법 2018년 5월부터 2018년 7월까지소뇌교각종양환자 14명을대상으로분석을하였다. 나이는평균 50 (±11.64) 세였고, 여자 9명, 남자 5명이었다. 종양의분류는전정신경초종 (vestibular schwannoma) 이 9명, 수막종 (meningioma) 이 3 명, 경정맥공신경초종 (jugular foramen schwannoma) 이 1 명, 혈관아세포종 (hemangioblastoma) 이 1명이였고종양크기는 2 4.7 cm 이였다 (Table 1). 환자들은수술전의료진에게수술동의서를작성하였으며, 수술동의서에따라수술중유발전위검사를시행하였다. 자유진행근전도와직접적인안면신경자극법을이용해서안면신경의위치를탐색하고 [20] 안면운동유발전위를이용해서경막절개전 (before dura open) 을기준파형 (baseline) 으로해서안면신경의기능적인완전성을감시하였다. 파형의진폭이 50% 이상감소되면즉시집도의에게 알리기로하였다. 수술종양제거후피부봉합때파형 (final) 을기준파형과비교한안면운동유발전위비율을측정하였다 [18]. 안정적인안면운동유발전위를위해자극법은 1 5 pulse, duration; 50 sec, interstimulus interval; 1 2 ms이고자극전극은음극 (cathode) 은 Mz (Cz전방으로 1 cm), 양극 (anode) 은수술부위가오른쪽일경우에 M3, 왼쪽일경우에 M4 (C3, C4 전방으로 1 cm) 에바늘전극으로부착했다 ( 전극배치법 : INTERNATIONAL 10 20 EEG SYSTEM) (Figure 2). 기록전극은수술동측구륜근 (orbicularis oris) 과턱근 (mentalis) 에바늘전극을 2개씩부착했다. 저체온이나저혈압등의전신적인원인, 기술적인에러, 마취심도에따른영향과안면신경의손상을구별하기위한대조군으로수술동측의단무지외전근 Table 1. Patient demographics SEX Male 5 Female 9 Median age, y 50 Range 23 64 Diagnosis Vestibular schwannoma 9 Meningioma 3 Jugular foramen schwannoma 1 Hemangioblastoma 1 Figure 2. Electrode placement. Figure 3. Single pulse response of the facial MEP recorded from the right orbicularis oris (o. oris) muscle. The facial MEP response is 160 V in amplitude, generated by transcranial electric stimulation of 3 pulses, 2 ms ISI and 300 V (A). During stimulation, the anode was at M3 the cathode was at Mz. A simultaneous APB and ADQ muscle response is also shown. Note the absence of the single pulse responses (B) and the facial MEP onset latency of 10 ms or more, which indicate a central origin.

Korean J Clin Lab Sci. Vol. 50, No. 4, December 2018 473 (abductor pollicis brevis) 혹은소지외전근 (abductor digiti quinti) 을같이기록하였고안면근육의단일펄스반응 (single pulse response, SPR) (Figure 3) 과 10 ms 보다긴잠복기을확인해서직접적인말초안면근육자극을배제하였다 [17]. 수술전과직후안면기능은 House-Brackmann grading scheme (HB grade 1 6) 을통해평가하였다 (Table 2)[19]. 3. 마취 Rocuronium bromide (0.8 1.0 mg/kg) 주입후기관내튜브삽관하고표적제어주입펌프를통해전달된프로포폴을사용하여신경마비를유지시켰다. 또한지속적으로레미펜타닐을투여하거나펜타닐을투여했다. 마취유도와삽관후에흡입제를사용하지않았다. 수술중마취수준을평가하기위해 bispectral index 방법을사용하여뇌파를모니터링하였다. 지 Table 2. Facial nerve grading system (HB grade I VI) Grade Description Characteristics I Normal Normal facial function in all areas II Mild dysfunction Gross: slight weakness noticeable on close inspection; may have very slight synkinesis At rest: normal symmetry and tone Forehead: moderate to good function/eye: complete closure with minimum effort/mouth: slight asymmetry III Moderate dysfunction Gross: obvious but not disfiguring difference between two sides; noticeable but not severe synkinesis, contracture, and/or hemifacial spasm At rest: normal symmetry and tone Forehead: slight to moderate movement/eye: complete closure with effort/mouth: slightly weak with maximum effort IV Moderately severe dysfunction Gross: obvious weakness and/or disfiguring asymmetry At rest: normal symmetry and tone Forehead: none/eye: incomplete closure/mouth: asymmetric with maximum effort V Severe dysfunction Gross: only barely perceptible motion At rest: asymmetry Forehead: none/eye: incomplete closure/mouth: slight movement VI Total paralysis No movement Abbreviation: HB, House-Brackmann. Table 3. Correlation between neurophysiological data and postoperative facial nerve outcomes No. Sex Age Diagnosis Size (cm) Stimulation Intensity Final facial MEP amplitude (%) Pre-operative HB grade Post-operative HB grade 1 F 43 LT VS 3.3 300 V 100% (100 V) 1 1 2 F 62 LT VS 3.1 220 V 300 V 120% (250 300 V) 1 2 3 F 58 LT CPA MNG 4.7 200 V 100% (220 V) 1 1 4 F 64 RT VS 3.1 500 V 100% (200 V) 1 1 5 M 39 RT VS 2 200 V 160% (50 80 V) 1 1 6 F 35 RT VS 4 250 V 100% (400 V) 1 2 7 M 47 LT VS 3.5 300 V 100% (300 V ) 1 1 8 F 58 HEMANGIO-BLASTOMA 2.6 400 V 100% (160 V) 1 1 9 F 57 RT CPA MNG 2.7 300 V 100% (150 V) 1 1 10 F 56 LT CPA MNG 3.1 400 V 630 V 50% (30 15 V) 1 3 11 M 23 LT VS(NF2) 3.6 300 V 350 V 100% (150 V) 1 2 12 F 61 LT VS 2.9 300 V 100% (200 V) 1 2 13 M 46 RT VS 3.6 300 V 100% (60 V) 1 1 14 M 59 RT JUGULAR FORAMEN SCHWANNOMA 3.9 300 V 160% (50 80 V) 1 1 Abbreviations: FMEP, facial motor evoked potential; HB, House-Brackmann; VS, vestibular schwannoma; NF2, neurofibromatosis type 2; CPA, cerebellopontine angle; MNG, meningioma.

474 Jae-Seung Baek, et al. Usefulness of the Facial Motor Evoked Potential during Cerebello-pontine Angle Tumor Surgery 수는 40 60 의범위로유지하였다. 정중신경을 4번연속적으로자극한후엄지손가락의움직임을관찰하는사연속자극 (train of four, TOF) 검사가적어도 2번이상되도록근이완제 (neuromuscular blocking agent) 의양을적절하게유지했다. 4. 통계학적분석 SPSS version 1.0.0 (SPSS Inc., Chicago, IL, USA) 을이용하여수행되었다. BASELINE TO FINAL 안면운동유발전위진폭비의 50% 이상감소여부와수술직후안면신경 HB grade 간의유의성을카이제곱검정 (chi-squared test) 을통해분석하였다. 수술직후 HB grade 1 2 을만족스러운결과, HB grade 3 6을불만족스러운결과로평가하였다 [18]. P< 0.05 일경우통계학적으로유의하다고하였다. 결과다중펄스경두개전기자극을이용한안면운동유발전위를실행한모든환자 (14/14) 에게서수술중에안면신경의기능적인완전성을감시했다 (Table 3). 안면근육에서단일펄스반응의 부재와 10ms 이상의잠복기를확인해서직접적인말초안면근육의자극을방지하였다 (Figure 3). 평균자극세기는 330.71 (±114.58) V이고, 환자의안면운동유발전위의평균잠복기는 13.5 (±1.5) ms이고, 평균진폭은 166.42 (±98.24) V이였다. 수술중 1명의환자에서안면운동유발전위진폭비가 50% 이상감소되었고수술후환자에게불만족스러운안면신경 HB grade 3가되었다. 13명의환자에서는잠복기와진폭의유의한변화없이종료되었고수술후만족스러운안면신경 HB grade 1 2 이였다. 진폭비의 50% 감소여부와안면신경 HB grade을교차분석하여 =14.000, P< 0.001 으로유의성을확인하였다 (Table 4). 이중에서수술종료전진폭이 120% 증가되었고 HB grade 2인환자 1명, 100% 유지되었고 HB grade 2인환자 3명이였다. 즉, 안면운동유발전위는호전되거나유지되었지만 HB grade는가벼운악화를나타낸것이다. 미세한진폭의증가는수술종료전환자를깨우기위해마취의심도가낮아져서마취가깊었던기준파형때보다진폭이커질수있다. 진폭의변화는없었지만 HB grade의가벼운악화는두개외전기자극의전파를방지하기위해최대상자극을줄수없고비교적약한자극을주기때문에전체가아닌부분적인안면신경의흥분을나타 Table 4. Correlation between a reduction in amplitude of more than 50% of FMEP and postoperative facial nerve outcomes Postoperative facial nerve HB GRAGE HB grage 2 HB grade 2< Baseline to final Amplitude 50%< 13 (100.0) 0 (0.0) 14.00*** 50% 0 (0.0) 1 (100.0) Total 13 (92.9) 1 (7.1) P=0.000 Chi-squared test, *P<0.05; **P<0.01; ***P<0.001. Figure 4. An example of facial MEP recorded from the left orbicularis oris (o. oris) and mentalis. In the left picture (A), The facial MEP response is 300 V in amplitude, generated by transcranial electric stimulation of 5 pulses, 2 ms ISI and 300 V (A). During stimulation, the anode was at M4 and the cathode was at Mz. On the mentalis rather than orbicularis oris, a smaller stimulus artifact and a larger CMAP occurs (A). Whereas in the right picture (B), a smaller artifact and a larger CMAP occurs on the orbicularis oris rather than mentalis. FMEP Recorded the o.oris and mentalis together can improve the accuracy and success rate rather than FMEP recorded from only the o.oris.

Korean J Clin Lab Sci. Vol. 50, No. 4, December 2018 475 낼수있기에미세한안면신경의손상은안면운동유발전위진폭의변화가없을수도있기때문이다 [18]. 그래서진폭의변화가없으면상관없으나감소되거나소실되면직접적인안면신경전기자극법을이용해서안면신경의추가적인기능확인이필요하다. 고찰다중펄스경두개전기자극을이용한안면운동유발전위는자유진행근전도와직접적인안면신경자극법의한계점을보완해서소뇌교각종양수술에서수술진행에방해없이실시간으로수술초기피부절개부터수술끝피부봉합완료시까지안면신경의기능적완전성을감시할수있다. 그러나자극의과도한전파로인해피질연수로뿐만아니라두개외로직접적인말초안면근육자극이생겨서안면신경에손상이생겨도안면운동유발전위는변화가없어위음성이될수있다. 그래서안면근육의단일펄스반응의부재와 10 ms 이상의잠복기를확인하여자극세기를조절하고말초안면근육이직접적으로흥분되는것을방지하였다. 또한 low frequency filter 를 100 150 HZ 까지조절해서자극잡파를최소화시켜자극파형과안면근육반응이혼합되지않도록하였다. M3-M4 자극법보다 Mz-M3/M4 자극법은자극으로인한환자의움직임도거의없고검사의정확도도좋아진다 [20]. 본연구에서는구륜근과턱근를동시에감시해서구륜근만을검사할때보다검사정확도와성공률을높였다 (Figure 4). Baseline to final 안면운동유발전위진폭비가 50% 이상감소될때를경고기준으로하여수술직후안면신경의 HB grade 가만족스러운 grade 1 2 와불만족스러운 grade 3 6 에서유의하였다. 그래서집도의는소뇌교각종양수술중에안면운동유발전위를통해안면신경의기능적인완전성을예측하는데도움이될수있다. 결론적으로, 소뇌교각종양수술중에자유진행근전도와직접적인안면신경자극법을이용해서안면신경의위치를파악하고안면운동유발전위로기능적인완전성을확인하면서종양절제를해서중대한후유증인안면마비발생률를최소화할수있다. 요약다중펄스경두개전기자극 (mptes) 을이용한안면운동유발전위 (FMEP) 는자유진행근전도와직접적인안면신경자극법 의한계점을보완하고소뇌교각종양수술중에안면신경의기능적인완전성을예측할수있다. 본논문의목적은이검사의표준화된검사방법과안면신경의기능예측인자로서의유용성을알아보고수술후중대한후유증인안면마비발생률을최소화하는것이다. Mz ( 음극 )-M3, M4 ( 양극 ) 전극으로경두개전기자극을주고안면운동유발전위의단일펄스반응 (SPR) 의부재와 10 ms이상의잠복기를확인해서직접적인두개외말초안면근육자극을배제하고구륜근 (orbicularis oris) 과턱근 (mentalis) 에서동시에측정하면구륜근에서만측정했을때보다안면운동유발전위의정확도와성공률을높일수있다. 본논문에서는안면운동유발전위의 50% 진폭감소를경고기준으로해서수술직후안면신경의결과를효과적으로예측할수있었다. 결론적으로, 소뇌교각종양수술중에 FMEP는자유진행근전도와직접적인안면신경자극법과더불어서수술후중대한후유증인안면마비발생률을최소화할수있는유용한검사방법이다. Acknowledgements: None Conflict of interest: None Author s information (Position): Baek JS 1, M.T.; Park SK 1, M.T.: Kim DJ 1, M.T.; Park CW 1, M.T.; Lim SH 1, M.T.; Lee JH 2, Professor; Cho YK 3, Professor. REFERENCES 1. Sala F, Manganotti P, Tramontano V, Bricolo A, Gerosa M. Monitoring of motor pathways during brain stem surgery: what we have achieved and what we still miss? Neurophysiol Clin. 2007;37:399-406. 2. Goldbrunner RH, Schlake HP, Milewski C, Tonn JC, Helms J, Roosen K. Quantitative parameters of intraoperative electromyography predict facial nerve outcomes for vestibular schwannoma surgery. Neurosurgery. 2000;46:1140-1146. 3. Harper CM, Daube JR. Facial nerve electromyography and other cranial nerve monitoring. J Clin Neurophysiol. 1998;15: 206-216. 4. Moller AR, Jannetta PJ. Preservation of facial function during removal of acoustic neuromas: use of monopolar constant-voltage stimulation and EMG. J Neurosurg. 1984;61: 757-760. 5. Romstock J, Strauss C, Fahlbusch R. Continuous electromyography monitoring of motor cranial nerves during cerebellopontine angle surgery. J Neurosurg. 2000;93:586-593. 6. Hone SW, Commins DJ, Rames P, Chen JM, Rowed D, McLean A, et al. Prognostic factors in intraoperative facial nerve monitoring for acoustic neuroma. J Otolaryngol. 1997; 26:374-378. 7. Nakao Y, Piccirillo E, Falcioni M, Taibah A, Kobayashi T, Sanna M. Electromyographic evaluation of facial nerve damage in acoustic neuroma surgery. Otol Neurotol. 2001;22:554-557.

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