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CLINICAL STUDY

Intraoperative Neurophysiologic Monitoring for Prediction of Postoperative Neurological Improvement in a Child With Chiari Type I Malformation Yukari Kawasaki, MD, Susumu Uchida, MD, PhD, Kouhei Onishi, MD, Masako Toyokuni, MD, Kazuo Okanari, MD,y and Minoru Fujiki, MD, PhD Introduction: Although many surgical treatment strategies for Chiari malformation type I (CM-I) have been reported, the most appropriate surgical technique remains controversial. It is wholly ascribable to the complicacy of pathological condition in CM-I. Recently, intraoperative neurophysiologic monitoring (INM) is becoming prevalent in spinal surgery. Indeed, motor-evoked potentials (MEPs) monitoring and somatosensory-evoked potentials (SSEPs) monitoring are standard tools to minimize the risk of neurologic injury and postoperative deficits. The most recent study suggested that multimodality INM can be beneficial in foramen magnum decompression surgery for CM-I patients for surgical positioning and planning. Various authors have investigated the consistency of intraoperative evoked potential changes that might aid the surgeon to determine the appropriate extent of decompression required for an individual patient. Patient Description: The authors report the case of a 7-year-old boy who had the signs of medullary and cerebellar dysfunction, clumsy hands, and ataxic gait. He underwent a surgery of foramen magnum decompression with tonsillectomy and duraplasty for CMI with cervicomedullary compression. His intraoperative MEPs improved (indicated increased-amplitude and shortened-latency) both after craniotomy and durotomy, whereas SSEPs improved only after durotomy. Those results were correlated well with a functional improvement that was apparent in the immediate postoperative hospitalization. Conclusions: The authors’ data provides 1 possible interpretation of INM for safety aspect, but also which degree of decompression in each patient will require. The improvement in MEPs and SSEPs observed during decompression procedure may be a good indicator for the prediction of the clinical improvement seen postoperatively. Key Words: Chiari malformation, intraoperative neurophysiologic monitoring, motor-evoked potentials (J Craniofac Surg 2017;00: 00–00)

From the Department of Neurosurgery; and yDepartment of Pediatrics, Graduate School of Medicine, Oita University, Oita, Japan. Received March 21, 2017. Accepted for publication April 11, 2017. Address correspondence and reprint requests to Yukari Kawasaki, MD, Department of Neurosurgery, School of Medicine, Oita University, 1-1, Idaigaoka, Hasama-machi, Yufu, Oita 879-5593, Japan; E-mail: [email protected] The authors report no conflicts of interest. Copyright # 2017 by Mutaz B. Habal, MD ISSN: 1049-2275 DOI: 10.1097/SCS.0000000000003926

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he most appropriate surgical strategy for foramen magnum decompression in Chiari malformation Type I (CM-I) remains unclear.1 The majority of neurosurgeons believe that an occipital bone decompression with duraplasty is enough for improvement of symptoms; however, there may be a group of patients who improve in response to foramen magnum decompression with the removal of the outer layer of the dura mater alone, and others may even require a more invasive surgical procedure at the cerebellar tonsils and fourth ventricle outlet.2– 4 There are significant anatomical variations among individuals in CM-I. Symptoms are believed to result from compression of neural structures in the posterior fossa and can also be associated with a syrinx in the spinal cord or brainstem. The operative procedure should be individualized according to the specific pathophysiology, biomechanics, and clinical significance of each patient. While a large-scale most recent study suggested that preoperative evaluation with evoked potential for CM-I does not add any clinically relevant information,5,6 potential benefit of motor-evoked potentials (MEPs) monitoring is also pointed out in the same year.7 We describe a pediatric patient who underwent surgery for CM-I with cervicomedullary compression whose intraoperative MEPs and somatosensory-evoked potentials (SSEPs) improved during surgery; those were correlated well with a functional improvement that was apparent in the immediate postoperative hospitalization.

CLINICAL REPORT A 7-year-old boy presented with a 2-year history of progressive gait difficulties, clumsy hands was consulted our department. Neurological examination revealed weakness in the bilateral intrinsic muscles with clumsiness of his hands. His tendon reflexes were hyperactive in all of the limbs, and he had positive bilateral Babinski signs. Superficial sensation was normal, but position sensation was notable for hypermetria. The patient’s gait was ataxic, and Romberg sign was positive. The finger-nose tests were abnormal, with bilateral dysmetria. He also had the signs of medullary dysfunction, such as snoring, downbeat nystagmus. The most common presenting symptoms associated with CM-I are occipital pain and scoliosis; however, he had neither of them. A T2-weighed magnetic resonance imaging study demonstrated the descent of the cerebellar tonsils below the level of the foramen magnum and the presyrinx state (T2 hyperintensity with indistinct T1 prolongation and without cavitation) at the C3-4 dorsal spinal cord. There was no evidence of hydrocephalus, syringomyelia, scoliosis, and the other malformation (basilar invagination, platybasia, hypoplasia of C1 posterior arch; Fig. 1). And the functional radiographs did not pick up craniocervical instabilities. Because of these findings, associated with progressive severe neurological deterioration, a foramen magnum decompression was indicated.

OPERATION The patient was positioned in prone position with the head fixated neutrally in a head holder after induction of general anesthesia.

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FIGURE 2. Intraoperative screenshots and quantitative illustrations in amplitudes and latencies of the bilateral APB-MEPs during operation. Superimposed left APB-MEP (A: left, B: right). Quantitative illustration of the time course in amplitudes (C) and latencies (D) in APB-MEPs (blue: left, red: right). The stage of decompression: from positioning to craniotomy (1), craniotomy to durotomy (2), and durotomy to dural plasty (3).

FIGURE 1. Sagittal T2-weighted magnetic resonance images. Left: preoperative image illustrating the representative features of the Chiari malformation type I with tonsillar herniation below the foramen magnum and associated T2 high lesion. Right: postoperative image demonstrating reestablished cerebrospinal fluid flow and released ventral compression at the craniocervical junction.

After a midline skin incision of 5 cm, we dissected carefully the paraspinal muscles from the bone and harvested fascia for later duraplasty. After exposing the foramen magnum, a C1 posterior arch removal and a dome-shaped suboccipital craniotomy of approximately 3025 mm was enlarged. The thickened reactive fibrous tissue band was noted between C1 and the occipital bone. We opened the dura in a Y shape and dissected arachnoid membranes between the cerebellar tonsils and the medulla oblongata, and applied bipolar cautery to shrink the tonsils. Cerebrospinal fluid (CSF) flow was established at the level of the craniocervical junction. We sutured arachnoid membranes for the prevention of adhesive arachnoiditis and performed a duraplasty with a fascia in a watertight fashion and augmented with fibrin glue to prevent cerebrospinal fluid leakage. The wound was closed meticulously in layers.

ELECTROPHYSIOLOGICAL MONITORING For the intraoperative neurophysiologic monitoring (INM), anesthesia was induced with thiopental and a subsequent infusion of sufentanil and vecuronium bromide and then maintained with a continuous infusion of remifentanil and propofol. Both transcranial electrical MEPs and SSEPs were monitored and recorded continuously throughout the entire operation, from positioning of the patient through wound closure. All electrophysiological data were stored, and completion time points of positioning, craniotomy, durotomy, tonsillectomy and duraplasty, and wound closure were noted. Multimodal monitoring of SSEPs and MEPs was continuously performed by an experienced electrophysiological team (MEE1200, Nihon Kohden, Tokyo, Japan). Baseline studies were obtained prior to positioning the patient into the prone position and thereafter. Somatosensory-evoked potentials were measured (bandpass filter: 10–1000 Hz) after stimulation of the medial by surface electrodes on the wrist using square-wave electrical pulses. A high current amplitude was used (16–40 mA), sufficient enough to elicit a moderate twitch of the target muscle, as a low duration of stimulus was used (0.2 ms duration at a frequency of 5.3 Hz). Recording electrodes were placed in the parietal area at C3’, C4’, CZ’, and FZ according to the international 10/20 system.

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Series of up to 500 responses with sweeps of 50 or 100 responses were amplified averaged, and superimposed to ensure reproducibility. The N20 peak was used to determine the latency and amplitude of the responses. A subgroup of patients received an equivalent preoperative electrophysiological evaluation 1 day before the surgery using the same setup. Motor-evoked potentials were recorded after transcranial electrical stimulation using corkscrew-like electrodes inserted into the scalp at C3 or C4. Constant-voltage stimulation was applied in trains of 5 rectangular pulses (pulse duration 50 ms, interstimulus interval 2 ms, 160–600 V, 120% of motor threshold, 365 V of stimulus intensity). Motor-evoked potentials (bandpass filter: 150– 3000 Hz) were recorded from paired needles inserted into the bilateral abductor pollicis brevis (APB-MEP). If MEPs were reproducibly evoked twice, the peak-to-peak amplitude and latency were determined. The impedances of all electrodes were maintained below 5 kV. Somatosensory-evoked potentials and MEPs were monitored continuously. We did not add lower extremity muscle to the MEP montage. Upper extremity, that is, bilateral APB muscles were chosen for target muscles to avoid excess stimulus intensity. Metrics of SSEPs and MEPs after positioning (baseline) and after closure of the dura (final) were noted for further analysis. Final-tobaseline MEP and SSEP amplitude and latency ratios were calculated. Left- and right-sided data were pooled for statistical evaluation.

EVALUATION OF INTRAOPERATIVE MOTOREVOKED POTENTIALS AND SOMATOSENSORYEVOKED POTENTIALS The MEPs signals were observed continuously during the operation by a trained neurosurgeon. Significant changes in amplitudes and latencies were supposed to be communicated to the operative team. A change of 50% in amplitude from the baseline value, and a change of 10% in latency from the baseline value were considered significant for intraoperative use both in MEPs and SSEPs. The amplitudes of baseline MEP responses are very low below 100 mV with 120% of motor threshold in this patient. Baseline amplitudes of right APB-MEPs were significantly lower than left. APB-MEPs, whereas baseline latency of right and left APB-MEPs were qualitatively, quantitatively equivalent (Fig. 2A–D, Table 1). Within a few minutes after craniotomy, a 25% increase of the amplitude of the right side over the baseline value was observed. #

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INM for Chiari

TABLE 1. The Mean Amplitudes and Latencies of the Motor-Evoked Potentials and N20 at Different Stages of Decompression From Positioning Through Dural Plasty Surgical Step Parameter

Side

Positioning to Craniotomy C1 Laminectomy (1)

Craniotomy to Dura Opened (2)

Dura Opened to Dural Plasty (3)

Mean Mean Mean Mean Mean Mean Mean Mean

Left

82.8 23.4 2.81 16.9 28.7 24.1 2.09 16.8

104 22.9 2.84 17.1 34.4 22.7 2.08 16.8

106 21.1 3.49 17.1 81.7 18.3 2.88 16.8

amplitude MEP (mV) latency MEP (ms) amplitude N20 (mV) latency N20 (ms) amplitude MEP (mV) latency MEP (ms) amplitude N20 (mV) latency N20 (ms)

Right

Baseline amplitudes of right abductor pollicis brevis (APB-MEPs) were significantly lower than left, whereas statistically significant laterality of latency was not seen. After craniotomy, a 25% increase of the amplitude of the right side over the baseline value was observed. Simultaneously, a 6% decrease of the latency from the baseline value was observed. And more, after durotomy, 185% increase of the amplitude over the baseline value was observed. Simultaneously, a 24% decrease of the latency was observed. After opening the dura, a 38% increase of the N20 amplitude of the right side over the baseline value was observed. Simultaneously, a 24% increase of the left side was observed. MEP, motor-evoked potential.

Simultaneously, a 6% decrease of the latency from the baseline value was observed. And more, within a few minutes after durotomy, 185% increase of the amplitude over the baseline value was observed. Simultaneously, a 24% decrease of the latency was observed. This clear MEPs improvement persisted until the end of the operation. Statistically significant increases of amplitudes were seen after craniotomy and durotomy (Fig. 2A–D, Table 1). From positioning to completion of craniotomy no significant change in SSEPs parameters could be observed. Within a few minutes after opening the dura, a 38% increase of the N20 amplitude of the right side over the baseline value was observed. Simultaneously, a 24% increase of the left side was observed. A statistically significant increase of N20 amplitudes was only seen after opening the dura. In this regard, both MEP amplitudes and latencies predominantly improved in severity-dependent and phase-dependent manner (ie, degree of improvements was more robust in more impaired right APB-MEP; Fig. 2A–D). Motor-evoked potential recoveries were always earlier than those of SSEPs (Tables 1 and 2).

POSTOPERATIVE COURSE The patient was extubated and awoke without any cardiorespiratory problems. Postoperative neurological examination revealed dramatically improved spastic gait compared with the preoperative state. It was also markedly different than that seen preoperatively, and had generated a significant and noticeable functional TABLE 2. The P Values of the Two-Tailed t Test for Motor-Evoked Potential and N20 Parameters at the Different Stages of Operation P Value Parameter

Side

(1) Versus (2)

(2) Versus (3)

MEP amplitudes MEP latencies N20 amplitudes N20 latencies MEP amplitudes MEP latencies N20 amplitudes N20 latencies

Left

Intraoperative Neurophysiologic Monitoring for Prediction of Postoperative Neurological Improvement in a Child With Chiari Type I Malformation.

Although many surgical treatment strategies for Chiari malformation type I (CM-I) have been reported, the most appropriate surgical technique remains ...
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