Intraoperative neurophysiological monitoring during endoscopic endonasal surgery for pediatric skull base tumors

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OBJECT

The aim of this study was to evaluate the value of intraoperative neurophysiological monitoring (IONM) using electromyography (EMG), brainstem auditory evoked potentials (BAEPs), and somatosensory evoked potentials (SSEPs) to predict and/or prevent postoperative neurological deficits in pediatric patients undergoing endoscopic endonasal surgery (EES) for skull base tumors.

METHODS

All consecutive pediatric patients with skull base tumors who underwent EES with at least 1 modality of IONM (BAEP, SSEP, and/or EMG) at our institution between 1999 and 2013 were retrospectively reviewed. Staged procedures and repeat procedures were identified and analyzed separately. To evaluate the diagnostic accuracy of significant free-run EMG activity, the prevalence of cranial nerve (CN) deficits and the sensitivity, specificity, and positive and negative predictive values were calculated.

RESULTS

A total of 129 patients underwent 159 procedures; 6 patients had a total of 9 CN deficits. The incidences of CN deficits based on the total number of nerves monitored in the groups with and without significant free-run EMG activity were 9% and 1.5%, respectively. The incidences of CN deficits in the groups with 1 staged and more than 1 staged EES were 1.5% and 29%, respectively. The sensitivity, specificity, and negative predictive values (with 95% confidence intervals) of significant EMG to detect CN deficits in repeat procedures were 0.55 (0.22–0.84), 0.86 (0.79–0.9), and 0.97 (0.92–0.99), respectively. Two patients had significant changes in their BAEPs that were reversible with an increase in mean arterial pressure.

CONCLUSIONS

IONM can be applied effectively and reliably during EES in children. EMG monitoring is specific for detecting CN deficits and can be an effective guide for dissecting these procedures. Triggered EMG should be elicited intraoperatively to check the integrity of the CNs during and after tumor resection. Given the anatomical complexity of pediatric EES and the unique challenges encountered, multimodal IONM can be a valuable adjunct to these procedures.

ABBREVIATIONSBAEP = brainstem auditory evoked potential; CMAP = compound muscle action potential; CN = cranial nerve; EEA = endoscopic endonasal approach; EES = endoscopic endonasal surgery; EMG = electromyography; ICA = internal carotid artery; IONM = intraoperative neurophysiological monitoring; JNA = juvenile nasopharyngeal angiofibroma; SSEP = somatosensory evoked potential.

Abstract

OBJECT

The aim of this study was to evaluate the value of intraoperative neurophysiological monitoring (IONM) using electromyography (EMG), brainstem auditory evoked potentials (BAEPs), and somatosensory evoked potentials (SSEPs) to predict and/or prevent postoperative neurological deficits in pediatric patients undergoing endoscopic endonasal surgery (EES) for skull base tumors.

METHODS

All consecutive pediatric patients with skull base tumors who underwent EES with at least 1 modality of IONM (BAEP, SSEP, and/or EMG) at our institution between 1999 and 2013 were retrospectively reviewed. Staged procedures and repeat procedures were identified and analyzed separately. To evaluate the diagnostic accuracy of significant free-run EMG activity, the prevalence of cranial nerve (CN) deficits and the sensitivity, specificity, and positive and negative predictive values were calculated.

RESULTS

A total of 129 patients underwent 159 procedures; 6 patients had a total of 9 CN deficits. The incidences of CN deficits based on the total number of nerves monitored in the groups with and without significant free-run EMG activity were 9% and 1.5%, respectively. The incidences of CN deficits in the groups with 1 staged and more than 1 staged EES were 1.5% and 29%, respectively. The sensitivity, specificity, and negative predictive values (with 95% confidence intervals) of significant EMG to detect CN deficits in repeat procedures were 0.55 (0.22–0.84), 0.86 (0.79–0.9), and 0.97 (0.92–0.99), respectively. Two patients had significant changes in their BAEPs that were reversible with an increase in mean arterial pressure.

CONCLUSIONS

IONM can be applied effectively and reliably during EES in children. EMG monitoring is specific for detecting CN deficits and can be an effective guide for dissecting these procedures. Triggered EMG should be elicited intraoperatively to check the integrity of the CNs during and after tumor resection. Given the anatomical complexity of pediatric EES and the unique challenges encountered, multimodal IONM can be a valuable adjunct to these procedures.

Surgical treatment of pediatric cranial base tumors such as craniopharyngiomas, chordomas, angiofi-bromas, pituitary adenomas, and Rathke’s cleft cysts has been evolving from conventional open skull base approaches to novel, less invasive techniques like endoscopic endonasal surgery (EES).5,18,19,32,41 For properly selected tumors, EES offers several advantages over traditional methods, including the sparing of disfiguring facial incisions and craniotomy. EES allows the surgeons to access the entire ventral skull base, from the crista galli to the upper cervical spine, with minimal postoperative complications.15–17 The morbidity and mortality after pediatric skull base tumor resection has been reduced significantly with EES.5 However, during any cranial base surgery, there is potential risk to neurovascular structures such as the internal carotid artery (ICA), anterior cerebral arteries, and cranial nerves (CNs) that cause temporary or permanent neurological deficits.36 Neurological complications, including hemiparesis and cranial nerve palsies, can be predicted and prevented by utilizing real-time continuous intraoperative neurophysiological monitoring (IONM).25– 27,35–39 IONM using somatosensory evoked potentials (SSEPs),2 brainstem auditory evoked potentials (BAEPs), and electromyography (both free-run electromyography [EMG] and triggered EMG)26,27 have been valuable in conventional skull base surgeries. Similarly, the SSEP and BAEP values and free-run EMG of the CNs during EES for skull base tumors in adults have been previously described.35–39 However, to our knowledge, sufficient data to establish the value of IONM in pediatric EES have not been published.

EES for pediatric skull base tumors poses unique challenges, including anatomical limitations, when compared with adults. For example, the size of the nasal aperture and limited pneumatization of the sinuses is likely to limit dissection in patients younger than 2 years.33 Staged and repeat procedures are performed for bulky tumors20,23 and frequently recurring lesions like craniopharyngiomas, pituitary tumors, and chordomas. During staged procedures, the anatomical distortion caused by primary dissection can increase the risk of neurovascular injury in later stages. Similarly, there is an increased risk of neurovascular injury during repeat procedures because of scar tissue from previous surgery.14 In the event of a vessel injury or highly vascular tumors, blood loss is poorly tolerated in children in comparison with adults.42 Even with these significant risks, EES is associated with better quality of life,1 which can have lasting importance in the pediatric population.

The aim of this study is to investigate the value of significant changes in IONM for predicting and/or preventing postoperative neurological deficit following EES for pediatric skull base tumors. This information will be very useful for optimizing the utilization of various intraoperative monitoring modalities in order to reduce the morbidity and mortality associated with EES for pediatric skull base tumors.

Methods

We retrospectively reviewed all consecutive EES procedures performed in children at our institution between 1999 and 2013. In total, 129 patients younger than 18 years who underwent 159 procedures with IONM were identified. The inclusion criteria for the study were patients who underwent EES with IONM using at least 1 modality (BAEP, SSEP, and/or EMG); 2 patients who did not have documented postoperative neurological status were excluded. This study was approved by the local institutional review board for retrospective review of the clinical outcomes. The subsequent description of the neurophysiological monitoring techniques has been discussed in detail in earlier publications,35–39 and a brief overview is given below.

The monitoring protocol was decided preoperatively based on the neurovascular structures at risk. Since the locations of the tumors in patients differed, different protocols were tailored for individual patients. EMG was used based on the surgeon’s impression of the potential involvement during exposure or resection.

Neurophysiological Monitoring

Physician oversight and interpretation were performed using a combined on-site and remote model used by the University of Pittsburgh Medical Center. In all cases, a board-certified neurophysiologist was on-site and immediately available for interpretation and consultation, and physician (neurologist) oversight, supervision, and interpretation were performed in person or remotely. The overseeing physician provided supervision to 4 to 5 cases simultaneously on average, with a maximum of 8 cases. No special adaptations were required for pediatric cases.

BAEP

Baseline BAEP levels were obtained by stimulating both ears independently: left ear and right ear. Recordings were made continuously throughout the procedure by delivering a click stimulus to 1 ear, either the left ear or right ear, at an 85-dB hearing level at a stimulus rate of 17.5 Hz. White noise was applied to the contralateral ear at a 65-dB hearing level. The observation interval was 12 msec. Recording channels included Cz-A1, Cz-A2, and Cz-Cv2. Amplifier bypass was 100 Hz to 1 KHz for all channels. Baseline BAEP responses were obtained after the initiation of anesthesia, positioning of the patient, and in some cases before any major manipulations.

SSEP

After the induction of anesthesia and positioning of the patient, baseline SSEP responses were established, except in cases of basilar invagination or other severe brainstem or cervicomedullary compression, in which case baseline SSEP values were obtained prior to positioning. Upper-and lower-extremity SSEP responses were continuously obtained throughout the procedure. Subdermal needle electrode pairs were used for stimulating the median or ulnar nerves bilaterally for the upper-extremity SSEPs and the tibial and peroneal nerves bilaterally for the lower-extremity SSEPs. Recordings were obtained from the scalp, cervical region, and Erb’s point with subdermal electrodes. All electrodes were placed per the international 10–20 system. P4/Fz and P3/Fz scalp electrodes were used to record cortical potentials for upper-extremity SSEPs. An extra Pz/Fz channel was used for lower-extremity cortical SSEPs. A cervical electrode was localized at the C7 spinous process or mastoid and referenced to the scalp electrode Fz. Erb’s point recordings were obtained using EPs and EPd electrodes that were placed close to the brachial plexus. Band-pass filters were set from 10 to 250 Hz for cortical recordings and 30 to 1000 Hz for cervical and Erb’s point recordings. The stimulation frequency was 2.33 to 2.45 Hz with a duration of 0.2 to 0.3 msec. The averages were computed for either 128 or 256 trials, depending on the signal quality.

EMG Monitoring

Continuous free-run EMG activity was recorded using pairs of subdermal needle electrodes that were placed 1 cm apart in or near the muscle groups innervated by a CN. The sensitivity, time base, and bandwidth were established at 50 μV/division, 100 msec/division, and 3 Hz to 1 KHz for recording the responses. The details of the monitored CNs and muscle groups are shown in Table 1. Triggered EMG was recorded from the appropriate CNs (Table 1) during the procedure using the same electrodes placed for free-run EMG recording. The CNs were stimulated using a constant-voltage monopolar stimulator with current intensity ranging from 0.2 to 2 V based on the amplitude of the response. The lowest current stimulation, which was used to obtain a response, was determined as the threshold. The monopolar stimulator was introduced separately outside the endoscope. A return electrode was placed to field. The sensitivity, time base, and bandwidth were established at 50 μV/division, 5 msec/division, and 3 Hz to 1 KHz for recording the triggered EMG responses.

TABLE 1.

Monitored CNs and muscle groups

CNMonitored Muscle Group
Occulomotor nerveMedial rectus muscle
Trochlear nerveSuperior oblique muscle
Abducent nerveLateral rectus muscle
Trigeminal nerveMasseter
Facial nerveOrbicularis oris, orbicularis oculi, & mentalis (ipsilateral)
Motor component of the glosso-pharyngeal nerveSoft palate (after intubation)
Recurrent laryngeal component of the vagus nerveCricothyroid muscle
Spinal accessory nerveTrapezius muscle
Hypoglossal nerveTongue muscles

Alarm Criteria

For BAEPs, persistent decreases in amplitude of more than 50% of wave V and/or a persistent absolute latency increase of the peak of wave V ≥ 0.5 msec were considered clinically significant. Changes in more than 2 consecutive averaged trials were considered “persistent changes.” For SSEPs, a 10% increase in latency or 50% decrease in amplitude relative to baseline was considered clinically significant.31,35–37

Changes in more than 2 consecutive averaged trials were considered persistent changes. The absence of free-run EMG activity was considered baseline in each case. The detection of nerve manipulation, compression, stretch, and/or permanent injury was based on changes from the baseline recordings. Significant free-run EMG activity, when present for prolonged periods of time (≥ 100 msec) from a CN, was reported to the surgeons as 1 alert and was also recorded in the patient’s records.38,39 Triggered EMG responses were obtained upon request using a constant-current stimulator. All negative and positive responses were communicated to the surgeons. When appropriate, the lowest possible current required to stimulate a nerve was obtained. Furthermore, we also attempted to obtain triggered EMG responses after tumor resection was completed.

Medical Records Review

The medical records of the 129 patients were reviewed to determine if any new neurological deficits were present after the surgical procedure. The medical records were reviewed independently without knowledge of the IONM changes. Any new postoperative motor or sensory deficits were considered to be due to iatrogenic injuries. Deficits were classified as transient or permanent. Transient deficits had to have documented evidence in the medical records of complete improvement to baseline. Permanent deficits were defined as those that did not improve to baseline in subsequent follow-up visits (> 1 month).

Data Analysis

The means and standard deviations were calculated for the continuous variables, and ratios were calculated for categorical variables. We calculated the percentages to determine the distributions of the types of procedures, as well the postoperative pathological diagnoses. For the data analysis, the number of nerves monitored for each patient was calculated by considering unilateral as “1” and bilateral as “2” nerves monitored. Depending on the presence or absence of significant free-run EMG activity, data were divided into 2 groups and analyzed. Staged procedures and repeat procedures were identified and analyzed separately to determine the incidence of significant activity and CN deficits. To evaluate the diagnostic accuracy of significant free-run EMG activity, we calculated the prevalence of CN deficits and the sensitivity, specificity, and positive and negative predictive values. We further calculated the likelihood ratios in order to compare the probability of obtaining significant free-run EMG activity if the patient had a deficit to the probability of obtaining a significant free-run EMG activity if the patient was healthy. To evaluate the measure of uncertainty, we calculated the 95% confidence intervals.

Results

Demographic Data

The total number of children who underwent at least 1 IONM modality was 129, of whom 74% were male and 26% were female. Angiofibroma, pituitary adenoma, chordoma, and craniopharyngioma were the most common diagnoses. The most common surgical approaches were transsellar (32%) and transclival (29%), followed by transpterygoid (11%) and others. There were 16 planned staged procedures (in 14 patients) and 10 repeat procedures. Two patients underwent a repeat staged procedure. A detailed description of the demographic information is shown in Table 2.

TABLE 2.

Demographic data

VariableNo. (%)
No. of procedures159
No. of patients129
 Male91 (71)
 Female0038 (29)
 Transclival46 (29)
 Transsellar51 (32)
 Transplanum11 (7)
 Transpterygoid17 (11)
 Transcavernous1 (0.6)
 Other (>1 approach)33 (21)
 1–525 (19)
 5–1026 (20)
 10–1878 (61)
 Craniopharyngioma14 (11)
 Chordoma19 (15)
 Pituitary tumor21 (16)
 Rathke’s cyst9 (7)
 Angiofibroma22 (17)
 Meningocele/encephalocele6 (5)
 CSF leak5 (4)
 Dermoid/epidermoid4 (3)
 Other29 (22)
Staged procedure16 (10)
Repeat procedure10 (6)
Monitoring
 SSEP156 (98)
 BAEP016 (10)
 Free-run EMG62 (39)
 EMG*7 (11)

Among 62 patients who underwent free-run EMG monitoring.

Clinical Outcomes

The incidence of postoperative CN deficits was 9 (2.8%) of 321 CNs monitored. Of the 6 patients who had 9 CN deficits, 3 had a diagnosis of chordoma and 3 had juvenile nasopharyngeal angiofibroma (JNA). Four CN deficits were transient (1.2%) and 5 were permanent (1.5%). Two patients underwent staged procedures, 1 patient underwent a repeat procedure, and 1 patient underwent a staged procedure followed by a repeat procedure at a later date. The details of the clinical deficits are shown in Table 3. No patient experienced quadriparesis, hemiparesis, or death after the procedure. There were no new postoperative vision deficits.

TABLE 3.

Clinical deficits in individual patients

Age (yrs)SexDiagnosisOpCN MonitoredSide MonitoredFree-Run EMG Performed?Nerve Deficit (type)No. of Stages/Repeat
10MJNATCIII, VILtYes, CN III; no, CN VILt CN III, lt CN VI (both transient)3 stages
13MJNATPVIBilatYes, lt CN VILt CN VI (permanent)5 stages/1 repeat
10FChordomaTCIXRtYesRt CN IX (permanent)1 stage
11MChordomaTPXIIBilatYes, lt CN XIILt CN XII (transient)1 stage
11MJNATCV, VIBilatYes, rtCNV; no, CNVIRt CN VIII (permanent); rt CN VI (transient)2 stages
10MChordomaTCVIBilatNoBilat VI (permanent)1 repeat

TC = transclival; TP = transpterygoidal.

Free-Run EMG Activity and Neurological Deficits

Free-run EMG monitoring was performed in 62 (39%) patients. The total number of CNs monitored in these cases was 321. Significant free-run EMG activity was observed in 55 (17%) nerves, and 266 (83%) nerves did not have significant free-run EMG activity. Five CN deficits were observed among the CNs with significant free-run EMG activity; 3 deficits were permanent and 2 were transient. Four CN deficits were observed among CNs without significant free-run EMG activity. All 4 of these deficits were in CN VI; 2 were transient and 2 were permanent. Seven CN deficits were observed in staged or revision EES, whereas 2 CN deficits were observed after the first stage of the procedure. The overall incidence of CN deficits was 2.8%. The incidence of CN deficits, when significant free-run EMG activity was observed, was 9% (3.6% were transient deficits and 5.4% were permanent deficits), and the incidence of CN deficits in the group without significant free-run EMG activity was 1.5% (0.75% were transient deficits and 0.75% were permanent deficits). The incidence of CN deficits in the group with only 1 staged EES was 1.5%, and the incidence of CN deficits in the group with a revision or staged procedure was 27%. An overview of significant EMG activity and CN deficits is detailed in Table 4. In addition, we evaluated significant free-run EMG activity in patients who underwent staged or repeat procedures and those with nerve deficits (Table 5).

TABLE 4.

Incidence of significant free-run EMG activity in the monitored CNs and nerve deficits

CNNo. of Monitored CNsSignificant Free-Run EMG ActivityNo Significant Free-Run EMG Activity
No. (%)No. of Nerve DeficitsNo. of Permanent DeficitsNo. (%)No. of Nerve DeficitsNo. of Permanent Deficits
III5414 (26)1040 (74)00
IV454 (9)0041 (91)00
V114 (36)117 (64)00
VI875 (5.7)1182 (94.3)42
VII163 (19)0013 (81)00
IX299 (31)1120 (69)00
X309 (30)0021 (70)00
XI102 (20)008 (80)00
XII395 (13)1034 (87)00
Total32155 (17)53266 (83)42
TABLE 5.

Incidence of significant free-run EMG activity in the staged procedure and CN deficits

CNNo. of CNs MonitoredSignificant Free-Run EMG ActivityCN Deficits, ≥2 Stages/Repeat
Total1 Stage≥2 Stages/Repeat, nNo.1 Stage, n (%)≥2 Stages/Repeat, n (%)1 Stage, n ≥≥2 Stages/Repeat, n
III5435191410 (71)4 (29)01
IV45341143 (75)1 (25)00
V11110404 (100)01
VI87384953 (60)2 (40)05
VII167931 (33)2 (67)00
IX29131694 (44)5 (56)10
X30131797 (78)2 (22)00
XI1028202 (100)00
XII39132652 (40)3 (60)10
Total3211561655530 (55)25 (45)27

Statistical Analysis of Significant Free-Run EMG Activity

The prevalence of CN deficits in staged procedures was 4.2%, which is higher than the prevalence of 2.8% in the first staged procedure for all CNs monitored (p = 0.35). Free-run EMG activity had a high specificity and negative predictive value for all procedures, and higher specificity for repeat procedures (Table 6). The sensitivity of this study was low for all procedures. The likelihood of having a significant EMG activity was significantly higher in patients undergoing a staged or repeat procedure.

TABLE 6.

Prevalence, sensitivity, specificity, predictive value, and likelihood ratios of significant EMG activity to detect CN deficits

Significant Free-Run EMG ActivityAll Procedures≥2 Stages
No. of CNs321165
No. of deficits97
Prevalence2.8%4.2%
Sensitivity (95% CI)0.55 (0.22–0.84)0.42 (0.11–0.79)
Specificity (95% CI)0.83 (0.79–0.87)0.86 (0.79–0.9)
Positive predictive value (95% CI)0.08 (0.03–0.2)0.12 (0.03–0.32)
Negative predictive value (95% CI)0.98 (0.95–0.99)0.97 (0.92–0.99)
Likelihood ratio (95% CI)0.02 (0.00–0.04)3.07 (1.2–7.8)

Triggered EMGs were recorded in 7 patients and 12 cranial nerves; we were able to obtain compound muscle action potential (CMAP) responses from all 12 CNs (Fig. 1). No deficit was noted in those CNs without a significant change after tumor resection.

FIG. 1.
FIG. 1.

Left: MR image obtained in a patient with JNA extending into the cavernous sinus. Right: Triggered EMG was performed to identify right CNs III, IV, and VI.

BAEP and SSEP

BAEP monitoring was performed in 16 (10%) patients, of whom 2 patients showed significant BAEP changes intraoperatively. One patient underwent a primarily transclival resection of JNA, and the other was a JNA that had a primarily transpterygoid route. We observed a significant decrease in the amplitude of the wave V of the BAEPs during tumor resection. These changes were transient and improved with an increase in mean arterial pressure. No postoperative hearing deficits or weakness was observed. No SSEP changes were noted in any of the patients. No postoperative sensory or motor deficits were seen.

Case Example

A 7-year-old boy presented with nasopharyngeal obstruction, headache, and diplopia from left CN VI palsy. MRI revealed a large clival lesion, consistent with chordoma, involving the left parapharyngeal and petrous ICA (Fig. 2). A left cervical incision was made to isolate the ICA for proximal control. Intraoperatively, the left petrous ICA, just distal to foramen lacerum, was injured with a cutting rongeur. The site of bleeding was packed, and a vascular clip was placed on the cervical ICA with no change in SSEPs over 15 minutes. After removal of the packing, there was brisk back-bleeding from the distal stump of the injured ICA but still no change in the baseline SSEPs. Consequently, the ICA was sacrificed using endoscopic bipolar electrocautery.

FIG. 2.
FIG. 2.

Preoperative T2-weighted axial MR images showing a large chordoma in a 7-year-old patient adjacent to the left parapharyngeal ICA (left) and extensive involvement of the left petrous ICA (right).

The patient remained hemodynamically and electro-physiologically stable, and a decision was made to proceed with resection. Following resection, under continued SSEP monitoring, the patient was taken for endovascular evaluation and permanent occlusion of the ICA. Angiography showed an ipsilateral persistent trigeminal artery that filled the middle cerebral artery, and there was rapid cross-fill across the anterior communicating artery. As predicted by the IONM, the patient awoke without deficit. Postoperative MRI showed no diffusion-weighted imaging restriction and complete tumor removal, which was safely facilitated by IONM (Figs. 3 and 4).

FIG. 3.
FIG. 3.

Postoperative angiogram showing a persistent trigeminal artery filling the ICA and middle cerebral artery (lateral view) (left), as well as brisk cross-fill via the anterior communicating artery (anteroposterior view) (right).

FIG. 4.
FIG. 4.

Postoperative T2-weighted MR image showing the complete resection of an extensive skull base chordoma (left), which was adjacent to the now occluded left ICA (right).

Discussion

The wide variation in pathology in this series is shown in Table 2. The most common pathologies were craniopharyngioma, chordoma, JNA, and Rathke’s cleft cyst. While invasive chordomas could potentially damage the CNs in the foramina, Rathke’s cyst and craniopharyngioma (being noninvasive) have less propensity to do so. However, nerve compression could occur. Similarly, intracranial extension of the JNAs could cause compressive lesions. The neurovascular structures that were at risk varied in individual cases depending on the stage of tumor.

EMG Monitoring

Our results show that free-run EMG monitoring has high specificity and a negative predictive value for detecting CN deficits. This allows the surgeon to feel relatively confident during tumor removal that there is no CN injury if there is no significant EMG activity. However, if a nerve is transected abruptly, there will be only brief or no EMG activity.12 We also observed that free-run EMG has a lower sensitivity for detecting cranial deficits during EES. Free-run EMG activity is observed secondary to the activation of a CN due to manipulation during tumor dissection, bipolar use, as well as other maneuvers during the surgery.38,39 Free-run EMG activity has been classified as bursts, spikes, and neurotonic discharges based on the amplitude and frequency of the discharges.21,22 It has been observed that manipulation of the CN is the primary reason for bursts and spike discharges with no correlation to nerve injury.25,27,28 In our practice, we use free-run EMG activity as a guide to alert the surgeon to the proximity of the nerve, wherein the surgeon understands the limitations and risks where a positive test indicates that he might be very close to a nerve. Our alarm criteria for significant free-run EMG activity allows for a careful dissection of the tumor, thereby reducing the incidence of neurological deficits.

In our study, the incidence of CN deficits in the group with significant free-run EMG activity was higher when compared with the group without significant activity. This is expected given the relationships between nerve dissection/manipulation and free-run EMG and supports the concept that increased activity can be associated with injury. We also observed that children who had recurrent tumors or underwent staged procedures had a higher likelihood of significant free-run EMG activity, as well as a corresponding increase in the prevalence of CN deficits. Staging is used more often in pediatric cases since blood loss is poorly tolerated in children with bulky or vascular tumors. Recurrent tumors require dissection of the fibrotic areas that are in close proximity to critical structures. There are scar tissues and adhesions from previous surgery, which makes tumor dissection challenging and in turn increases the risk of CN deficit. Neurotonic discharges, which are the high-frequency, high-amplitude discharges observed mostly in facial nerve monitoring, are a precursor of postoperative nerve injury.21,25 We did not observe neurotonic discharges uniformly in all instances of CN free-run EMG monitoring. Since we recorded all changes in significant free-run EMG activities, this could have lowered the sensitivity rate during the analysis.

Triggered EMG responses are obtained secondary to electrical stimulation of the CN in the tumor field during dissection, which produces CMAPs with specific latencies that identify the CN during a procedure.27,29 Triggered EMG can be used as a mapping tool to identify the CNs along their tracts during the procedure. In our series, not all patients received triggered EMG monitoring; the adoption of triggered EMG coincided with increased surgeon experience that facilitated more aggressive resection. We believe adequate mapping of a CN during dissection and obtaining a triggered EMG CMAP response from a proximal site after complete resection provides valuable information regarding the integrity of the nerve. Based on this study and published suggestions, CN free-run EMG and triggered EMG monitoring, especially during staged procedures and for recurrent tumors, might be valuable for reducing morbidity by identifying the nerve during tumor dissection.11,12 Communicating free-run EMG activity to the surgeon plays a key role in complex decision making during tumor dissection. The predictability of the increased risk of clinically significant injury by free-run EMG and the lack of deficits in those few cases with documented triggered EMG strongly support the role of these modalities during EES.

We report 9 CN deficits of 321 monitored CNs in children. Four CN deficits were transient and 5 CN deficits were permanent, which were seen in children with JNA and chordoma. Studies on the endoscopic and conventional resection of JNA have reported CN deficits in 0.6% to 15% of patients.6,9 Studies show that CN deficits were higher in the conventional resection of JNA, as well in patients who underwent surgery for recurrence (43%).24 The wide variation in results was secondary to the degree of tumor resection, tumor size, and intracranial extension.6,9,10,13,24 Our reported CN deficits of CNs III, V, and VI after JNA resection in children are similar to previously reported series, especially given tumor size and the completeness of the resections. An even wider range in CN deficits after chordoma resection has been reported as 8% to 70%.28,30,40 Since traditional skull base surgery used for resection of JNA and chordomas includes lateral and midline approaches where neurovascular structures are encountered before the tumor, the incidence of postoperative deficits may be higher in those patient groups. In our series with pediatric patients, the use of free-run EMG and triggered EMG contributed to the identification of the CNs during tumor dissection. This may not only improve the ability to preserve the nerves, but also help increase the degree of resection by increasing surgeon confidence in nerve location and involvement relative to the tumor. Free-run EMG and triggered EMG have been shown to be effective in the past.26,27,35–39 However, a control group was not used during this study, as it is difficult to set up a control group in a pediatric patient population.

SSEP and BAEP

JNAs are vascular tumors whose resection could be complicated by vascular injury and intraoperative hemorrhage that lead to hypovolemia.13 Chordomas, which are tumors of the clival region, can compress the brainstem, and dissection at this location can lead to changes in BAEPs as observed in our study. Chordoma resections that involve the brainstem had previously reported motor weakness secondary to brainstem infarction.8,28,30 In the series by Brockmeyer et al. involving 55 patients, they reported 2 patients with hemiparesis and 4 patients with permanent CN deficits.4 In a series involving 26 patients, Teo et al. reported 1 patient with quadriparesis and 12 CN deficits.34 We observed significant changes in BAEPs, which were reversed with an increase in mean arterial pressure. No patient who underwent EES for resection of pediatric skull base tumors experienced quadriparesis, hemiparesis, or death after the procedure. BAEPs are sensitive to changes in stretch on the auditory nerve, and hypoperfusion along the brainstem lemniscal pathways. BAEP changes can be measured by changes in latency and amplitude of waveforms, though wave V is the most prominent.31 A larger decrease in brainstem blood flow causes changes in the amplitudes of SSEP and BAEP.3 Monitoring SSEP and BAEP for tumors in proximity to the brainstem can provide a multimodal approach that protects the brainstem’s sensory and auditory pathways since the blood supply to the brainstem consists of single end arteries, and a sudden change in 1 pathway may not be reflective of changes in the other pathway.

SSEP plays a critical role in the resection of tumors with a high risk of ICA injury such as chordomas.7 In the absence of prior balloon test occlusion, intraoperative SSEP becomes the surrogate for the physiological impact of arterial injury or occlusion. This is illustrated by the case example, whereby the decision to completely occlude the injured ICA both intraoperatively and postoperatively was made based solely on SSEP data. In addition, the stability of intraoperative potentials allowed for the removal of the remainder of tumor, thereby significantly impacting outcome.

This is a retrospective analysis of the results, which limits our capacity to collect long-term information and is therefore a limitation. Also, our series includes patients with pituitary adenomas, Rathke’s cysts, and CSF leak repairs, which are low risk for carotid artery injury. SSEP monitoring was used in these patients early on during the development of EES as a standard protocol. Our review of a previous large series40 did indicate that the changes in mean arterial blood pressure and anesthetic protocols did have an effect on SSEP, which were more common during the early part of the procedure. This was attributed to the learning effect of the surgical and neuroanesthesia team. This could have introduced potential selection bias in our study. But, in the current study, we did not find any neurovascular deficits in the patients without monitoring.

Deficits were determined by a chart review. This method has its pros (a relatively inexpensive modality for researching rich, readily accessible, and existing data) and cons (incomplete documentation, unrecorded/unrecoverable documents, and problematic verification of information). The best possible outcome would be obtained by doing a prospective study.

Conclusions

IONM can be applied effectively and reliably during pediatric EES. EMG monitoring is specific for detecting CN deficits and can be an effective guide to dissection in these procedures. Triggered EMG can be elicited intraoperatively to check the integrity of the CNs during and after tumor resection. Given the anatomical complexity of pediatric EES and the unique challenges encountered, multimodal IONM can be a valuable adjunct to these procedures.

Author Contributions

Conception and design: Thirumala, Elangovan, Gardner, Snyderman, Tyler-Kabara, Habeych, Crammond, Balzer. Acquisition of data: Thirumala, Gardner, Snyderman, Tyler-Kabara, Habeych, Crammond, Balzer. Analysis and interpretation of data: Thirumala, Elangovan, Singh. Drafting the article: Elangovan. Critically revising the article: Elangovan, Singh. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Thirumala. Statistical analysis: Thirumala, Elangovan. Administrative/technical/material support: Thirumala, Gardner, Snyderman, Tyler-Kabara, Habeych, Crammond, Balzer. Study supervision: Thirumala.

References

  • 1

    Abergel ACavel OMargalit NFliss DMGil Z: Comparison of quality of life after transnasal endoscopic vs open skull base tumor resection. Arch Otolaryngol Head Neck Surg 138:1421472012

  • 2

    Bejjani GKNora PCVera PLBroemling LSekhar LN: The predictive value of intraoperative somatosensory evoked potential monitoring: review of 244 procedures. Neurosurgery 43:4915001998

  • 3

    Branston NMSymon LCrockard HAPasztor E: Relationship between the cortical evoked potential and local cortical blood flow following acute middle cerebral artery occlusion in the baboon. Exp Neurol 45:1952081974

  • 4

    Brockmeyer DGruber DPHaller JShelton CWalker ML: Pediatric skull base surgery. 2 Experience and outcomes in 55 patients. Pediatr Neurosurg 38:9152003

  • 5

    Chivukula SKoutourousiou MSnyderman CHFernandez-Miranda JCGardner PATyler-Kabara EC: Endoscopic endonasal skull base surgery in the pediatric population. J Neurosurg Pediatr 11:2272412013

  • 6

    Cloutier TPons YBlancal JPSauvaget EKania RBresson D: Juvenile nasopharyngeal angioflbroma: does the external approach still make sense?. Otolaryngol Head Neck Surg 147:9589632012

  • 7

    Gardner PATormenti MJPant HFernandez-Miranda JCSnyderman CHHorowitz MB: Carotid artery injury during endoscopic endonasal skull base surgery: incidence and outcomes. Neurosurgery 73:2 Suppl Operativeons2612702013

  • 8

    Gay ESekhar LNRubinstein EWright DCSen CJanecka IP: Chordomas and chondrosarcomas of the cranial base: results and follow-up of 60 patients. Neurosurgery 36:8878971995

  • 9

    Godoy MDBezerra TFPinna FdeRVoegels RL: Complications in the endoscopic and endoscopic-assisted treatment of juvenile nasopharyngeal angioflbroma with intracranial extension. Braz J Otorhinolaryngol 80:1201252014

  • 10

    Hackman TSnyderman CHCarrau RVescan AKassam A: Juvenile nasopharyngeal angioflbroma: The expanded endonasal approach. Am J Rhinol Allergy 23:95992009

  • 11

    Harner SGDaube JREbersold MJBeatty CW: Improved preservation of facial nerve function with use of electrical monitoring during removal of acoustic neuromas. Mayo Clin Proc 62:921021987

  • 12

    Harper CM: Intraoperative cranial nerve monitoring. Muscle Nerve 29:3393512004

  • 13

    Huang YLiu ZWang JSun XYang LWang D: Surgical management of juvenile nasopharyngeal angioflbroma: analysis of 162 cases from 1995 to 2012. Laryngoscope 124:194219462014

  • 14

    Hwang JMKim YHKim JWKim DGJung HWChung YS: Feasibility of endoscopic endonasal approach for recurrent pituitary adenomas after microscopic trans-sphenoidal approach. J Korean Neurosurg Soc 54:3173222013

  • 15

    Kassam ASnyderman CHMintz AGardner PCarrau RL: Expanded endonasal approach: the rostrocaudal axis. Part I Crista galli to the sella turcica. Neurosurg Focus 19:1E32005

  • 16

    Kassam ASnyderman CHMintz AGardner PCarrau RL: Expanded endonasal approach: the rostrocaudal axis. Part II Posterior clinoids to the foramen magnum. Neurosurg Focus 19:1E42005

  • 17

    Kassam ABSnyderman CGardner PCarrau RSpiro R: The expanded endonasal approach: a fully endoscopic transnasal approach and resection of the odontoid process: technical case report. Neurosurgery 57:1 SupplE2132005

  • 18

    Komotar RJRoguski MBruce JN: Surgical management of craniopharyngiomas. J Neurooncol 92:2832962009

  • 19

    Laufer IAnand VKSchwartz TH: Endoscopic, endonasal extended transsphenoidal, transplanum transtuberculum approach for resection of suprasellar lesions. J Neurosurg 106:4004062007

  • 20

    Pirris SMPollack IFSnyderman CHCarrau RLSpiro RMTyler-Kabara E: Corridor surgery: the current paradigm for skull base surgery. Childs Nerv Syst 23:3773842007

  • 21

    Prass RLKinney SEHardy RW JrHahn JFLüders H: Acoustic (loudspeaker) facial EMG monitoring: II. Use of evoked EMG activity during acoustic neuroma resection. Otolaryngol Head Neck Surg 97:5415511987

  • 22

    Prass RLLüders H: Acoustic (loudspeaker) facial electromyographic monitoring: Part 1. Evoked electromyographic activity during acoustic neuroma resection. Neurosurgery 19:3924001986

  • 23

    Prosser JDVender JRAlleyne CHSolares CA: Expanded endoscopic endonasal approaches to skull base meningiomas. J Neurol Surg B Skull Base 73:1471562012

  • 24

    Pryor SGMoore EJKasperbauer JL: Endoscopic versus traditional approaches for excision of juvenile nasopharyngeal angioflbroma. Laryngoscope 115:120112072005

  • 25

    Romstöck JStrauss CFahlbusch R: Continuous electromyography monitoring of motor cranial nerves during cerebellopontine angle surgery. J Neurosurg 93:5865932000

  • 26

    Schlake HPGoldbrunner RSiebert MBehr RRoosen K: Intraoperative electromyographic monitoring of extra-ocular motor nerves (Nn, III, VI) in skull base surgery. Acta Neurochir (Wien) 143:2512612001

  • 27

    Schlake HPGoldbrunner RHMilewski CKrauss JTraut-ner HBehr R: Intraoperative electromyographic monitoring of the lower cranial motor nerves (LCN IX-XII) in skull base surgery. Clin Neurol Neurosurg 103:72822001

  • 28

    Sekhar LNPranatartiharan RChanda AWright DC: Chordomas and chondrosarcomas of the skull base: results and complications of surgical management. Neurosurg Focus 10:3E22001

  • 29

    Sekiya THatayama TIwabuchi TMaeda S: Intraoperative recordings of evoked extraocular muscle activities to monitor ocular motor nerve function. Neurosurgery 32:2272351993

  • 30

    Sen CTriana AIBerglind NGodbold JShrivastava RK: Clival chordomas: clinical management, results, and complications in 71 patients. J Neurosurg 113:105910712010

  • 31

    Shah ANikonow TThirumala PHirsch BChang YGardner P: Hearing outcomes following microvascular decompression for hemifacial spasm. Clin Neurol Neurosurg 114:6736772012

  • 32

    Stippler MGardner PASnyderman CHCarrau RLPrevedello DMKassam AB: Endoscopic endonasal approach for clival chordomas. Neurosurgery 64:2682782009

  • 33

    Tatreau JRPatel MRShah RNMcKinney KAWheless SASenior BA: Anatomical considerations for endoscopic endonasal skull base surgery in pediatric patients. Laryngoscope 120:173017372010

  • 34

    Teo CDornhoffer JHanna EBower C: Application of skull base techniques to pediatric neurosurgery. Childs Nerv Syst 15:1031091999

  • 35

    Thirumala PLai DEngh JHabeych MCrammond DBalzer J: predictive value of somatosensory evoked potential monitoring during resection of intraparenchymal and intraventricular tumors using an endoscopic port. J Clin Neurol 9:2442512013

  • 36

    Thirumala PDKassasm ABHabeych MWichman KChang YFGardner P: Somatosensory evoked potential monitoring during endoscopic endonasal approach to skull base surgery: analysis of observed changes. Neurosurgery 69:1 Suppl Operativeons64ons762011

  • 37

    Thirumala PDKodavatiganti HSHabeych MWichman KChang YFGardner P: Value of multimodality monitoring using brainstem auditory evoked potentials and somatosensory evoked potentials in endoscopic endonasal surgery. Neurol Res 35:6226302013

  • 38

    Thirumala PDMohanraj SKHabeych MWichman KChang YFGardner P: Value of free-run electromyographic monitoring of extraocular cranial nerves during expanded endonasal surgery (EES) of the skull base. J Neurol Surg Rep 74:43502013

  • 39

    Thirumala PDMohanraj SKHabeych MWichman KChang YFGardner P: Value of free-run electromyographic monitoring of lower cranial nerves in endoscopic endonasal approach to skull base surgeries. J Neurol Surg B Skull Base 73:2362442012

  • 40

    Tzortzidis FElahi FWright DNatarajan SKSekhar LN: Patient outcome at long-term follow-up after aggressive microsurgical resection of cranial base chordomas. Neurosurgery 59:2302372006

  • 41

    Venkataramana NKAnantheswar YN: Pediatric anterior skull base tumors: Our experience and review of literature. J Pediatr Neurosci 5:1112010

  • 42

    Winter V: Blood loss in pediatric neurosurgery. J Neurosurg Nurs 2:31391970

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Article Information

Correspondence Parthasarathy D. Thirumala, Center for Clinical Neurophysiology, Department of Neurological Surgery, UPMC Presbyterian, Ste. B-400, 200 Lothrop St., Pittsburgh, PA 15213. email address: thirumalapd@upmc.edu.

INCLUDE WHEN CITING Published online October 30, 2015; DOI: 10.3171/2015.7.PEDS14403.

Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Left: MR image obtained in a patient with JNA extending into the cavernous sinus. Right: Triggered EMG was performed to identify right CNs III, IV, and VI.

  • View in gallery

    Preoperative T2-weighted axial MR images showing a large chordoma in a 7-year-old patient adjacent to the left parapharyngeal ICA (left) and extensive involvement of the left petrous ICA (right).

  • View in gallery

    Postoperative angiogram showing a persistent trigeminal artery filling the ICA and middle cerebral artery (lateral view) (left), as well as brisk cross-fill via the anterior communicating artery (anteroposterior view) (right).

  • View in gallery

    Postoperative T2-weighted MR image showing the complete resection of an extensive skull base chordoma (left), which was adjacent to the now occluded left ICA (right).

References

1

Abergel ACavel OMargalit NFliss DMGil Z: Comparison of quality of life after transnasal endoscopic vs open skull base tumor resection. Arch Otolaryngol Head Neck Surg 138:1421472012

2

Bejjani GKNora PCVera PLBroemling LSekhar LN: The predictive value of intraoperative somatosensory evoked potential monitoring: review of 244 procedures. Neurosurgery 43:4915001998

3

Branston NMSymon LCrockard HAPasztor E: Relationship between the cortical evoked potential and local cortical blood flow following acute middle cerebral artery occlusion in the baboon. Exp Neurol 45:1952081974

4

Brockmeyer DGruber DPHaller JShelton CWalker ML: Pediatric skull base surgery. 2 Experience and outcomes in 55 patients. Pediatr Neurosurg 38:9152003

5

Chivukula SKoutourousiou MSnyderman CHFernandez-Miranda JCGardner PATyler-Kabara EC: Endoscopic endonasal skull base surgery in the pediatric population. J Neurosurg Pediatr 11:2272412013

6

Cloutier TPons YBlancal JPSauvaget EKania RBresson D: Juvenile nasopharyngeal angioflbroma: does the external approach still make sense?. Otolaryngol Head Neck Surg 147:9589632012

7

Gardner PATormenti MJPant HFernandez-Miranda JCSnyderman CHHorowitz MB: Carotid artery injury during endoscopic endonasal skull base surgery: incidence and outcomes. Neurosurgery 73:2 Suppl Operativeons2612702013

8

Gay ESekhar LNRubinstein EWright DCSen CJanecka IP: Chordomas and chondrosarcomas of the cranial base: results and follow-up of 60 patients. Neurosurgery 36:8878971995

9

Godoy MDBezerra TFPinna FdeRVoegels RL: Complications in the endoscopic and endoscopic-assisted treatment of juvenile nasopharyngeal angioflbroma with intracranial extension. Braz J Otorhinolaryngol 80:1201252014

10

Hackman TSnyderman CHCarrau RVescan AKassam A: Juvenile nasopharyngeal angioflbroma: The expanded endonasal approach. Am J Rhinol Allergy 23:95992009

11

Harner SGDaube JREbersold MJBeatty CW: Improved preservation of facial nerve function with use of electrical monitoring during removal of acoustic neuromas. Mayo Clin Proc 62:921021987

12

Harper CM: Intraoperative cranial nerve monitoring. Muscle Nerve 29:3393512004

13

Huang YLiu ZWang JSun XYang LWang D: Surgical management of juvenile nasopharyngeal angioflbroma: analysis of 162 cases from 1995 to 2012. Laryngoscope 124:194219462014

14

Hwang JMKim YHKim JWKim DGJung HWChung YS: Feasibility of endoscopic endonasal approach for recurrent pituitary adenomas after microscopic trans-sphenoidal approach. J Korean Neurosurg Soc 54:3173222013

15

Kassam ASnyderman CHMintz AGardner PCarrau RL: Expanded endonasal approach: the rostrocaudal axis. Part I Crista galli to the sella turcica. Neurosurg Focus 19:1E32005

16

Kassam ASnyderman CHMintz AGardner PCarrau RL: Expanded endonasal approach: the rostrocaudal axis. Part II Posterior clinoids to the foramen magnum. Neurosurg Focus 19:1E42005

17

Kassam ABSnyderman CGardner PCarrau RSpiro R: The expanded endonasal approach: a fully endoscopic transnasal approach and resection of the odontoid process: technical case report. Neurosurgery 57:1 SupplE2132005

18

Komotar RJRoguski MBruce JN: Surgical management of craniopharyngiomas. J Neurooncol 92:2832962009

19

Laufer IAnand VKSchwartz TH: Endoscopic, endonasal extended transsphenoidal, transplanum transtuberculum approach for resection of suprasellar lesions. J Neurosurg 106:4004062007

20

Pirris SMPollack IFSnyderman CHCarrau RLSpiro RMTyler-Kabara E: Corridor surgery: the current paradigm for skull base surgery. Childs Nerv Syst 23:3773842007

21

Prass RLKinney SEHardy RW JrHahn JFLüders H: Acoustic (loudspeaker) facial EMG monitoring: II. Use of evoked EMG activity during acoustic neuroma resection. Otolaryngol Head Neck Surg 97:5415511987

22

Prass RLLüders H: Acoustic (loudspeaker) facial electromyographic monitoring: Part 1. Evoked electromyographic activity during acoustic neuroma resection. Neurosurgery 19:3924001986

23

Prosser JDVender JRAlleyne CHSolares CA: Expanded endoscopic endonasal approaches to skull base meningiomas. J Neurol Surg B Skull Base 73:1471562012

24

Pryor SGMoore EJKasperbauer JL: Endoscopic versus traditional approaches for excision of juvenile nasopharyngeal angioflbroma. Laryngoscope 115:120112072005

25

Romstöck JStrauss CFahlbusch R: Continuous electromyography monitoring of motor cranial nerves during cerebellopontine angle surgery. J Neurosurg 93:5865932000

26

Schlake HPGoldbrunner RSiebert MBehr RRoosen K: Intraoperative electromyographic monitoring of extra-ocular motor nerves (Nn, III, VI) in skull base surgery. Acta Neurochir (Wien) 143:2512612001

27

Schlake HPGoldbrunner RHMilewski CKrauss JTraut-ner HBehr R: Intraoperative electromyographic monitoring of the lower cranial motor nerves (LCN IX-XII) in skull base surgery. Clin Neurol Neurosurg 103:72822001

28

Sekhar LNPranatartiharan RChanda AWright DC: Chordomas and chondrosarcomas of the skull base: results and complications of surgical management. Neurosurg Focus 10:3E22001

29

Sekiya THatayama TIwabuchi TMaeda S: Intraoperative recordings of evoked extraocular muscle activities to monitor ocular motor nerve function. Neurosurgery 32:2272351993

30

Sen CTriana AIBerglind NGodbold JShrivastava RK: Clival chordomas: clinical management, results, and complications in 71 patients. J Neurosurg 113:105910712010

31

Shah ANikonow TThirumala PHirsch BChang YGardner P: Hearing outcomes following microvascular decompression for hemifacial spasm. Clin Neurol Neurosurg 114:6736772012

32

Stippler MGardner PASnyderman CHCarrau RLPrevedello DMKassam AB: Endoscopic endonasal approach for clival chordomas. Neurosurgery 64:2682782009

33

Tatreau JRPatel MRShah RNMcKinney KAWheless SASenior BA: Anatomical considerations for endoscopic endonasal skull base surgery in pediatric patients. Laryngoscope 120:173017372010

34

Teo CDornhoffer JHanna EBower C: Application of skull base techniques to pediatric neurosurgery. Childs Nerv Syst 15:1031091999

35

Thirumala PLai DEngh JHabeych MCrammond DBalzer J: predictive value of somatosensory evoked potential monitoring during resection of intraparenchymal and intraventricular tumors using an endoscopic port. J Clin Neurol 9:2442512013

36

Thirumala PDKassasm ABHabeych MWichman KChang YFGardner P: Somatosensory evoked potential monitoring during endoscopic endonasal approach to skull base surgery: analysis of observed changes. Neurosurgery 69:1 Suppl Operativeons64ons762011

37

Thirumala PDKodavatiganti HSHabeych MWichman KChang YFGardner P: Value of multimodality monitoring using brainstem auditory evoked potentials and somatosensory evoked potentials in endoscopic endonasal surgery. Neurol Res 35:6226302013

38

Thirumala PDMohanraj SKHabeych MWichman KChang YFGardner P: Value of free-run electromyographic monitoring of extraocular cranial nerves during expanded endonasal surgery (EES) of the skull base. J Neurol Surg Rep 74:43502013

39

Thirumala PDMohanraj SKHabeych MWichman KChang YFGardner P: Value of free-run electromyographic monitoring of lower cranial nerves in endoscopic endonasal approach to skull base surgeries. J Neurol Surg B Skull Base 73:2362442012

40

Tzortzidis FElahi FWright DNatarajan SKSekhar LN: Patient outcome at long-term follow-up after aggressive microsurgical resection of cranial base chordomas. Neurosurgery 59:2302372006

41

Venkataramana NKAnantheswar YN: Pediatric anterior skull base tumors: Our experience and review of literature. J Pediatr Neurosci 5:1112010

42

Winter V: Blood loss in pediatric neurosurgery. J Neurosurg Nurs 2:31391970

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