Original Article

Intraoperative Monitoring of Facial Nerve Motor-Evoked Potentials in Children Oliver Bozinov1,2, Michael A. Grotzer2,3, Johannes Sarnthein1,2,4

OBJECTIVE: To determine whether transcranial motorevoked potential monitoring of the facial nerve (FNMEP) during eloquent tumor resection is feasible in children and can predict both immediate and postoperative facial nerve (FN) function.

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METHODS: We included 24 consecutive procedures involving 21 patients (median age 5.5 years, range 5 months to 15 years, 8 female) who were operated on with FNMEP monitoring by the first author in 2013 and 2014. During surgery, we maintained a constant response amplitude by increasing the stimulation intensity and aimed to establish a warning criterion based on the “threshold-level” method. A threshold increase of greater than 20 mA for eliciting the FNMEP in the most reliable facial nerve target muscle was considered to be a prediction of reduced postoperative facial nerve function and consequently, a warning was given to the surgeon. The preoperative and early postoperative function was documented with the HouseBrackmann grading system.

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RESULTS: Monitoring of the FNMEP was feasible in all the surgeries in at least one facial nerve target muscle. The orbicularis oris muscle yielded the best result (95% of the trials), followed by the mentalis (87%) and orbicularis oculi muscles (86%). The median stimulation threshold was initially 65 mA (range 40e110 mA) for the FNMEP and 60 mA

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Key words Infants - Facial nerve - House-Brackmann grade - Motor-evoked potentials - Pediatrics - Threshold-level -

Abbreviations and Acronyms CI: Confidence interval CPA: Cerebellopontine angle DES: Direct electrical stimulation EMG: Electromyography FN: Facial nerve Fneg: False negative FNMEP: Facial nerve motor-evoked potential FP: False positive FPR: False-positive rate HB: House-Brackmann IONM: Intraoperative neurophysiologic monitoring

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(15e220 mA) for the motor-evoked potential of the thenar muscles. The FNMEP deterioration showed a sensitivity of 100% for House-Brackmann deterioration and specificity of 74%. CONCLUSIONS: Intraoperative FNMEP monitoring is feasible and safe in infants and children. We found no evidence that the procedures and thresholds should differ from FNMEP monitoring in adults. FNMEP monitoring provides valid evidence for FN function in pediatric eloquent area surgery; its use is complementary to direct electrical FN stimulation and continuous EMG monitoring of FN target muscles.

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INTRODUCTION

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urgery near pyramidal or corticobulbar tracts or the motor cranial nerve, particularly in the cerebellopontine angle, carries a risk of impaired motor function, also through damage to the facial nerve (FN). Among the technical measures to preserve FN function, intraoperative neurophysiological monitoring (IONM) has become mandatory and its use is increasing (3). During surgery, IONM serves to communicate impending nerve damage to the surgeon and to predict the postoperative neurologic state. As a standard method of IONM, direct electrical stimulation (DES) of

MEP: Motor-evoked potential TES: Transcranial electric stimulation TN: True negative TP: True positive WHO: World Health Organization From the 1Neurosurgery Department, University Hospital Zurich, Zurich, Switzerland; 2 University of Zurich, Zurich, Switzerland; 3Department of Pediatric Oncology, University Children’s Hospital Zurich, Zurich, Switzerland; and 4Zurich Neuroscience Center, ETHZ, Zurich, Switzerland To whom correspondence should be addressed: Dr. Johannes Sarnthein, PhD [E-mail: [email protected]] Citation: World Neurosurg. (2015) 84, 3:786-794. http://dx.doi.org/10.1016/j.wneu.2015.05.008 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.

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ORIGINAL ARTICLE OLIVER BOZINOV ET AL.

the FN serves to elicit compound muscle potentials recorded from FN target muscles. DES is used to identify the FN in the surgical field and to map its course as well as to intermittently test the FN function. As another standard method, continuous electromyography (EMG) of FN target muscles provides continuous feedback on FN activity. More recently, the facial nerve motor-evoked potential (FNMEP) has been introduced (4, 8). The FNMEP activates the motor pathway proximate to the surgical field by transcranial electric stimulation (TES) of the motor cortex and records the responses in the FN target muscles. With this technique, the supranuclear tract and FN function can be monitored continuously. Despite this advantage, FNMEP has not become a standard tool of IONM, possibly because of artifacts in the signals and uncertainties in the interpretation of the results. Particular care is necessary to avoid confounding the muscle response to stimulation through the corticobulbar tract with muscle response to peripheral stimulation. This confounding is illustrated in Figure 1. In adult patients, most authors use a decrease in the FNMEP response amplitude as a warning criterion (1-4, 10, 13); however, FNMEP responses have inherent variability and are difficult to quantify. In addition, high FNMEP stimulation intensity is needed to achieve the maximal FNMEP response at baseline so that subsequent response deterioration can be assessed. In an earlier publication (14), we monitored the increase in the stimulation threshold needed to elicit the FNMEP to communicate with the surgeon and to predict postoperative function of the facial nerve. In children, the motor system is not fully matured. For the corticospinal tract, the predictive power of MEP has been

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documented (6); however, D-waves might be absent in very young children (15). Given these findings, we aimed to investigate the feasibility and safety of FNMEP monitoring during neurosurgical interventions in children and infants and whether FNMEP would similarly predict FN function in a pediatric population. PATIENTS AND METHODS Patient Selection We included all consecutive pediatric patients in 2013 and 2014 who were operated on by the first author (O.B.) for eloquent lesions requiring facial nerve monitoring in which the last author (J.S.) performed the IONM. The collection of personal patient data was prospective. The scientific workup was approved upfront by the institutional ethics review board (Kantonale Ethikkommission KEK-ZH 2012-0212). The selection criterion resulted in a series of 24 surgical procedures in 21 patients (median age 5.5 years, range 5 months to 15 years, 8 female). The patient characteristics are listed in Table 1. Pathology and Treatment Table 1 lists the patients’ pathology. Fourteen patients were operated on for astrocytoma, 6 for ependymoma, and 4 for other pathologies (glioblastoma, medulloblastoma, aneurysmatic bone cyst, glioneuronal tumor). The lesions are depicted in Figure 2A together with postoperative images (Figure 2B) to estimate the extent of resection. Neurologic Assessment The House-Brackmann (HB) Grading System (range 1e6; grade 1: normal facial muscle function, grade 6: total palsy) was used to determine the facial nerve function (House and Brackmann, 1985). The preoperative scores and postoperative scores at the first postoperative day were obtained by a pediatric neuro-oncologist (M.A.G). Anesthesia Management Following our standard protocol for neurosurgical interventions, anesthesia was induced with intravenous application of Propofol (1.5-2 mg/kg) and Fentanyl (2-3 mg/kg). The intratracheal intubation was facilitated by Atracurium (0.5 mg/kg). Anesthesia was maintained with Propofol (5-10 mg/kg/h) and Remifentanil (0.1-2 mg/kg/min).

Figure 1. Activation of the corticobulbar tract versus peripheral stimulation of facial nerve (FN) target muscles. During activation of the corticobulbar tract, anodal stimulation of the motor cortex (red arrow) elicits activation of the lower motor neurons in the FN nucleus of the brainstem where FN target muscles are activated. Additionally, as a confounder, peripheral stimulation (yellow arrows) might activate FN target muscles, although at shorter latencies and in response to single stimulation pulses.

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Neurophysiologic Monitoring Technique IONM with continuous EMG of the FN target muscles was recorded using the ISIS system (inomed Medizintechnik GmbH, Emmendingen, Germany; www.inomed.com). DES for the precise localization of the FN in the surgical field was initiated with 0.2 mA at a large distance from the FN and was reduced to a minimal current of 0.05 mA as long as the FN was well identified. TES for the FNMEP was performed using a constant current stimulator with a maximal stimulator output 220 mA. The upper-limb motorevoked potential (MEP) and FNMEP responses were amplified and filtered (100e3000 Hz) before display.

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Case No.

Age, years

Age, months

1

2

32

F

2

2

32

M

3

1

14

M

Sex

Pathology and WHO Grade

FNMEP Start, mA

FNMEP End, mA

No

95

110

No

No

100

150

Yes

No

75

80

No

Lesion Location

Preoperative HB Grade

Postoperative HB Grade

HB Grade Deterioration

Pilomyxoid astrocytoma II

Pons

3

3

Pilomyxoid astrocytoma II

Opticus

3

3

Anaplastic ependymoma III

Pons

1

1

FNMEP Increase, ‡20 mA

2

27

M

Astrocytoma SEGA

Precentral

1

1

No

90

95

No

5

2

31

M

Astrocytoma II

Mesencephalon

1

3

Yes

45

65

Yes

6

15

182

F

Astrocytoma II

Medulla oblongata

2

2

No

40

63

No

7

8

96

M

Astrocytoma III

CPA

2

2

No

40

45

No

8

10

121

M

Pilocytic astrocytoma I

Medulla oblongata

1

1

No

75

80

No

9

3

37

M

Pilocytic astrocytoma I

CPA

1

1

No

63

61

No

10

5

63

F

Pilocytic astrocytoma I

IV ventricle

1

1

No

60

80

Yes

11

5

64

F

Pilocytic astrocytoma

IV ventricle

1

1

No

60

80

Yes

12

8

97

M

Anaplastic ependymoma III

IV ventricle

1

1

No

40

55

No

13

14

174

M

Medulloblastoma

IV ventricle

1

1

No

45

55

No

14

12

150

F

Ependymoma II

15

3

41

M

Diffuse astrocytoma II

16

11

137

M

Glioblastoma IV

17

14

172

F

Glioneural tumor I

18

6

72

M

Aneurysmatic bone cyst

19

9

113

M

Pilocytic astrocytoma I

Pons

1

20

6

74

F

Ependymoma II

Pons

2

21

3

46

M

Pilocytic astrocytoma

Pons

1

1

1

18

M

Anaplastic ependymoma III

23

12

150

F

Pilocytic astrocytoma

24

0

5

M

Anaplastic ependymoma III

1

1

No

65

65

No

1

1

No

73

140

Yes

Skull base

1

1

No

50

50

No

Mesencephalon

1

1

No

65

75

No

Thalamus

1

1

No

110

115

No

1

No

100

110

No

2

No

70

80

No

No

65

90

No

Mesencephalon

3

2

No

80

80

Yes

Cervical

1

1

No

100

100

No

Pons

2

2

No

45

75

Yes

WHO, World Health Organization; HB, House-Brackmann; FNMEP, facial nerve motor-evoked potential; F, female; M, male; SEGA, subependymal giant cell astrcytoma; CPA, cerebellopontine angle.

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Figure 2. Representative magnetic resonance imaging (MRI) of the targeted lesion in the 24 cases preoperatively (A) and early postoperatively (B). Only B-18 is a MRI control 3 months postoperatively. Two of these cases had an open biopsy only (patients 6 and 7), whereas 5 others had a partial resection with decompression (patients 1, 2, 5, 10, and 15). In 10 cases, a gross total resection was achieved and confirmed with extent of resection (EOR) >95% (patients 8, 9, 11, 13, 14, 16, 17, 19, 20, and 24). The remaining 7 cases (patients 3, 4, 12, 18, 21, 22, and 23) were resected completely and confirmed by early postoperative MRI. With increasing experience in the monitoring technique presented here, the latter half of this consecutive series has a significantly greater rate of EOR.

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Sites for Recording Muscle Activity We recorded the FN responses from the facial nerve target muscles orbicularis oculi, orbicularis oris, and mentalis. Depending on the requirements of the surgery, in some patients only a subset of the facial nerve target muscles was recorded. The MEP responses from other cranial nerve target muscles and thenar muscles are presented here for comparison.

Electrodes for Recording Muscle Activity We used twisted-pair noninsulated straight needle electrodes placed under the skin (stainless steel, 0.4  12 mm Neuroline twisted pair; Ambu, Ballerup, Denmark, www.ambu.com) in the FN target muscles (Figure 1) and in the thenar muscles. Impedance typically was less than 5 kU. For the FN target muscles, we used the same electrodes for adults and children.

Transcranial Electric Stimulation TES current was delivered through pairs of corkscrew electrodes (inomed Medizintechnik GmbH) placed on the scalp overlying the hand area of the motor cortex. Same as in adults, a roll of gauze was placed in the mouth to prevent bite injuries of the tongue or gingivae resulting from motor stimulation of the jaw. When intraoperative 3-T magnetic resonance imaging was used, corkscrew electrodes were replaced by platinum/iridium 0.4  12-mm straight needles (529500; inomed Medizintechnik GmbH), as described recently (7). In cases in which the laterality of the response was an issue, we stimulated in the C3 versus Cz and C4 versus Cz montages. TES was then performed by applying anodal pulses with 0.5 ms pulse width. In cases in which low thresholds were required, we stimulated in the C3 versus C4 montage, which is optimal for low MEP stimulation thresholds for the upper extremities (16). TES was then performed by applying symmetrically biphasic rectangular pulses with positive and negative deflections during the pulse width. The width of the anodal phase was 0.5 ms. Only the phase of the anodal current was considered in the calculation of the effective charge that was delivered to the patient. The TES pulses were applied in trains of 3e7 pulses for the FNMEP. We used an interstimulus interval ISI ¼ 2 ms between pulses to widen the interval between the TES artifact in the signal traces and the FNMEP response. To distinguish between a true corticobulbar tract activation and a motor response elicited by peripheral FN activation (17), we added a 20-ms control pulse before the pulse train. FNMEP was considered feasible if the parameters could be selected so that, for at least one target muscle of the respective FN, the TES pulse train, and not the control pulse, elicited a response. For stimulation of the MEP we used ISI ¼ 4 ms, which has been shown to be optimal in most cases (16). In addition, we had the option of using the double train technique, i.e., 2 trains (intertrain interval, 20 ms) of 5 pulses each. This stimulation technique yields more robust MEP responses with low stimulation intensity. It is recommended in situations in which anesthetic agents accumulate during long surgeries or in which the depth of anesthesia oscillates, which is more likely in children than in adults.

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Determination of the FNMEP Stimulation Threshold The baseline FNMEP stimulation threshold was determined before the opening of the dura. To obtain the baseline MEP threshold, we started with a fixed pattern of stimulus intensity at 20 mA and increased it by 5 mA-increments until one of the target muscles responded reliably to stimulation. At least 2 seconds elapsed from one stimulus train to another. An evoked FNMEP response as low as 20 mV with appropriate response latency qualified as a reliable FNMEP response (5, 14), although the responses typically were >100 mV. The FNMEP stimulation threshold was kept as low as possible, because greater stimulation might lead to disturbing body jerks and peripheral stimulation of FN target muscles (11). If jerks were inevitable, the timing of the stimulation had to be coordinated with the surgeon as not to jeopardize micro dissections. The testing was repeated continuously and at short intervals when the FN function was assumed to be at risk. Neurophysiologic Data Analysis When reduced FNMEP amplitude responses were observed, technical failures were ruled out first and the anesthesia parameters were checked. Second, the number of stimulating pulses and subsequently the FNMEP stimulation intensity were increased to obtain a constant FNMEP response amplitude. Gradually progressive threshold elevations were attributed to anesthetic fade (12), and the baseline FNMEP threshold was adjusted (5, 14). Rapid threshold elevations within minutes were analyzed in the context of the surgical manipulations and were considered to be possibly pathologic. The FNMEPs were considered deteriorated, and the surgical team was notified whenever the FNMEP intensity threshold had to be increased by >20 mA (5, 14). The data analysis focused on the facial nerve target muscle with the most salient FNMEP response and in which corticobulbar—as opposed to peripheral—stimulation was most clearly evident. Statistical Analysis Statistical analyses were performed with custom scripts in Matlab R2012a (MathWorks, Natick, Massachusetts, USA; www. mathworks.com). For the ratios, 95% confidence intervals (CI) were obtained on the basis of the binomial distribution. The distributions were compared by nonparametric testing. Statistical significance was established as P < 0.05. The outcomes of the FNMEP and neurologic examinations were dichotomized for the statistical treatment in contingency tables with the c2 test. A contingency table contains the following elements: true positive (TP), true negative (TN), false positive (FP), and false negative (Fneg). Derivations of these elements are the sensitivity or true positive rate TPR ¼ TP/(TP þ Fneg), the falsepositive rate (FPR) ¼ FP/(FP þ TN), the accuracy ¼ (TP þ TN)/ (TP þ TN þ FP þ Fneg), the specificity 1  FPR and the negative predictive value ¼ TN/(TN þ Fneg), and the positive predictive value ¼ TP/(TP þ FP). RESULTS Illustrative FNMEP Responses Figure 3 shows large responses to biphasic TES (C3 vs. C4) in patient 22 (8 years, World Health Organization [WHO] grade III astrocytoma). The control pulse was delivered 20 ms before the

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C4 versus Cz and C3 versus Cz montages. Thenar responses were restricted to the contralateral side as expected from adults. For FN target muscles, we observed both contralateral and ipsilateral responses. For stimulation on the left side (Figure 4A), the ipsilateral responses (blue lines) appeared at the same latency as the contralateral responses (red lines). Peripheral conduction can be ruled out, because there was no response to the control pulse and the responses show polyphasic traces. For both left and right stimulation, ipsilateral responses exceeded contralateral responses, which might reflect the importance of the ipsilateral anatomic pathway in this infant. Figure 5 shows the responses to unilateral TES (C3 vs. Cz) in patient 22 (18 months, WHO III anaplastic ependymoma). The FNMEP responses in M. mentalis and M. orbicularis oris could only be obtained after tumor resection. This finding might be a result of the decompression of the nerve fibers. The patient had presented with HB grade III and improved to grade II immediately after surgery.

Figure 3. Responses to biphasic transcranial electric stimulation (C3 vs. C4) in patient 7. The facial nerve motor-evoked potential response amplitude in the facial nerve target muscles exceeds that of the thenar muscles in this patient. The control pulse was delivered 20 ms before the train of 5 pulses. None of the muscles responded to the control pulse, which excludes peripheral stimulation for the selected set of stimulation parameters.

train of 5 pulses. None of the muscles responded to the control pulse, which excludes peripheral stimulation for the chosen set of stimulation parameters. The train of 5 pulses elicited an FNMEP response in the FN target muscles, whose amplitude exceeds that of the thenar muscles in this patient. Figure 4 shows the FNMEP responses in patient 24 (5 months, WHO grade III anaplastic ependymoma) to unilateral TES in the

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Illustrative Case in Which FNMEP Recording Influenced the Surgical Strategy In patient 1 (32 months, WHO grade II pilomyxoid astrozytoma). The DES of the FN in the rhomboid fossa did not elicit muscle responses. Figure 6 shows representative responses to biphasic TES in patient 1, who presented with preoperative HB grade III. The traces were recorded from the bilateral thenar muscles and from several cranial nerve target muscles, among them M. orbicularis oris of the FN. The control pulse was delivered 20 ms before the train of 5 pulses. None of the muscles responded to the control pulse, which excludes peripheral stimulation from the selected set of stimulation parameters. The train of 5 pulses elicited a response in the target muscles of all the cranial nerves. The response latency exceeded 20 ms for the thenar muscles. The target muscles showed a variety of response latencies, and the responses were polyphasic to a varying degree. The variability of the responses might be related to the modification of the cranial nerve anatomy in the presence of the lesion. This finding advanced the interpretation that the absence of a DES response might have resulted from anatomical changes induced by the tumor. Therefore, the surgeon (O.B.) decided to initiate tumor resection. The postoperative evaluation revealed unchanged FN function (HB ¼ 3 preoperative and postoperative). In this case, the presence of FNMEP recordings—as opposed to DES alone—contributed to tumor resection. FNMEP Was Feasible in All the Surgeries Monitoring FNMEP was feasible in all the 24 surgeries in at least one FN target muscle. Not all of the muscles were monitored in all the patients. We obtained reliable results in 12 of 14 (86%) recordings at the orbicularis oculi muscle, in 20 of 21 (95%) recordings at the orbicularis oris muscle and in 20 of 23 (92%) recordings at the mentalis muscle. The orbicularis oris yielded the best result among all the FN target muscles. In adults the mentalis muscle had yielded the best result (92%) among all the FN target muscles (14). During the course of surgery, the FNMEP threshold increased more in the younger half of patients (t test, P ¼ 0.041).

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Figure 4. Facial nerve motor-evoked potential response to monophasic transcranial electric stimulation in patient 24. Right-sided stimulation (A, C3 vs. Cz) and left-sided stimulation (B, C4 vs. Cz) yield ipsilateral responses in the facial muscles but not in the thenar muscles. For both left and right stimulation, ipsilateral facial responses exceed contralateral facial responses.

We attribute this difference to the greater variability of anesthesia levels in younger children. The median stimulation threshold to elicit FNMEP responses at baseline was 65 mA, which corresponds to a pulse with a charge 33 mC. This threshold was greater than the MEP threshold for eliciting responses at the thenar muscle (median 60 mA, 30 mC) in 11 cases, equal in 9, and lower in 4 cases. Although TES for FNMEP was restricted to a maximum of 7 pulses, we had to apply the double-train technique in 9 of 24 surgeries to obtain robust MEP responses. Absence of Intraoperative Warning Is Associated with the Absence of HB Grade Deterioration The pre- and early postoperative HB grades of the patients are listed in Table 1. The HB grade remained unchanged in 23 of 24 surgeries (96% CI 79%e100%). During the course of surgery, the stimulation threshold increased to the warning criterion in 7 of the 24 surgeries (29% CI 13%e51%), and a warning was issued to the surgical team (Table 1). In at least one of these patients (patient 2), the threshold increase was caused by subdural air collection. In all the surgeries of this series, the waveforms remained polyphasic (6). In all 24 cases, TP ¼ 1 had a warning and a new deficit, TN ¼ 18 had no warning and no HB deterioration, and FP ¼ 5 had

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warnings without a new deficit, (FPR ¼ 22% CI 7%e44%). The sensitivity was 100% CI [3%e100%], and the specificity was 78% CI [56%e93%]. With 18 true-negative cases of all 18 negative cases, the negative predictive value was 100% CI [81%e100%]. With 1 true positive of all 6 positive cases, the positive predictive value was 17% CI [0%e64%].

DISCUSSION In this study, we described a consecutive series of 24 procedures in which FNMEP was performed to monitor the FN function in a pediatric population. This specific method has been previously described in an adult population (14). We have now applied FNMEP in surgeries of young patients as young as 5 months. In all the cases we were successful in eliciting a corticobulbar (as opposed to peripheral) response in FN target muscles, which was also true for other cranial nerves on an anecdotal basis because of the small number of patients examined. In comparison with our adult population (14), the median baseline stimulation thresholds were significantly lower in adults than in children for the thenar MEP (median charge 22 mC, t test, P ¼ 0.023) and also, albeit not significantly, for the FNMEP (median charge 26 mC, t test, P ¼ 0.2). We attribute this

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Figure 5. Response to unilateral transcranial electric stimulation (C3 vs. Cz) in patient 22.

difference to the immature myelination of the motor system in children (6, 15). In some children, the FNMEP gave even more salient responses than the MEP of the thenar muscles. Possibly this may be attributable to earlier maturation in the corticobulbar tract as opposed to the corticospinal tract, where responses still increase with the age of children (6, 15). Across the whole patient group, also observed that the FNMEP remained more stable than the MEP in the course of long surgeries. In particular, FNMEP could be elicited throughout surgery with a train of 5 pulses, whereas for MEP we had to introduce double-trains of 5 pulses each to overcome the accumulation of anesthetic agents in long surgeries. We have observed some cases of ipsilateral FNMEP response to TES stimulation. The following three possible causes come to mind: First, in a C3/C4 montage, anodal as well as cathodal stimulation might elicit responses, although not at the low TES intensity we aimed for. Cathodal stimulation could be ruled out in a unilateral montage against Cz. Second, there might be peripheral conduction of muscle activity across the midline. Whereas peripheral conduction is more likely in the faces of small children than of adult faces, one would not expect larger responses on the ipsilateral side. Third, during the course of maturation, remnants of the ipsilateral pathway (9) might continue to be functional in young children. The presence of the ipsilateral pathway might, on one hand, mask unilateral damage to the corticobulbar tract. On the other hand, its presence might assure a faster recovery and better clinical outcome in the HB grade. From the perspective of the surgeon (O.B.), the presence of FNMEP responses was reassuring, particularly in intrinsic glioma cases, for continuing the planned surgical procedure even in the absence of anatomical landmarks or response to DES of the FN. In patient 22, we were only able to elicit reliable FNMEP responses at a later stage of surgery, which might be because of decompression of the FN after the initial tumor reduction.

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Figure 6. Response to biphasic transcranial electric stimulation (C3 vs. C4) in patient 1. In this surgery, the presence of facial nerve motor-evoked potential recordings—as opposed to direct electrical stimulation alone—contributed to tumor resection. The preoperative House Brackmann grade III was preserved postoperatively.

Continuous EMG is less reassuring than FNMEP, because indicative EMG activity occurs only at the time when the FN is irritated, e.g., by mechanical manipulation or heat or desiccation, and the absence of EMG activity may indicate a healthy FN as well as total loss of FN function. We therefore view the use of FNMEP to be complementary to DES and continuous EMG monitoring. Along this case series of a single surgeon, we observe a tendency to more aggressive resection in later surgeries (Figure 2). Given the small number of cases and the heterogeneous group

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of lesions, this observation is of course highly speculative. We attribute this tendency, among other factors, also to the enhanced experience with FNMEP as a relatively new modality of IONM in children. In the prediction of the postoperative HB grade, the sensitivity and specificity achieved here were in the range of those described for adult populations (1-4, 8, 10, 13, 14). In this child study, the 20 mA threshold-level method yielded a FPR ¼ 26% CI [10%e48%]. In some cases, the FP warning was placed in the context of subdural air collection or variability in anesthesia depth. Whereas the child FPR is greater than that of our adult series (FPR ¼ 18% CI [4%e43%]) (14), the overlapping confidence intervals show no evidence of a difference between the 2 populations. In the tradeoff between sensitivity and specificity, we emphasize sensitivity because warnings might affect the surgical procedure, promote a better neurological outcome and thereby lead to a prediction error. Considering conflicts between postoperative

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facial nerve function and the completeness of tumor resection, surgical management decisions should depend on individual patient factors such as tumor entity (malignant vs. benign), patient age, and individual tolerance of facial nerve deficits. CONCLUSIONS Intraoperative FNMEP monitoring is feasible and safe in young and very young children. We found no evidence that the procedures and thresholds should differ from FNMEP monitoring in adults. FNMEP monitoring is a valid indicator of FN function in very eloquent surgery. Its use is complementary to direct electrical FN stimulation and continuous EMG monitoring of FN target muscles. ACKNOWLEDGMENTS The authors thank Peter Roth for providing the artwork shown in Figure 1.

7. Cornaz F, Neidert MC, Piccirelli M, Bozinov O, Regli L, Sarnthein J: Compatibility of intraoperative 3T MR imaging and intraoperative neurophysiological monitoring. Clin Neurophysiol 126:218-220, 2015.

14. Sarnthein J, Hejrati N, Neidert MC, Huber AM, Krayenbühl N: Facial nerve motor evoked potentials during skull base surgery to monitor facial nerve function using the threshold-level method. Neurosurg Focus 34:E7, 2013.

8. Dong CCJ, Macdonald DB, Akagami R, Westerberg B, Alkhani A, Kanaan I, Hassounah M: Intraoperative facial motor evoked potential monitoring with transcranial electrical stimulation during skull base surgery. Clin Neurophysiol 116: 588-596, 2005.

15. Szelenyi A, Bueno de Camargo A, Deletis V: Neurophysiological evaluation of the corticospinal tract by D-wave recordings in young children. Childs Nerv Syst 19:30-34, 2003.

9. Fregosi M, Hamadjida A, Rouiller EM: Corticobulbar projections from the premotor cortex in the macaque monkey. Swiss Society for Neuroscience. Fribourg, Switzerland, 2015. 10. Fukuda M, Oishi M, Takao T, Saito A, Fujii Y: Facial nerve motor-evoked potential monitoring during skull base surgery predicts facial nerve outcome. J Neurol Neurosurg Psychiatry 79: 1066-1070, 2008. 11. Hemmer LB, Zeeni C, Bebawy JF, Bendok BR, Cotton MA, Shah NB, Gupta DK, Koht A: The incidence of unacceptable movement with motor evoked potentials during craniotomy for aneurysm clipping. World Neurosurg 81:99-104, 2014. 12. Lyon R, Feiner J, Lieberman JA: Progressive suppression of motor evoked potentials during general anesthesia: the phenomenon of “anesthetic fade”. J Neurosurg Anesthesiol 17:13-19, 2005. 13. Matthies C, Raslan F, Schweitzer T, Hagen R, Roosen K, Reiners K: Facial motor evoked potentials in cerebellopontine angle surgery: technique, pitfalls and predictive value. Clin Neurol Neurosurg 113:872-879, 2011.

16. Szelenyi A, Kothbauer KF, Deletis V: Transcranial electric stimulation for intraoperative motor evoked potential monitoring: stimulation parameters and electrode montages. Clin Neurophysiol 118:1586-1595, 2007. 17. Ulkatan S, Deletis V, Fernandez-Conejero I: Central or peripheral activations of the facial nerve? J Neurosurg 106:519-520; author reply 520, 2007.

Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 27 January 2015; accepted 3 May 2015 Citation: World Neurosurg. (2015) 84, 3:786-794. http://dx.doi.org/10.1016/j.wneu.2015.05.008 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2015 Elsevier Inc. All rights reserved.

WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.05.008

Intraoperative Monitoring of Facial Nerve Motor-Evoked Potentials in Children.

To determine whether transcranial motor-evoked potential monitoring of the facial nerve (FNMEP) during eloquent tumor resection is feasible in childre...
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