Intraoperative Neuromonitoring as an Added Safety Measure to Prevent Iatrogenic Injury in Chiari I Malformation Surgery

doi:10.21203/rs.3.rs-2758320/v1

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Intraoperative Neuromonitoring as an Added Safety Measure to Prevent Iatrogenic Injury in Chiari I Malformation Surgery

https://doi.org/10.21203/rs.3.rs-2758320/v1

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PURPOSE

To assess the surgical utility of intraoperative neuromonitoring (IONM) as a safety measure to ensure safe operative conditions in Chiari I malformation patients undergoing FMD.

METHODS

This represents a retrospective cohort study examining symptomatic Chiari I malformation patients at one tertiary care center that underwent FMD using IONM between January 2017 and 2022. Brainstem auditory evoked response (BAER), somatosensory evoked potentials (SSEP), motor evoked potentials (MEP), and electromyography (EMG) were utilized in all cases. Patients with and without IONM changes were directly compared. Linear regression analysis was completed to identify variables predictive of IONM changes.

RESULTS

Forty-eight patients met inclusion criteria, with ages ranging from 1 to 52 years (mean 15 years). The incidence of co-existing syringomyelia was 40% (n = 19), scoliosis 15% (n = 7), and tethered cord 0%. Four patients (8%) experienced IONM changes intraoperatively, all manifesting as decreases in MEPs. These were corrected by increasing mean arterial pressure (n = 1) or patient and head and neck repositioning (n = 3). Scoliosis predicted IONM changes (Beta 0.30, p = 0.04). Absence of syringomyelia trended towards predicting against IONM changes, however this did not reach significance (Beta − 0.24, p = 0.09).

CONCLUSION

Foramen Magnum

Motor-evoked-potentials

Scoliosis

Chiari I malformations are defined as cerebellar tonsillar ectopia through the foramen magnum, commonly cited as greater than 5mm, with the well-established surgical treatment being foramen magnum decompression (FMD) with or without duraplasty in symptomatic patients [1–5]. Intraoperative neuromonitoring (IONM) is a widely used tool in neurosurgical practice, most often used to identify high risk surgical maneuvers or events resulting in injury to neurological structures [6, 7]. Previous studies have investigated the use of IONM as a tool to predict the success of FMD in Chiari malformation patients. These studies have suggested that IONM does not significantly alter the surgical plan or predict decompression success, limiting its utility in Chiari decompression surgery [2, 8–15]. Types of IONM modalities assessed in the context of FMD include brainstem auditory evoked response (BAER), somatosensory evoked potentials (SSEP), motor evoked potentials (MEP), and electromyography (EMG) [2, 4, 11, 12, 16].

Due to the cervicomedullary junction compression in Chiari I malformation, adequate patient positioning is essential in avoiding iatrogenic injury. The optimal degree of neck flexion or extension to facilitate working angles for FMD, and an attempt to maintain near anatomic alignment to avoid neurological structure injury, can sometimes prove challenging. IONM may provide an additional safety check for these patients to reduce the likelihood of neurological injury throughout the duration of surgery [15, 17]. Changes in IONM findings may alert the surgeon of impending damage to the brainstem or spinal cord. Modifications in patient positioning, cerebral or spinal cord perfusion, or anesthetic use can be instituted in an attempt to correct IONM changes before they result in patient injury [18].

The objective of this study was to assess the surgical utility of IONM as a safety measure to ensure optimal operative conditions for the compressed cervicomedullary junction in Chiari I malformation patients undergoing FMD.

Study design

This represents a retrospective observational, cohort study. One sample of Chiari malformation patients was assessed with no control group. This study was approved by the institutional review board.

Inclusion criteria

Patients aged 1 year to 60 years with symptomatic Chiari I malformation that underwent FMD between January 2017 and January 2022 were included in this study. All patients were treated at a single academic institution by the same attending neurosurgeon (senior author MA) with resident assistance. Patients were determined to be symptomatic from their Chiari I malformation if they experienced headaches worsened by valsalva, dysphagia, central sleep apnea, bowel or bladder dysfunction, extremity sensory loss, extremity weakness, or gait instability.

Data collection

All data was collected by retrospective electronic health record review. Demographic data including patient age, sex, indications for surgery, tonsillar descent on sagittal magnetic resonance imaging (MRI), presence of syringomyelia, presence of scoliosis, presence of tethered cord, expansile duraplasty performed, tonsillar coagulation performed, arachnoid dissection performed, type of IONM used, and anesthesia type was collected. The outcomes assessed were IONM changes that took place, interventions to correct these changes, and postoperative new symptoms or neurologic deficits in these cases.

Intraoperative neuromonitoring

Nuvasive clinical services™ (10275 Little Patuxent Parkway, Suite 300, Columbia, MD 21044, Phone 410-740-2375, Fax 410-740-1518) IONM was used for all cases. BAER, upper and lower limb SSEP, upper and lower limb transcranial MEP, and electromyography (EMG) were used in all cases. IONM was provided by a certified intraoperative technician with real time supervision and tracing interpretation by a board-certified neurologist. Reader rating of data quality for interpretation was listed as good in all cases. SSEPs were measured from the median nerve distributions, the posterior tibial distributions, and the ulnar nerve distributions bilaterally in all cases. MEPs were measured in all four limbs in all cases. EMG was measured from the body of the trapezius muscle bilaterally in all cases. Baseline BAER, SSEPs, MEPs, and EMG were obtained and reported to the surgeon at the beginning of every case. Care was taken to ensure that each was reproducible and monitorable. MEPs were only done at the surgeon’s request during the procedure. In all cases the attending neurosurgeon requested MEPs at each step of the case at regular intervals.

Operative procedure

All patients underwent surgery under general anesthesia. Patients were positioned prone on the operating room table. The head was fixed with a head clamp with pins for 3-point fixation with the chin tucked and the neck flexed. All pressure points were padded with gel and foam padding. At this point, baseline BAER, SSEP, MEP, and EMG were obtained. The hair was clipped, the skin was cleaned, prepped, and draped in the usual sterile fashion. A linear incision was made from the inion to the C2 spinous process. The soft tissue was dissected down to the occipital bone. Suboccipital craniectomy was then performed starting approximately 2cm superior to the foramen magnum. The posterior ligamentous structures were divided at the midline and freed from the underlying dura. Care was taken to remove the dural band at the level of the atlanto-occipital membrane. C1 laminectomy was then performed. Intraoperative ultrasonography was then used to view the degree of cerebellar tonsillar compression and cerebrospinal fluid flow. A decision was then made if duraplasty was necessary based on the degree of cerebellar tonsillar compression and cerebrospinal fluid flow after the craniectomy and laminectomy decompressions were finished, as well as the preoperative imaging. Duraplasty was performed if the cerebellar tonsils remained compressed and cerebrospinal fluid flow was obstructed. A Y-shaped incision was made in the dura exposing the underlying cerebellar tonsils. Arachnoid adhesions were dissected and removed until a clear view of the obex of the fourth ventricle could be obtained. To create more space, the most caudal aspects of the cerebellar tonsils were cauterized in some cases. The dura was then closed with synthetic dural substitute and a running suture. Hemostasis was obtained and the incision was then closed.

Addressing IONM changes

All patients that were found to have IONM changes were treated under the direction of the attending operating neurosurgeon. If a change was detected, the surgical procedure was first paused and the action preceding the IONM change was undone if possible. Non-invasive measures were then utilized including repositioning of the patient’s head and neck by manipulation of the head clamp with pins, changes in anesthetic administration by the anesthesia team, and increases in mean arterial pressure. Further measures were at the discretion of the attending operating neurosurgeon depending on the circumstances of the individual situation.

Statistical analysis: All statistics were performed using IBM SPSS statistics (IBM Corp. Released 2021. IBM SPSS Statistics for Windows, Version 28.0. Armonk, NY: IBM Corp). Descriptive data is reported with means, standard deviation (SD), range, and percentages as appropriate. Outcome data is reported as frequency data with associated percentages. Comparison of means between groups are made using T-tests of independent samples. Comparison of frequency data is made using Chi Square tests or Fisher Exact Probability Tests depending on sample size. The ability of an independent variable to predict the outcome/dependent variable was assessed using linear regression analysis. An alpha value of 0.05 was used as a threshold to determine statistical significance.

Forty-eight patients met inclusion criteria. Patient age ranged from 1 to 52 years. Mean age was 15 years (SD = 10 years). Sixty-seven percent (n = 32) were female. The incidence of syringomyelia was 40% (n = 19), scoliosis 15% (n = 7), and tethered cord 0% (n = 0). All patients underwent suboccipital craniectomy and C1 laminectomy with or without duraplasty for Chiari I malformation decompression. Twelve patients (25%) underwent expansile duraplasty, tonsillar coagulation, and arachnoid dissection. All patients underwent surgery with IONM including BAER, SSEP, MEP, and EMG with signals consistent with each patient’s baseline at the start of each respective procedure. All patients underwent surgery with general anesthesia (Table 1).

Table 1

Descriptive data of cohort (n = 48)
Patient Age
Age Range	1–52 years
Mean Age (SD)	15 years (10 years)
Patient sex
Male (%)	16 (33%)
Female (%)	32 (67%)
Tonsillar descent on sagittal MRI
Range	5–26mm
Mean (SD)	12mm (5mm)
Syringomyelia
Incidence (%)	19 (40%)
Scoliosis
Incidence (%)	7 (15%)
Tethered cord
Incidence (%)	0 (0%)
Expansile duraplasty performed
Number (%)	12 (25%)
Tonsillar coagulation performed
Number (%)	12 (25%)
Arachnoid dissection performed
Number (%)	12 (25%)
SD – standard deviation. % - percentage of patients.

Four patients (8%) experienced changes in IONM. All 4 instances were discovered as decreases in MEPs. Each change was addressed by the operating attending neurosurgeon. One patient (25%) experienced return of MEP to baseline after increasing mean arterial pressure. Three patients (75%) experienced return of MEP to baseline after repositioning of the patient’s head and neck by manipulation of the head clamp with pins. The incidence of postoperative new neurologic deficit was 0% (Table 2).

Table 2

Changes in IONM, interventions to correct these changes, and incidence of resulting new neurologic deficit (n = 48)
Neurophysiologic monitoring change
Present (%)	4 (8%)
Absent (%)	44 (92%)
Interventions
Increase mean arterial pressure (%)	1 (25%)
Patient repositioning (%)	3 (75%)
Neurophysiologic monitoring modality that changed
BAER (%)	0 (0%)
SSEP (%)	0 (0%)
MEP (%)	4 (100%)
EMG (%)	0 (0%)
New post-operative symptoms or neurologic deficit
Incidence	0 (0%)
IONM – intraoperative neuromonitoring, % - percentage of patients, BAER – brainstem auditory evoked response, SSEP – somatosensory evoked response, MEP – motor evoked potentials, EMG – electromyography

A comparison of cases with IONM changes and those without can be viewed in Table 3. No significant differences were identified between the groups.

Table 3

Comparison of cases with IONM changes (n = 4) to cases without (n = 44)
Variable	IONM changes	No IONM changes	P-value
Mean patient age (SD)	13 years (3 years)	14 years (9 years)	0.38
Tonsillar descent on sagittal MRI (SD)	11mm (5mm)	12mm (5mm)	0.41
Syringomyelia (%)	0 (0%)	19 (43%)	0.13
Scoliosis (%)	2 (50%)	5 (11%)	0.10
Tethered cord (%)	0 (0%)	0 (0%)
Expansile duraplasty performed (%)	1 (25%)	11 (25%)	0.74
Tonsillar coagulation performed (%)	1 (25%)	11 (25%)	0.74
Arachnoid dissection performed (%)	1 (25%)	11 (25%)	0.74
IONM – intraoperative neuromonitoring, SD – standard deviation, MRI – magnetic resonance imaging, % - percentage of patients

Linear regression analysis was completed to assess the relationships between independent variables and the dependent variable, IONM changes (Table 4). The presence of scoliosis predicted IONM changes (Beta 0.30, p = 0.04). The absence of syringomyelia trended towards predicting against IONM changes, however this did not reach statistical significance (Beta − 0.24, p = 0.09).

Table 4

Linear regression analysis to assess the relationship between independent variables and IONM changes
Independent Variable	Beta	P-Value
Age	-0.05	0.75
Tonsillar descent on sagittal MRI	-0.03	0.82
Syringomyelia	-0.24	0.09
Scoliosis	0.30	0.04
Expansile duraplasty performed	0.00	1.00
Tonsillar coagulation performed	0.00	1.00
Arachnoid dissection performed	0.00	1.00
IONM – intraoperative neuromonitoring

IONM may be a useful tool to help facilitate safe FMD in Chiari I malformation patients. While this represents a single center experience with a small patient sample size, our data suggests that the utilization of IONM as a safety measure to prevent iatrogenic temporary or permanent neurologic deficit may be beneficial and warrants further study. The incidence of IONM changes in our patient cohort was 8%, representing a noteworthy proportion of patients. IONM allowed for these changes to be quickly addressed through non-invasive intraoperative maneuvers with no post-operative new neurologic deficits. Conclusions from this small sample are limited, however the data does suggest scoliosis and syringomyelia may be related to risk of IONM changes. In linear regression analysis, the presence of scoliosis predicted IONM changes (p = 0.04), while the absence of syringomyelia trended towards predicting against IONM changes (p = 0.09). Further study with a larger patient sample may be beneficial to further investigate these findings and assess the efficacy of IONM as an added patient safety mechanism in FMD for Chiari I malformation.

IONM use during Chiari I malformation decompression surgery remains controversial in the literature. Studies have demonstrated that while IONM findings may improve or remain constant during FMD, this may not correlate with patient outcome raising question of its clinical utility [2, 8, 10–13]. Additionally, IONM has not been shown to enhance the safety of FMD in multiple series. Of note, these studies reported patient post-operative outcomes, but did not report individual intraoperative events that may have been detected and managed using the findings of IONM [2–4, 12, 15, 16, 19]. To our knowledge, this represents the first series reporting these events and actions taken to correct them. Our cohort demonstrated a 0% incidence of new post operative neurologic deficit, however 8% of patients experienced an IONM change that was detected immediately and managed effectively. In a high-volume center or practice, this may represent a significant number of FMD patients. Our study is the first to identify a sub-population of Chiari I malformation patients who may be more likely to experience IONM changes during FMD

Limitations in our study design and findings are worth discussion. The small sample size limits conclusions that can be drawn from the study as important findings may be missed if insufficient power is present. This is especially important when the outcome of interest is rare. All data is collected through retrospective electronic health record review and therefore subject to limitations with documentation and data retrieval. The retrospective study design limits the strength of conclusions that can be drawn from the study due to an inferior level of evidence, the potential for recall bias, misclassification bias, and confounding, and the inability to determine causation. This analysis does not examine the cost effectiveness of IONM in Chiari I malformation surgery, an important factor when considering when to utilize any surgical adjunct.

Critical analysis of this work provides direction for future research in this area. Pooling patient data from multiple centers may provide a larger sample for data analysis to draw stronger conclusions on the utility of IONM as an added safety measure to prevent iatrogenic neurologic injury in Chiari I malformation patients. Adding an analysis of cost effectiveness of IONM in this patient population may be useful to provide more information to guide the neurosurgeon on its utilization.

Conflicts of Interest: The authors report no conflicts of interest in any form.

Statements & Declarations: The authors report no conflicts of interest in any form, including those of employment, funding, financial interests, or non-financial interests.

Acknowledgements: None

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No competing interests reported.

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Intraoperative Neuromonitoring as an Added Safety Measure to Prevent Iatrogenic Injury in Chiari I Malformation Surgery

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Abstract

PURPOSE

METHODS

RESULTS

CONCLUSION

Introduction

Methods

Results

Discussion

Declarations

References

Additional Declarations

Status:

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