Neurosurg Rev (2014) 37:669–676 DOI 10.1007/s10143-014-0561-7
ORIGINAL ARTICLE
Intraoperative continuous monitoring of facial motor evoked potentials in acoustic neuroma surgery Hiroshi Tokimura & Sei Sugata & Hitoshi Yamahata & Shunji Yunoue & Ryosuke Hanaya & Kazunori Arita
Received: 9 June 2013 / Revised: 23 March 2014 / Accepted: 18 May 2014 / Published online: 13 July 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract The preservation of facial nerve function is one of the primary objectives in acoustic neuroma surgery. We detail our method of continuous intraoperative facial motor evoked potential (MEP) monitoring and present criteria for the preservation of facial nerve function to avoid postoperative facial nerve palsy. Our study population was comprised of 15 patients who did not (group 1), and 20 who did (group 2) undergo facial MEP monitoring during surgery to remove acoustic neuromas. In group 2, we continuously stimulated the facial motor cortex at 5- or 10-s intervals throughout surgery. Electromyograms (EMGs) were recorded from the contralateral orbicularis oculi- and orbicularis oris muscles. Optimal anode and cathode placement was at the facial motor cortex and the vertex, respectively. Postoperative facial palsy occurred in 8 of the 15 group 1 patients; in 2 it improved to grade II at 6 months after the operation. Of the 20 group 2 patients, 7 suffered postoperative facial palsy. At 6 months after the operation, their facial nerve function was normal. At the end of the operation, the ratio of the amplitude of the supramaximal EMG to the amplitude at the dural opening was 39.6 % in patients with- and 94.3 % in patients without transient postoperative facial palsy. Continuous facial MEP monitoring not only alerts to surgical invasion of the facial nerves but also helps to predict postoperative facial nerve function. To preserve a minimum amplitude ratio of 50 %, even transient postoperative facial palsy must be avoided. MEP monitoring is an additional useful modality for facial nerve monitoring during acoustic neuroma surgery.
Keywords Intraoperative monitoring . Facial nerve . Motor evoked potential . Acoustic neuroma
Introduction Observation of the A-train on free-run electromyograms (EMG) and continuous facial nerve monitoring upon stimulation at the root exit zone of the facial nerve are among the techniques accepted for the preservation of facial nerve function in patients undergoing the removal of acoustic neuromas [1, 2, 4, 12, 17]. Intraoperative monitoring of facial motor evoked potentials (MEP), introduced to evaluate facial nerve function [2, 4, 8, 10], cannot be used for continuous intraoperative monitoring because of body movement artifacts. Conventional MEP monitoring at neurological surgeries may require the placement of electrodes on the scalp to deliver highintensity electrical stimulation to not only the targeted—but also to systemic muscles. Operative manipulations must be stopped during recording of the MEP [9, 13, 15, 16]. In this study, we first attempted to identify the optimal conditions for continuous MEP monitoring of facial nerve function. Based on our findings, we then applied facial MEP monitoring throughout acoustic neuroma surgery in efforts to preserve postoperative facial nerve function. To our knowledge, this is the first report of the successful monitoring of continuous facial MEP during acoustic neuroma surgery.
Patients and methods H. Tokimura (*) : S. Sugata : H. Yamahata : S. Yunoue : R. Hanaya : K. Arita Department of Neurosurgery, Graduate School of Medical and Dental Sciences, University of Kagoshima, 8-35-1 Sakuragaoka, Kagoshima City 890-8544, Japan e-mail: [email protected]
Our study population consisted of 35 consecutive patients with acoustic neuroma treated by one neurosurgeon (H.T.) between June 2009 and January 2013. In all operated patients, we monitored facial nerve function with occasional electrical stimulation of the facial nerve. Intraoperative facial MEP
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monitoring was not used in 15 patients (group 1) and was used in 20 (group 2). In three patients, we investigated the optimal placement of electrodes affixed to the scalp and the stimulus intensity appropriate for the continuous intraoperative recording of facial MEP without eliciting body movement. Then, we recorded the facial MEP continuously from opening of the dura to the end of the tumor removal procedure. We analyzed the supramaximal amplitude of the facial MEP at the start and conclusion of the operation. Acoustic tumors were classified by the grading system of Koos et al. [7]. It classifies the tumors as grades I– IV where grade I=small intracanalicular tumor, II=small tumor with protrusion into the cerebellopontine angle, III=tumor occupying the cerebellopontine cistern with no brainstem displacement, and IV=large tumor with brainstem- and cranial nerve displacement. The size of the tumor was determined with image analysis software (Image-J, version 1.46; National Institutes of Health, Bethesda, MD) based on its maximal diameter and the area involved by the tumor on gadoliniumenhanced axial magnetic resonance images (MRI). The extirpation rate was calculated by the ratio of the postoperative tumor-free area to the area involved by the tumor. Facial nerve function was classified by the House and Brackmann grading system [5] where I=normal function, II–V reflect slight-, moderate-, moderately severe-, and severe dysfunction, respectively, and VI=total paralysis. Facial nerve function was evaluated at discharge from the hospital and 6 months after the operation.
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through two corkscrew electrodes (KS211-024, Unique Medical Co. Ltd., Tokyo, Japan) affixed to the scalp; the cathode was at Cz and the anode was above the facial motor cortex. The KS211-024 stimulator was interfaced with an electrophysiological recording system (MEE-1232, Nihon Kohden Corp.) so that a triggered EMG response was elicited by each stimulus. EMG activity evoked by transcranial electrical stimulation was recorded with subdermal needle electrodes (Medtronic Xomed, Inc., Jacksonville, FL, USA) placed in the orbicularis oculi muscle at the lateral angle of the ipsilateral eye and in the orbicularis oris muscle at the ipsilateral angle of the mouth. Recording and filtering parameters were 5–1,500 Hz. The amplifier gain was initially set at 200 μV/ division and adjusted based on the size of the EMG responses. After opening the dura, we obtained the baseline facial MEP. The facial MEP amplitude was maintained at above the threshold evoked with a stimulus approximately 50 V stronger than the threshold stimulus intensity. The stimulus intensity was adjusted to avoid body movements. The facial MEP was recorded at 5- or 10-s intervals starting at the dural opening and ending at the conclusion of tumor removal. When deterioration of the facial MEP was detected, we stopped all manipulation until the facial MEP recovered. Then, we increased the stimulus intensity and recorded the supramaximal response of the amplitude. If recovery failed to reach 50 % of the baseline, we did not continue tumor removal. We calculated the ratio of the amplitude of the supramaximal EMG response at the end of the operation to the amplitude at the dural opening.
Optimal electrode placement Just before the operation, most patients underwent MRI for intraoperative navigation. After placing the patients in a lateral position suitable for retromastoid craniotomy, we investigated the primary facial motor area (Fig. 1) using a navigation system (StealthStation, Medtronic, Minneapolis, MN, USA). The anode for electrical stimulation was affixed to the scalp just above the facial motor cortex. In three patients, we then identified the best cathode placement site to obtain a good facial MEP response at the lowest stimulus intensity.
Surgical strategy All but one patient underwent tumor removal via the retrosigmoid approach. In order, we performed internal tumor decompression, removal of the tumor in the auditory meatus, and identification and preservation of the cranial nerves. Tumor resection was extracapsular in the meatal- and intracapsular in the cisternal and brainstem parts of the tumor. To avoid cranial nerve injury, we avoided dissection parallel to the nerve fibers [19].
Facial nerve monitoring Anesthesia management In group 1, we only applied occasional electrical stimulation (NIM 2.0 systems, Medtronic Xomed, Inc., Jacksonville, FL, USA) to identify the location of the facial nerve in the operative field. In group 2, we applied not only occasional electrical stimulation but also monitored facial MEP. For facial MEP monitoring, multipulse transcranial electrical stimulation was generated with a SEN-4100 instrument (Nihon Kohden Corp., Tokyo, Japan). The stimulator produced five pulses at a fixed duration of 200 μsec; the interstimulus interval was 2.0 msec. Stimuli were delivered
After induction with rocuronium bromide (0.8–1.0 mg/kg), neuroanesthesia was maintained with propofol delivered via a target-controlled infusion pump. We also administered remifentanil on a continuous basis or fentanyl as a bolus. No inhalation agents or neuromuscular blockers were used after anesthesia induction and intubation. To evaluate the anesthetic level intraoperatively, we monitored the EEG using the bispectral index method; the index was kept in the range of 40–60 (0=flat EEG, 90–100=conscious).
Neurosurg Rev (2014) 37:669–676 Fig. 1 Coronal (a) and axial (b) MRI of the neuronavigation system. a Small and large arrows indicate the left Sylvian fissure and the facial motor cortex above the Sylvian fissure, respectively. b Small and large arrows indicate the left central sulcus and the facial motor cortex anterior to the central sulcus, respectively
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a
b
Data were analyzed with the Mann–Whitney U test to compare quantitative variables in the two groups. Receiver operating characteristic (ROC) analysis was performed to estimate the cut-off point. P values equal to or less than 0.05 were considered to indicate statistically significant differences. The ethics committee of Kagoshima University Hospital approved the acquisition of facial MEP during the surgical removal of acoustic neuromas (25–174).
1), and patients 16–35 (group 2) did undergo intraoperative facial MEP monitoring. Group 1 consisted of 6 men and 9 women ranging in age from 16 to 74 years (56.9±14.4), group 2 of 7 men and 13 women (age range 27 to 75 years, 55.2± 13.9). Of the 15 group 1 patients, 7 had tumors of Koos grade III, and 5 of grade IV. In group 2, Koos grade III was recorded in 8 patients and grade IV in 7. The maximum tumor diameter ranged from 5.9 to 44.2 mm (24.5±10.9) in group 1, and from 12.2 to 41.7 mm (26.1±8.4) in group 2. The tumor extirpation rate was 93.1±7.5 % in group 1 and 92.1±5.5 % in group 2. There was no statistically significant difference between the two groups.
Results
Electrophysiological results
Statistical analysis
Optimal electrode placement We first used a navigation system to study the facial motor cortex contralateral to the operative field (Fig. 1). On axial and coronal MRI scans, we identified the Sylvian fissure, central sulcus, and the facial motor cortex just above the Sylvian fissure on the primary motor cortex. We then placed the anode on the scalp just above the facial motor cortex and the cathode at C3 or C4, and Cz. The anode and cathode of another electrode were placed at C3 and C4, respectively. With these combinations, we were able to evoke good facial MEP responses at the lowest stimulus intensity by affixing an anode to the scalp above the facial motor cortex and a cathode at Cz (Fig. 2). Surgical results Table 1 presents a summary of the characteristics of the 35 patients with acoustic neuromas; patients 1–15 did not (group
In one patient (case 21), continuous facial MEP recording failed due to movement artifacts even at 150 V stimulation. Figure 3 shows the monitored waveforms recorded from the orbicularis oculi- and orbicularis oris muscles of a patient (case 20) who manifested no postoperative facial palsy. Stable EMG responses were recorded from both muscles in response to 5-train stimulation delivered at 5-s intervals throughout the operation. Figure 4 shows the monitored EMG responses of another patient (case 25) who suffered transient postoperative facial palsy grade II. Her facial MEP deteriorated during removal of the tumor near the facial nerve and recovered after release; her final supramaximal EMG response was 300 uV; it recovered to only 47.6 % of the supramaximal EMG at the dural opening. The ratio of the amplitude of the supramaximal EMG response at the end of the operation to the amplitude at the dural opening was 39.6 ± 8.1 % in patients with transient- and 94.3 ± 27.2 % in patients without
672 Fig. 2 Raw waveforms of electromyograms (EMGs) evoked by transcranial electrical stimulation with three types of electrode combinations; anode– cathode EMGs appearing at a stimulus intensity of 200 V as a threshold (black arrow) with the C3-C4 combination, and at 150 V with the FM-C4- or the FM-Cz combination. Note the supramaximal EMGs (white arrow) observed at a stimulus intensity of 300 V with the FMCz, the 350 V with the FM-C4, and the 400 V with the C3-C4 combination
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a
C3-C4
b
FM-C4
c
FM-Cz
400V
300V
200V
100V 1mV 10msec
postoperative facial palsy. In one patient (case 17) who manifested transient postoperative facial palsy grade III, the final amplitude ratio was 32.4 %. In her case, the EMG response suddenly deteriorated during dissection of the tumor capsule near the root exit zone of the facial nerve. At that point, her EMG responses to direct facial nerve stimulation from the root exit zone to the internal auditory canal were normal. This indicated that the injured site was within the brainstem, or at the most proximal site of the root exit zone or the gross anatomical brainstem. In such cases, the facial MEP may show a lesion thought to be located in the brainstem or near the root exit zone. None of the 20 patients who underwent acoustic neuroma surgery with continuous facial MEP monitoring experienced postoperative seizures. Outcomes of facial nerve function Facial nerve function at discharge from the hospital was rated grade II in 6, and grade III and IV in one patient each from group 1; at 6 months after the operation it had improved to grade II in 2 patients. Of the 20 group 2 patients, 3 manifested grade II and 4 were recorded as grade III; in these patients facial nerve function was normal 6 months after the operation. ROC analysis indicated that patients whose facial MEP recovery rate exceeded 47.7 % tended to suffer no transient postoperative facial palsy at discharge from the hospital.
Discussion Intraoperative neurophysiological monitoring aims at detecting and preserving the function of the central or peripheral nervous system. It immediately alerts to invasion of the nervous system and helps to predict postoperative function. Preservation of postoperative facial nerve function is an important goal of acoustic neuroma surgery. According to Romstöck et al. [17], the A-train is a highly reliable predictor of postoperative facial palsy. Besides the continuous free-running EMG signals method, continuous evoked facial nerve EMGs were reported to be useful [2] and intraoperative monitoring by direct stimulation of the facial nerve in the operative field is widely accepted [12] as it facilitates the safer and faster identification of the facial nerve in pathologic-anatomic conditions. To estimate postoperative facial nerve function, facial MEP monitoring was reported to be of value [1, 4, 8, 10] although neither method allows for continuous monitoring. To preserve postoperative facial nerve function, the immediate detection of invasion of the facial nerve and the estimation of postoperative function are important. As facial nerve invasion results in postoperative dysfunction, continuous EMG monitoring by direct stimulation of the root exit zone of the facial nerves appears necessary. However, it can only be applied after exposure of the root exit zone of the facial nerve and displacement of the stimulation electrode must be corrected. Facial MEP monitoring by transcranial electrical stimulation of the motor cortex does not require the presence of an electrode in the operative field and can be used
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Table 1 Characteristics of the 35 patients with acoustic neuroma Number
Age/Sex
Koos
Size (mm)
Ext. r (%)
PreHB
PostHB1
PostHB2
AmpS (μV)
AmpE (μV)
Ratio (%)
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
53/F 41/M 59/F 69/F 72/F 74/F 63/F 49/F 59/M 56/M 16/M 69/F 54/F 62/M 58/M 65/F 75/F
IV IV III IV III IV III III I III I III II IV III IV III
30 43.6 20.7 32 21 37.4 20.5 22.2 5.9 20.4 13.2 19.8 15.9 44.2 20.1 31.9 20.6
95.5 92.9 68.1 98.0 96.1 92.7 88.9 97.8 92.2 97.1 93.5 91.5 98.9 98.6 94.2 96.2 92.0
1 2 2 1 1 1 1 1 1 1 1 1 1 2 1 2 1
1 1 2 1 2 4 2 2 1 2 1 1 2 3 1 2 3
1 1 2 1 1 2 1 1 1 1 1 1 1 1 1 1 1
128 330
61 107
18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35
42/M 59/F 45/M 27/F 31/F 57/M 59/M 42/F 61/F 73/F 61/F 54/F 65/M 62/F 62/F 72/M 57/M 34/F
IV III IV III II IV III IV IV III III IV III III II II II I
39.6 17.3 29.2 22.8 17.4 30 23.3 38.2 36.6 30 21.7 41.7 19.5 25.3 19.4 12.2 16.7 27.9
91.2 93.9 98.7 94.1 95.3 97.9 93.1 85.9 91.8 94.8 98.2 92.4 91.1 96.3 88.2 76.8 81.3 92.3
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
3 1 1 1 1 1 1 2 1 2 1 2 1 1 3 1 1 1
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
477 3,380 1,020 ns 412 102 320 630 120 517 360 167 720 523 630 510 221 618
149 3,750 1,410
31.2 110.9 138.2
333 146 185 300 109 196 280 52 700 477 300 432 121 644
80.8 143.1 57.8 47.6 90.8 37.9 77.8 31.1 97.2 91.2 47.6 84.7 54.8 104.2
47.7 32.4
ext. r extirpation rate, PreHB preoperative House and Brackmann grading, PostHB1 postoperative House and Brackmann grading at discharge from the hospital, PostHB2 postoperative House and Brackmann grading 6 months after operation, AmpS supramaximal amplitude of facial MEP at the start of operation, AmpE supramaximal amplitude of facial MEP at the end of operation, ratio ratio of AmpE/AmpS, F female, M male
throughout the operation even in patients with large tumors covering the root exit zone of the facial nerve. Transcranial electrical stimulation was first applied to the human brain by Merton and Morton [11] to activate corticofugal motor pathways. Their method was found to be practical and effective intraoperatively [20, 22], and it is now widely accepted as necessary in the neurosurgical field [9, 13, 15, 16]. Intraoperative MEP monitoring has been used during acoustic neuroma surgery for the evaluation of facial nerve function [1, 4, 8, 10]; it facilitates observation of the function
of both the first- and second motor neuron and helps to predict postoperative facial nerve function. Although intraoperative MEP monitoring reports on the function of the first and/or second motor neurons, it cannot be used with continuous stimulation because the high voltage of transcranial electrical stimulation elicits undesirable body movements. As this interferes with and raises the risks involved in neurosurgery, Macdonald [9] recommended adjusting the stimulus intensity to threshold or minimal levels, or halting all manipulations in the surgical field. Rothwell
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Orbicularis oculi
Orbicularis oris
Orbicularis oculi
500uV 10msec
7 6 5
4
1mV 10msec
Fig. 3 Patient 20. Thread of EMGs recorded from the orbicularis oculi(left columns) and the orbicularis oris muscle (right column). Transcranial electrical stimulation was applied at 5-s intervals. The waveforms were almost stable and the amplitude was retained in response to an unchanged stimulus intensity of 170 V
et al. [18] stressed that the anode must be placed above the targeted motor cortex. Elsewhere, we documented that continuous intraoperative facial MEP monitoring can be performed without eliciting undesirable body movements if the anode is placed on the scalp over the facial motor cortex and the cathode is placed on the vertex [21]. The safety of transcranial electrical stimulation is an important issue. We delivered transcranial electrical stimuli to the cerebral cortex every 10 s during intradural procedures. MacDonald [9] reviewed the safety of intraoperative transcranial electrical stimulation MEP monitoring. He found that although very brief high-frequency transcranial pulse trains appear to have a very low but not negligible association with seizures, their incidence is very low compared with other clinical brain stimulation methods. This may be attributable to the delivery of very short stimuli, to anesthesia, and to an absence of seizurepredisposing factors. Only 43 adverse events such as tongue or lip laceration, mandibular fracture, seizure, cardiac arrhythmia, scalp burn, and intraoperative awareness were reported in more than 15,000 patients who underwent MEP monitoring. His review did not address limitations with respect to the total number of stimuli delivered but concluded that the wellestablished benefits of transcranial electrical stimulation MEP monitoring decidedly outweigh the associated risks.
3
2
1 Fig. 4 Patient 25. Example of waveforms from patients with transient postoperative facial palsy. Supramaximal EMGs at the dural opening (1), base waveforms of the monitored EMG after the dural opening (2), deterioration (3), recovery (4), disappearance (5), recovery from disappearance (6), and supramaximal EMGs after removal of the tumor (7). The amplitude of EMG 7 is less than half the amplitude of EMG 1. The supramaximal amplitude (1), baseline amplitude (2), and the amplitudes after deterioration are identified with a dotted line and bilateral arrows
In a mouse model of epilepsy, low-frequency stimulation applied at 3 Hz significantly reduced the seizure frequency and duration [6], suggesting that our method of using a frequency of 0.1 Hz is safe. In their review of the efficacy and safety of motor cortex stimulation for chronic neuropathic pain, Fontaine et al. [3] reported that 12 % of patients suffered seizures during the operation or the postoperative stimulation trial. However, they noted that none of the patients presented with seizures or epilepsy in the course of prolonged follow-up. None of our patients manifested epilepsy or other adverse
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effects intraoperatively, postoperatively, or during a follow-up period ranging from 1 year to 4 years and 5 months. Facial palsy after acoustic neuroma surgery severely compromises the patients’ quality of life. Even transient facial palsy can last for several months and in some instances is accompanied by crocodile tears syndrome [14]. Our use of continuous intraoperative facial MEP monitoring helped to reduce the incidence and severity of postoperative facial palsy and resulted in a high tumor extirpation ratio. Based on our findings, we suggest a minimum amplitude preservation ratio of 50 % to avoid even transient postoperative facial palsy. Our method is applicable in patients with large acoustic tumors and does not require the presence of electrodes in the operative field. We suggest that like other modalities used for facial nerve monitoring, continuous intraoperative facial MEP monitoring helps to preserve facial nerve function in patients undergoing acoustic neuroma surgery.
Conclusion Based on the findings reported here, we suggest that intraoperative continuous monitoring of the facial MEP combined with direct facial nerve stimulation in the operative field is necessary to avoid facial nerve palsy in patients undergoing acoustic neuroma surgery.
References 1. Acioly MA, Gharabaghi A, Liebsch M, Carvalho CH, Aguiar PH, Tatagiba M (2011) Quantitative parameters of facial motor evoked potential during vestibular schwannoma surgery predict postoperative facial nerve function. Acta Neurochir 153:1169–1179 2. Amano M, Kohno M, Nagata O, Taniguchi M, Sora S, Sato H (2011) Intraoperative continuous monitoring of evoked facial nerve electromyograms in acoustic neuroma surgery. Acta Neurochir 153:1059– 1067 3. Fontaine D, Hamani C, Lazano A (2009) Efficacy and safety of motor cortex stimulation for chronic neuropathic pain: critical review of the literature. J Neurosurg 110:251–256 4. Fukuda M, Oishi M, Takao T, Saito A, Fujii Y (2008) Facial nerve motor-evoked potential monitoring during skull base surgery predicts facial nerve outcome. J Neurol Neurosurg Psychiat 79:1066–1070 5. House JW, Brackmann DE (1985) Facial nerve grading system. Otolaryngol Head Neck Surg 93:146–147 6. Kile KB, Tian N, Durand DM (2010) Low frequency stimulation decreases seizure activity in a mutation model of epilepsy. Epilepsia 51:1745–1753 7. Koos WT, Day JD, Matula C, Levy D (1998) Neurotopographic considerations in the microsurgical treatment of small acoustic neurinomas. J Neurosurg 88:506–512 8. Liu BY, Tian YJ, Liu W, Liu SL, Qiao H, Zhang JT, Jia GJ (2007) Intraoperative facial motor evoked potentials monitoring with transcranial electrical stimulation for preservation of facial nerve function in patients with large acoustic neuroma. Chin Med J 120:323–325
675 9. MacDonald DB (2002) Safety of intraoperative transcranial electrical stimulation motor evoked potential monitoring. J Clin Neurophysiol 19:416–429 10. Matthies C, Raslan F, Schweitzer T, Hagen R, Roosen K, Reiners K (2011) Facial motor evoked potentials in cerebellopontine angle surgery: technique, pitfalls and predictive value. Clin Neurol Neurosurg 113:872–879 11. Merton PA, Morton HB (1980) Stimulation of the cerebral cortex in the intact human subject. Nature 285:227 12. Meurer J, Pelster H, Amedee RG, Mann WJ (1995) Intraoperative monitoring of motor cranial nerves in skull base surgery. Skull Base Surg 5:169–175 13. Motoyama Y, Kawaguchi M, Yamada S, Nakagawa I, Nishimura F, Hironaka Y, Park YS, Hayashi H, Abe R, Nakase H (2011) Evaluation of combined use of transcranial and direct cortical motor evoked potential monitoring during unruptured aneurysm surgery. Neurol Med Chir 51:15–22 14. Nakamizo A, Yoshimoto K, Amano T, Mizoguchi M, Sasaki T (2012) Crocodile tears syndrome after vestibular schwannoma surgery. J Neurosurg 116:1121–1125 15. Quiñones-Hinojosa A, Alam M, Lyon R, Yingling CD, Lawton MT (2004) Transcranial motor evoked potentials during basilar artery aneurysm surgery: technique application for 30 consecutive patients. Neurosurgery 54:916–924 16. Ritzl EK (2012) Intraoperative neuromonitoring during glioma surgery: bring in the expert neurophysiologists! J Clin Neurophysiol 29: 151–153 17. Romstöck J, Strauss C, Fahlbusch R (2000) Continuous electromyography monitoring of motor cranial nerves during cerebellopontine angle surgery. J Neurosurg 93:586–593 18. Rothwell JC, Thompson PD, Day BL, Dick JP, Kachi T, Cowan JM, Marsden CD (1987) Motor cortex stimulation in intact man. 1. General characteristics of EMG responses in different muscles. Brain 110:1173–1190 19. Sasaki T, Shono T, Hashiguchi K, Yoshida F, Suzuki SO (2009) Histological considerations of the cleavage plane for preservation of facial and cochlear nerve functions in vestibular schwannoma surgery. J Neurosurg 110:648–655 20. Thompson PD, Day BL, Crockard HA, Calder I, Murray NM, Rothwell JC, Marsden CD (1991) Intra-operative recording of motor tract potentials at the cervico-medullary junction following scalp electrical and magnetic stimulation of the motor cortex. J Neurol Neurosurg Psychiatry 54:618–623 21. Tokimura H, Sugata S, Yamahata H, Hanaya R, Hirano H, Arita K (2012) Intraoperative continuous monitoring of facial motor evoked potentials in acoustic neuroma surgery. DGNC 22. Ubags LH, Kalkman CJ, Been HD, Koelman JH, Ongerboer de Visser BW (1999) A comparison of myogenic motor evoked responses to electrical and magnetic transcranial stimulation during nitrous oxide/opioid anesthesia. Anesth Analg 88:568–572
Comments Michihiro Kohno, Tokyo, Japan Intraoperative facial motor evoked potential (FMEP) has been considered unsuitable for continuous monitoring because this method is affected by the problem of body movement, which is obstructive for fine dissection of a tumor and/or cranial nerves. The authors have succeeded in establishing a method of obtaining stable responses from the facial muscles without body movement, using a navigation system and adjusting the stimulus intensity. As they mention in the discussion, the safety of transcranial electrical stimulation is a very important issue. Different from minor electrical
676 stimulation for the facial nerve, we should pay attention to safety for continuous high voltage and high frequent stimulation, aware that this method might induce the formation of an epileptic focus or of later disturbance of higher brain function in the long-term, in not only the intraoperative or short-term postoperative aspect. We believe that monitoring of continuous direct stimulation (1 Hz) of the facial nerve at the root exit zone (REZ) with minimal electric stimuli (1, 2) is apparently more useful than FMEP monitoring in terms of safety, body movement, and stability of the waveforms, from our experience of comparative dual use. However, FMEP has the merit that it allows us to monitor the facial nerve function before we find a REZ of the facial nerve. Finally, I think this article is important for describing the development of a method of FMEP without body movement, which the authors applied for continuous use. Using either FMEP or direct stimulation of the facial nerve, the importance of continuous monitoring of the facial nerve function in acoustic neuroma surgery should be emphasized and this would be greatly beneficial for both patients and surgeons. References 1. Amano M, Kohno M, Nagata O, Taniguchi M, Sora S, Sato H (2011) Intraoperative continuous monitoring of evoked facial nerve electromyograms in acoustic neuroma surgery. Acta Neurochirurgica 153:1059–1067 2. Kohno M, Taniguchi M (2011) Intraoperative real-time continuous facial nerve monitoring in acoustic neuroma surgery. Acta Neurochirurgica 153:2273–2274 Kiyoshi Saito, Fukushima, Japan The authors have nicely presented methods and results of intraoperative continuous monitoring of facial MEP. The facial MEP monitoring is a popular technique. We have been using it during CPA tumor surgeries. To prevent body movements, stimulus intensity must be below the intensity inducing maximal MEP amplitude. In this paper, the authors used threshold intensity +50 V, which is similar to our methods. The authors first check the maximal amplitude at the dural opening. After the dural opening, they reduced the stimulus intensity down to threshold +50 V. When MEP amplitude deteriorated, they increased the intensity to get maximal MEP amplitude. When MEP amplitude deteriorated, we also increased the stimulus intensity to get stable MEP response, but not to get the maximal MEP amplitude. We agree with the authors that MEP amplitude >50 % of the control is a key to prevent postoperative facial nerve palsy. In our practice, patients with consistent MEP amplitude >50 % of the control had no postoperative
Neurosurg Rev (2014) 37:669–676 facial nerve palsy. Patients with deterioration of MEP amplitude 50 % at the end of surgery showed full recovery from transient postoperative facial nerve palsy. In our institute, surgeons are warned to stop procedures when MEP amplitudes deteriorate
ORIGINAL ARTICLE
Intraoperative continuous monitoring of facial motor evoked potentials in acoustic neuroma surgery Hiroshi Tokimura & Sei Sugata & Hitoshi Yamahata & Shunji Yunoue & Ryosuke Hanaya & Kazunori Arita
Received: 9 June 2013 / Revised: 23 March 2014 / Accepted: 18 May 2014 / Published online: 13 July 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract The preservation of facial nerve function is one of the primary objectives in acoustic neuroma surgery. We detail our method of continuous intraoperative facial motor evoked potential (MEP) monitoring and present criteria for the preservation of facial nerve function to avoid postoperative facial nerve palsy. Our study population was comprised of 15 patients who did not (group 1), and 20 who did (group 2) undergo facial MEP monitoring during surgery to remove acoustic neuromas. In group 2, we continuously stimulated the facial motor cortex at 5- or 10-s intervals throughout surgery. Electromyograms (EMGs) were recorded from the contralateral orbicularis oculi- and orbicularis oris muscles. Optimal anode and cathode placement was at the facial motor cortex and the vertex, respectively. Postoperative facial palsy occurred in 8 of the 15 group 1 patients; in 2 it improved to grade II at 6 months after the operation. Of the 20 group 2 patients, 7 suffered postoperative facial palsy. At 6 months after the operation, their facial nerve function was normal. At the end of the operation, the ratio of the amplitude of the supramaximal EMG to the amplitude at the dural opening was 39.6 % in patients with- and 94.3 % in patients without transient postoperative facial palsy. Continuous facial MEP monitoring not only alerts to surgical invasion of the facial nerves but also helps to predict postoperative facial nerve function. To preserve a minimum amplitude ratio of 50 %, even transient postoperative facial palsy must be avoided. MEP monitoring is an additional useful modality for facial nerve monitoring during acoustic neuroma surgery.
Keywords Intraoperative monitoring . Facial nerve . Motor evoked potential . Acoustic neuroma
Introduction Observation of the A-train on free-run electromyograms (EMG) and continuous facial nerve monitoring upon stimulation at the root exit zone of the facial nerve are among the techniques accepted for the preservation of facial nerve function in patients undergoing the removal of acoustic neuromas [1, 2, 4, 12, 17]. Intraoperative monitoring of facial motor evoked potentials (MEP), introduced to evaluate facial nerve function [2, 4, 8, 10], cannot be used for continuous intraoperative monitoring because of body movement artifacts. Conventional MEP monitoring at neurological surgeries may require the placement of electrodes on the scalp to deliver highintensity electrical stimulation to not only the targeted—but also to systemic muscles. Operative manipulations must be stopped during recording of the MEP [9, 13, 15, 16]. In this study, we first attempted to identify the optimal conditions for continuous MEP monitoring of facial nerve function. Based on our findings, we then applied facial MEP monitoring throughout acoustic neuroma surgery in efforts to preserve postoperative facial nerve function. To our knowledge, this is the first report of the successful monitoring of continuous facial MEP during acoustic neuroma surgery.
Patients and methods H. Tokimura (*) : S. Sugata : H. Yamahata : S. Yunoue : R. Hanaya : K. Arita Department of Neurosurgery, Graduate School of Medical and Dental Sciences, University of Kagoshima, 8-35-1 Sakuragaoka, Kagoshima City 890-8544, Japan e-mail: [email protected]
Our study population consisted of 35 consecutive patients with acoustic neuroma treated by one neurosurgeon (H.T.) between June 2009 and January 2013. In all operated patients, we monitored facial nerve function with occasional electrical stimulation of the facial nerve. Intraoperative facial MEP
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monitoring was not used in 15 patients (group 1) and was used in 20 (group 2). In three patients, we investigated the optimal placement of electrodes affixed to the scalp and the stimulus intensity appropriate for the continuous intraoperative recording of facial MEP without eliciting body movement. Then, we recorded the facial MEP continuously from opening of the dura to the end of the tumor removal procedure. We analyzed the supramaximal amplitude of the facial MEP at the start and conclusion of the operation. Acoustic tumors were classified by the grading system of Koos et al. [7]. It classifies the tumors as grades I– IV where grade I=small intracanalicular tumor, II=small tumor with protrusion into the cerebellopontine angle, III=tumor occupying the cerebellopontine cistern with no brainstem displacement, and IV=large tumor with brainstem- and cranial nerve displacement. The size of the tumor was determined with image analysis software (Image-J, version 1.46; National Institutes of Health, Bethesda, MD) based on its maximal diameter and the area involved by the tumor on gadoliniumenhanced axial magnetic resonance images (MRI). The extirpation rate was calculated by the ratio of the postoperative tumor-free area to the area involved by the tumor. Facial nerve function was classified by the House and Brackmann grading system [5] where I=normal function, II–V reflect slight-, moderate-, moderately severe-, and severe dysfunction, respectively, and VI=total paralysis. Facial nerve function was evaluated at discharge from the hospital and 6 months after the operation.
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through two corkscrew electrodes (KS211-024, Unique Medical Co. Ltd., Tokyo, Japan) affixed to the scalp; the cathode was at Cz and the anode was above the facial motor cortex. The KS211-024 stimulator was interfaced with an electrophysiological recording system (MEE-1232, Nihon Kohden Corp.) so that a triggered EMG response was elicited by each stimulus. EMG activity evoked by transcranial electrical stimulation was recorded with subdermal needle electrodes (Medtronic Xomed, Inc., Jacksonville, FL, USA) placed in the orbicularis oculi muscle at the lateral angle of the ipsilateral eye and in the orbicularis oris muscle at the ipsilateral angle of the mouth. Recording and filtering parameters were 5–1,500 Hz. The amplifier gain was initially set at 200 μV/ division and adjusted based on the size of the EMG responses. After opening the dura, we obtained the baseline facial MEP. The facial MEP amplitude was maintained at above the threshold evoked with a stimulus approximately 50 V stronger than the threshold stimulus intensity. The stimulus intensity was adjusted to avoid body movements. The facial MEP was recorded at 5- or 10-s intervals starting at the dural opening and ending at the conclusion of tumor removal. When deterioration of the facial MEP was detected, we stopped all manipulation until the facial MEP recovered. Then, we increased the stimulus intensity and recorded the supramaximal response of the amplitude. If recovery failed to reach 50 % of the baseline, we did not continue tumor removal. We calculated the ratio of the amplitude of the supramaximal EMG response at the end of the operation to the amplitude at the dural opening.
Optimal electrode placement Just before the operation, most patients underwent MRI for intraoperative navigation. After placing the patients in a lateral position suitable for retromastoid craniotomy, we investigated the primary facial motor area (Fig. 1) using a navigation system (StealthStation, Medtronic, Minneapolis, MN, USA). The anode for electrical stimulation was affixed to the scalp just above the facial motor cortex. In three patients, we then identified the best cathode placement site to obtain a good facial MEP response at the lowest stimulus intensity.
Surgical strategy All but one patient underwent tumor removal via the retrosigmoid approach. In order, we performed internal tumor decompression, removal of the tumor in the auditory meatus, and identification and preservation of the cranial nerves. Tumor resection was extracapsular in the meatal- and intracapsular in the cisternal and brainstem parts of the tumor. To avoid cranial nerve injury, we avoided dissection parallel to the nerve fibers [19].
Facial nerve monitoring Anesthesia management In group 1, we only applied occasional electrical stimulation (NIM 2.0 systems, Medtronic Xomed, Inc., Jacksonville, FL, USA) to identify the location of the facial nerve in the operative field. In group 2, we applied not only occasional electrical stimulation but also monitored facial MEP. For facial MEP monitoring, multipulse transcranial electrical stimulation was generated with a SEN-4100 instrument (Nihon Kohden Corp., Tokyo, Japan). The stimulator produced five pulses at a fixed duration of 200 μsec; the interstimulus interval was 2.0 msec. Stimuli were delivered
After induction with rocuronium bromide (0.8–1.0 mg/kg), neuroanesthesia was maintained with propofol delivered via a target-controlled infusion pump. We also administered remifentanil on a continuous basis or fentanyl as a bolus. No inhalation agents or neuromuscular blockers were used after anesthesia induction and intubation. To evaluate the anesthetic level intraoperatively, we monitored the EEG using the bispectral index method; the index was kept in the range of 40–60 (0=flat EEG, 90–100=conscious).
Neurosurg Rev (2014) 37:669–676 Fig. 1 Coronal (a) and axial (b) MRI of the neuronavigation system. a Small and large arrows indicate the left Sylvian fissure and the facial motor cortex above the Sylvian fissure, respectively. b Small and large arrows indicate the left central sulcus and the facial motor cortex anterior to the central sulcus, respectively
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a
b
Data were analyzed with the Mann–Whitney U test to compare quantitative variables in the two groups. Receiver operating characteristic (ROC) analysis was performed to estimate the cut-off point. P values equal to or less than 0.05 were considered to indicate statistically significant differences. The ethics committee of Kagoshima University Hospital approved the acquisition of facial MEP during the surgical removal of acoustic neuromas (25–174).
1), and patients 16–35 (group 2) did undergo intraoperative facial MEP monitoring. Group 1 consisted of 6 men and 9 women ranging in age from 16 to 74 years (56.9±14.4), group 2 of 7 men and 13 women (age range 27 to 75 years, 55.2± 13.9). Of the 15 group 1 patients, 7 had tumors of Koos grade III, and 5 of grade IV. In group 2, Koos grade III was recorded in 8 patients and grade IV in 7. The maximum tumor diameter ranged from 5.9 to 44.2 mm (24.5±10.9) in group 1, and from 12.2 to 41.7 mm (26.1±8.4) in group 2. The tumor extirpation rate was 93.1±7.5 % in group 1 and 92.1±5.5 % in group 2. There was no statistically significant difference between the two groups.
Results
Electrophysiological results
Statistical analysis
Optimal electrode placement We first used a navigation system to study the facial motor cortex contralateral to the operative field (Fig. 1). On axial and coronal MRI scans, we identified the Sylvian fissure, central sulcus, and the facial motor cortex just above the Sylvian fissure on the primary motor cortex. We then placed the anode on the scalp just above the facial motor cortex and the cathode at C3 or C4, and Cz. The anode and cathode of another electrode were placed at C3 and C4, respectively. With these combinations, we were able to evoke good facial MEP responses at the lowest stimulus intensity by affixing an anode to the scalp above the facial motor cortex and a cathode at Cz (Fig. 2). Surgical results Table 1 presents a summary of the characteristics of the 35 patients with acoustic neuromas; patients 1–15 did not (group
In one patient (case 21), continuous facial MEP recording failed due to movement artifacts even at 150 V stimulation. Figure 3 shows the monitored waveforms recorded from the orbicularis oculi- and orbicularis oris muscles of a patient (case 20) who manifested no postoperative facial palsy. Stable EMG responses were recorded from both muscles in response to 5-train stimulation delivered at 5-s intervals throughout the operation. Figure 4 shows the monitored EMG responses of another patient (case 25) who suffered transient postoperative facial palsy grade II. Her facial MEP deteriorated during removal of the tumor near the facial nerve and recovered after release; her final supramaximal EMG response was 300 uV; it recovered to only 47.6 % of the supramaximal EMG at the dural opening. The ratio of the amplitude of the supramaximal EMG response at the end of the operation to the amplitude at the dural opening was 39.6 ± 8.1 % in patients with transient- and 94.3 ± 27.2 % in patients without
672 Fig. 2 Raw waveforms of electromyograms (EMGs) evoked by transcranial electrical stimulation with three types of electrode combinations; anode– cathode EMGs appearing at a stimulus intensity of 200 V as a threshold (black arrow) with the C3-C4 combination, and at 150 V with the FM-C4- or the FM-Cz combination. Note the supramaximal EMGs (white arrow) observed at a stimulus intensity of 300 V with the FMCz, the 350 V with the FM-C4, and the 400 V with the C3-C4 combination
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a
C3-C4
b
FM-C4
c
FM-Cz
400V
300V
200V
100V 1mV 10msec
postoperative facial palsy. In one patient (case 17) who manifested transient postoperative facial palsy grade III, the final amplitude ratio was 32.4 %. In her case, the EMG response suddenly deteriorated during dissection of the tumor capsule near the root exit zone of the facial nerve. At that point, her EMG responses to direct facial nerve stimulation from the root exit zone to the internal auditory canal were normal. This indicated that the injured site was within the brainstem, or at the most proximal site of the root exit zone or the gross anatomical brainstem. In such cases, the facial MEP may show a lesion thought to be located in the brainstem or near the root exit zone. None of the 20 patients who underwent acoustic neuroma surgery with continuous facial MEP monitoring experienced postoperative seizures. Outcomes of facial nerve function Facial nerve function at discharge from the hospital was rated grade II in 6, and grade III and IV in one patient each from group 1; at 6 months after the operation it had improved to grade II in 2 patients. Of the 20 group 2 patients, 3 manifested grade II and 4 were recorded as grade III; in these patients facial nerve function was normal 6 months after the operation. ROC analysis indicated that patients whose facial MEP recovery rate exceeded 47.7 % tended to suffer no transient postoperative facial palsy at discharge from the hospital.
Discussion Intraoperative neurophysiological monitoring aims at detecting and preserving the function of the central or peripheral nervous system. It immediately alerts to invasion of the nervous system and helps to predict postoperative function. Preservation of postoperative facial nerve function is an important goal of acoustic neuroma surgery. According to Romstöck et al. [17], the A-train is a highly reliable predictor of postoperative facial palsy. Besides the continuous free-running EMG signals method, continuous evoked facial nerve EMGs were reported to be useful [2] and intraoperative monitoring by direct stimulation of the facial nerve in the operative field is widely accepted [12] as it facilitates the safer and faster identification of the facial nerve in pathologic-anatomic conditions. To estimate postoperative facial nerve function, facial MEP monitoring was reported to be of value [1, 4, 8, 10] although neither method allows for continuous monitoring. To preserve postoperative facial nerve function, the immediate detection of invasion of the facial nerve and the estimation of postoperative function are important. As facial nerve invasion results in postoperative dysfunction, continuous EMG monitoring by direct stimulation of the root exit zone of the facial nerves appears necessary. However, it can only be applied after exposure of the root exit zone of the facial nerve and displacement of the stimulation electrode must be corrected. Facial MEP monitoring by transcranial electrical stimulation of the motor cortex does not require the presence of an electrode in the operative field and can be used
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Table 1 Characteristics of the 35 patients with acoustic neuroma Number
Age/Sex
Koos
Size (mm)
Ext. r (%)
PreHB
PostHB1
PostHB2
AmpS (μV)
AmpE (μV)
Ratio (%)
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
53/F 41/M 59/F 69/F 72/F 74/F 63/F 49/F 59/M 56/M 16/M 69/F 54/F 62/M 58/M 65/F 75/F
IV IV III IV III IV III III I III I III II IV III IV III
30 43.6 20.7 32 21 37.4 20.5 22.2 5.9 20.4 13.2 19.8 15.9 44.2 20.1 31.9 20.6
95.5 92.9 68.1 98.0 96.1 92.7 88.9 97.8 92.2 97.1 93.5 91.5 98.9 98.6 94.2 96.2 92.0
1 2 2 1 1 1 1 1 1 1 1 1 1 2 1 2 1
1 1 2 1 2 4 2 2 1 2 1 1 2 3 1 2 3
1 1 2 1 1 2 1 1 1 1 1 1 1 1 1 1 1
128 330
61 107
18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35
42/M 59/F 45/M 27/F 31/F 57/M 59/M 42/F 61/F 73/F 61/F 54/F 65/M 62/F 62/F 72/M 57/M 34/F
IV III IV III II IV III IV IV III III IV III III II II II I
39.6 17.3 29.2 22.8 17.4 30 23.3 38.2 36.6 30 21.7 41.7 19.5 25.3 19.4 12.2 16.7 27.9
91.2 93.9 98.7 94.1 95.3 97.9 93.1 85.9 91.8 94.8 98.2 92.4 91.1 96.3 88.2 76.8 81.3 92.3
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
3 1 1 1 1 1 1 2 1 2 1 2 1 1 3 1 1 1
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
477 3,380 1,020 ns 412 102 320 630 120 517 360 167 720 523 630 510 221 618
149 3,750 1,410
31.2 110.9 138.2
333 146 185 300 109 196 280 52 700 477 300 432 121 644
80.8 143.1 57.8 47.6 90.8 37.9 77.8 31.1 97.2 91.2 47.6 84.7 54.8 104.2
47.7 32.4
ext. r extirpation rate, PreHB preoperative House and Brackmann grading, PostHB1 postoperative House and Brackmann grading at discharge from the hospital, PostHB2 postoperative House and Brackmann grading 6 months after operation, AmpS supramaximal amplitude of facial MEP at the start of operation, AmpE supramaximal amplitude of facial MEP at the end of operation, ratio ratio of AmpE/AmpS, F female, M male
throughout the operation even in patients with large tumors covering the root exit zone of the facial nerve. Transcranial electrical stimulation was first applied to the human brain by Merton and Morton [11] to activate corticofugal motor pathways. Their method was found to be practical and effective intraoperatively [20, 22], and it is now widely accepted as necessary in the neurosurgical field [9, 13, 15, 16]. Intraoperative MEP monitoring has been used during acoustic neuroma surgery for the evaluation of facial nerve function [1, 4, 8, 10]; it facilitates observation of the function
of both the first- and second motor neuron and helps to predict postoperative facial nerve function. Although intraoperative MEP monitoring reports on the function of the first and/or second motor neurons, it cannot be used with continuous stimulation because the high voltage of transcranial electrical stimulation elicits undesirable body movements. As this interferes with and raises the risks involved in neurosurgery, Macdonald [9] recommended adjusting the stimulus intensity to threshold or minimal levels, or halting all manipulations in the surgical field. Rothwell
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Orbicularis oculi
Orbicularis oris
Orbicularis oculi
500uV 10msec
7 6 5
4
1mV 10msec
Fig. 3 Patient 20. Thread of EMGs recorded from the orbicularis oculi(left columns) and the orbicularis oris muscle (right column). Transcranial electrical stimulation was applied at 5-s intervals. The waveforms were almost stable and the amplitude was retained in response to an unchanged stimulus intensity of 170 V
et al. [18] stressed that the anode must be placed above the targeted motor cortex. Elsewhere, we documented that continuous intraoperative facial MEP monitoring can be performed without eliciting undesirable body movements if the anode is placed on the scalp over the facial motor cortex and the cathode is placed on the vertex [21]. The safety of transcranial electrical stimulation is an important issue. We delivered transcranial electrical stimuli to the cerebral cortex every 10 s during intradural procedures. MacDonald [9] reviewed the safety of intraoperative transcranial electrical stimulation MEP monitoring. He found that although very brief high-frequency transcranial pulse trains appear to have a very low but not negligible association with seizures, their incidence is very low compared with other clinical brain stimulation methods. This may be attributable to the delivery of very short stimuli, to anesthesia, and to an absence of seizurepredisposing factors. Only 43 adverse events such as tongue or lip laceration, mandibular fracture, seizure, cardiac arrhythmia, scalp burn, and intraoperative awareness were reported in more than 15,000 patients who underwent MEP monitoring. His review did not address limitations with respect to the total number of stimuli delivered but concluded that the wellestablished benefits of transcranial electrical stimulation MEP monitoring decidedly outweigh the associated risks.
3
2
1 Fig. 4 Patient 25. Example of waveforms from patients with transient postoperative facial palsy. Supramaximal EMGs at the dural opening (1), base waveforms of the monitored EMG after the dural opening (2), deterioration (3), recovery (4), disappearance (5), recovery from disappearance (6), and supramaximal EMGs after removal of the tumor (7). The amplitude of EMG 7 is less than half the amplitude of EMG 1. The supramaximal amplitude (1), baseline amplitude (2), and the amplitudes after deterioration are identified with a dotted line and bilateral arrows
In a mouse model of epilepsy, low-frequency stimulation applied at 3 Hz significantly reduced the seizure frequency and duration [6], suggesting that our method of using a frequency of 0.1 Hz is safe. In their review of the efficacy and safety of motor cortex stimulation for chronic neuropathic pain, Fontaine et al. [3] reported that 12 % of patients suffered seizures during the operation or the postoperative stimulation trial. However, they noted that none of the patients presented with seizures or epilepsy in the course of prolonged follow-up. None of our patients manifested epilepsy or other adverse
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effects intraoperatively, postoperatively, or during a follow-up period ranging from 1 year to 4 years and 5 months. Facial palsy after acoustic neuroma surgery severely compromises the patients’ quality of life. Even transient facial palsy can last for several months and in some instances is accompanied by crocodile tears syndrome [14]. Our use of continuous intraoperative facial MEP monitoring helped to reduce the incidence and severity of postoperative facial palsy and resulted in a high tumor extirpation ratio. Based on our findings, we suggest a minimum amplitude preservation ratio of 50 % to avoid even transient postoperative facial palsy. Our method is applicable in patients with large acoustic tumors and does not require the presence of electrodes in the operative field. We suggest that like other modalities used for facial nerve monitoring, continuous intraoperative facial MEP monitoring helps to preserve facial nerve function in patients undergoing acoustic neuroma surgery.
Conclusion Based on the findings reported here, we suggest that intraoperative continuous monitoring of the facial MEP combined with direct facial nerve stimulation in the operative field is necessary to avoid facial nerve palsy in patients undergoing acoustic neuroma surgery.
References 1. Acioly MA, Gharabaghi A, Liebsch M, Carvalho CH, Aguiar PH, Tatagiba M (2011) Quantitative parameters of facial motor evoked potential during vestibular schwannoma surgery predict postoperative facial nerve function. Acta Neurochir 153:1169–1179 2. Amano M, Kohno M, Nagata O, Taniguchi M, Sora S, Sato H (2011) Intraoperative continuous monitoring of evoked facial nerve electromyograms in acoustic neuroma surgery. Acta Neurochir 153:1059– 1067 3. Fontaine D, Hamani C, Lazano A (2009) Efficacy and safety of motor cortex stimulation for chronic neuropathic pain: critical review of the literature. J Neurosurg 110:251–256 4. Fukuda M, Oishi M, Takao T, Saito A, Fujii Y (2008) Facial nerve motor-evoked potential monitoring during skull base surgery predicts facial nerve outcome. J Neurol Neurosurg Psychiat 79:1066–1070 5. House JW, Brackmann DE (1985) Facial nerve grading system. Otolaryngol Head Neck Surg 93:146–147 6. Kile KB, Tian N, Durand DM (2010) Low frequency stimulation decreases seizure activity in a mutation model of epilepsy. Epilepsia 51:1745–1753 7. Koos WT, Day JD, Matula C, Levy D (1998) Neurotopographic considerations in the microsurgical treatment of small acoustic neurinomas. J Neurosurg 88:506–512 8. Liu BY, Tian YJ, Liu W, Liu SL, Qiao H, Zhang JT, Jia GJ (2007) Intraoperative facial motor evoked potentials monitoring with transcranial electrical stimulation for preservation of facial nerve function in patients with large acoustic neuroma. Chin Med J 120:323–325
675 9. MacDonald DB (2002) Safety of intraoperative transcranial electrical stimulation motor evoked potential monitoring. J Clin Neurophysiol 19:416–429 10. Matthies C, Raslan F, Schweitzer T, Hagen R, Roosen K, Reiners K (2011) Facial motor evoked potentials in cerebellopontine angle surgery: technique, pitfalls and predictive value. Clin Neurol Neurosurg 113:872–879 11. Merton PA, Morton HB (1980) Stimulation of the cerebral cortex in the intact human subject. Nature 285:227 12. Meurer J, Pelster H, Amedee RG, Mann WJ (1995) Intraoperative monitoring of motor cranial nerves in skull base surgery. Skull Base Surg 5:169–175 13. Motoyama Y, Kawaguchi M, Yamada S, Nakagawa I, Nishimura F, Hironaka Y, Park YS, Hayashi H, Abe R, Nakase H (2011) Evaluation of combined use of transcranial and direct cortical motor evoked potential monitoring during unruptured aneurysm surgery. Neurol Med Chir 51:15–22 14. Nakamizo A, Yoshimoto K, Amano T, Mizoguchi M, Sasaki T (2012) Crocodile tears syndrome after vestibular schwannoma surgery. J Neurosurg 116:1121–1125 15. Quiñones-Hinojosa A, Alam M, Lyon R, Yingling CD, Lawton MT (2004) Transcranial motor evoked potentials during basilar artery aneurysm surgery: technique application for 30 consecutive patients. Neurosurgery 54:916–924 16. Ritzl EK (2012) Intraoperative neuromonitoring during glioma surgery: bring in the expert neurophysiologists! J Clin Neurophysiol 29: 151–153 17. Romstöck J, Strauss C, Fahlbusch R (2000) Continuous electromyography monitoring of motor cranial nerves during cerebellopontine angle surgery. J Neurosurg 93:586–593 18. Rothwell JC, Thompson PD, Day BL, Dick JP, Kachi T, Cowan JM, Marsden CD (1987) Motor cortex stimulation in intact man. 1. General characteristics of EMG responses in different muscles. Brain 110:1173–1190 19. Sasaki T, Shono T, Hashiguchi K, Yoshida F, Suzuki SO (2009) Histological considerations of the cleavage plane for preservation of facial and cochlear nerve functions in vestibular schwannoma surgery. J Neurosurg 110:648–655 20. Thompson PD, Day BL, Crockard HA, Calder I, Murray NM, Rothwell JC, Marsden CD (1991) Intra-operative recording of motor tract potentials at the cervico-medullary junction following scalp electrical and magnetic stimulation of the motor cortex. J Neurol Neurosurg Psychiatry 54:618–623 21. Tokimura H, Sugata S, Yamahata H, Hanaya R, Hirano H, Arita K (2012) Intraoperative continuous monitoring of facial motor evoked potentials in acoustic neuroma surgery. DGNC 22. Ubags LH, Kalkman CJ, Been HD, Koelman JH, Ongerboer de Visser BW (1999) A comparison of myogenic motor evoked responses to electrical and magnetic transcranial stimulation during nitrous oxide/opioid anesthesia. Anesth Analg 88:568–572
Comments Michihiro Kohno, Tokyo, Japan Intraoperative facial motor evoked potential (FMEP) has been considered unsuitable for continuous monitoring because this method is affected by the problem of body movement, which is obstructive for fine dissection of a tumor and/or cranial nerves. The authors have succeeded in establishing a method of obtaining stable responses from the facial muscles without body movement, using a navigation system and adjusting the stimulus intensity. As they mention in the discussion, the safety of transcranial electrical stimulation is a very important issue. Different from minor electrical
676 stimulation for the facial nerve, we should pay attention to safety for continuous high voltage and high frequent stimulation, aware that this method might induce the formation of an epileptic focus or of later disturbance of higher brain function in the long-term, in not only the intraoperative or short-term postoperative aspect. We believe that monitoring of continuous direct stimulation (1 Hz) of the facial nerve at the root exit zone (REZ) with minimal electric stimuli (1, 2) is apparently more useful than FMEP monitoring in terms of safety, body movement, and stability of the waveforms, from our experience of comparative dual use. However, FMEP has the merit that it allows us to monitor the facial nerve function before we find a REZ of the facial nerve. Finally, I think this article is important for describing the development of a method of FMEP without body movement, which the authors applied for continuous use. Using either FMEP or direct stimulation of the facial nerve, the importance of continuous monitoring of the facial nerve function in acoustic neuroma surgery should be emphasized and this would be greatly beneficial for both patients and surgeons. References 1. Amano M, Kohno M, Nagata O, Taniguchi M, Sora S, Sato H (2011) Intraoperative continuous monitoring of evoked facial nerve electromyograms in acoustic neuroma surgery. Acta Neurochirurgica 153:1059–1067 2. Kohno M, Taniguchi M (2011) Intraoperative real-time continuous facial nerve monitoring in acoustic neuroma surgery. Acta Neurochirurgica 153:2273–2274 Kiyoshi Saito, Fukushima, Japan The authors have nicely presented methods and results of intraoperative continuous monitoring of facial MEP. The facial MEP monitoring is a popular technique. We have been using it during CPA tumor surgeries. To prevent body movements, stimulus intensity must be below the intensity inducing maximal MEP amplitude. In this paper, the authors used threshold intensity +50 V, which is similar to our methods. The authors first check the maximal amplitude at the dural opening. After the dural opening, they reduced the stimulus intensity down to threshold +50 V. When MEP amplitude deteriorated, they increased the intensity to get maximal MEP amplitude. When MEP amplitude deteriorated, we also increased the stimulus intensity to get stable MEP response, but not to get the maximal MEP amplitude. We agree with the authors that MEP amplitude >50 % of the control is a key to prevent postoperative facial nerve palsy. In our practice, patients with consistent MEP amplitude >50 % of the control had no postoperative
Neurosurg Rev (2014) 37:669–676 facial nerve palsy. Patients with deterioration of MEP amplitude 50 % at the end of surgery showed full recovery from transient postoperative facial nerve palsy. In our institute, surgeons are warned to stop procedures when MEP amplitudes deteriorate
