Med Lasers 2024; 13(1): 47-53  https://doi.org/10.25289/ML.24.003
Study on the neurological prognosis of patients who have undergone spinal surgery with intraoperative neurophysiological monitoring in Republic of Korea: a retrospective single center study
Jin-Yong Kim, Seung Hoon Yun, Chang-Min Lee
Department of Neurology, Dankook University College of Medicine, Cheonan, Republic of Korea
Correspondence to: Chang-Min Lee
E-mail: nrdoc@dku.edu
ORCID: https://orcid.org/0000-0001-9947-5791
Received: February 5, 2024; Accepted: March 7, 2024; Published online: March 30, 2024.
© Korean Society for Laser Medicine and Surgery. All rights reserved.

This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Abstract
Background: The purpose of this study was to determine how intraoperative neurophysiological monitoring (IONM) affects the neurological prognosis of patients based on the data from outcomes of various spinal surgeries.
Methods: A retrospective cohort study was conducted by reviewing the medical records of 175 patients who underwent spinal surgery using IONM from March 2017 to February 2022 at the Dankook University Hospital. These patients were divided into two groups, namely IONM-alarmed patients and non-alarmed patients. Their neurological prognosis was compared based on their Medical Research Council (MRC) grade, the length of hospital stay in days, the neuropathic pain scale, and the American Spinal Cord Injury Association (ASIA) scale. The MRC grade, neuropathic pain scale, and ASIA scale were compared using the chi-squared test. The length of hospital stay in days was compared using the Kaplan–Meier survival analysis.
Results: There was no statistical relationship between the MRC grade and the results of the IONM (p = 0.364). However, survival analysis of the two groups showed a meaningful difference (p = 0.047). The average hospital stay in days was 9.734 ± 0.443 for the non-alarmed group and 13.278 ± 1.834 days for the alarmed group.
Conclusion: IONM during spinal surgery did not result in a significant difference between the alarm signs of IONM and the muscle strength grade of the patients in the short term. However, this study showed that the IONM can shorten the length of hospital stay in days related to returning to daily living.
Keywords: Intraoperative neurophysiological monitoring; Prognosis; Hospital stay; Muscle strength
INTRODUCTION

Intraoperative neurophysiological monitoring (IONM) is a testing method that detects neurological damage that occurs during surgery and complications that may occur after surgery. It was introduced in the 1990s in Republic of Korea (ROK) and has been used in various neurological surgeries, including spine surgery [1]. A variety of devices are used in IONM including somatosensory evoked potential (SSEP), motor evoked potential (MEP), brainstem auditory evoked potential, and visual evoked potential tests, and it also includes free-running and triggered electromyography (EMG) and electroencephalogram [2]. The application of these test methods varies depending on the type of surgery being performed, and SSEP, MEP, and EMG studies are usually required when performing spine surgery [3].

As the number of elderly patients increases, not only the number of patients undergoing spinal surgery, but also the incidence of complications and side effects increases. Nasser et al. [4] reported that an overall complication incidence after spine surgery was 16.4% per patient, and that complications were more common in thoracolumbar (17.8%) than cervical procedures (8.9%). Among these, neurological complications occurring after surgery accounted for 1.05%. To prevent these complications, surgeons began using IONM. Of course, theoretically, it is possible to further improve the safety of patients through IONM, but it has not yet been established exactly in what aspects and how these devices improve the prognosis of patients. Some studies have been conducted on IONM and the presence or absence of neurological deficits after spine surgery [5,6]. However, to the best of the authors’ knowledge, there are no retrospective studies on patients who underwent spine surgery at a single center in ROK using multimodal IONM including SSEP, MEP, and EMG. The authors sought to study the diagnostic and therapeutic value of IONM to determine exactly how it affects the neurological prognosis of patients.

METHODS
Ethics statement: This study was approved by the Institutional Review Board (IRB) of Dankook University Hospital (IRB no. 2024-02-022). The requirement for informed consent from individual patients was omitted because of the retrospective design of this study.

Subjects

The subjects of the study were 175 patients who underwent spinal surgery using IONM at the Department of Neurosurgery or Orthopedics of Dankook University Hospital, Cheonan, ROK from March 2017 to February 2022. This retrospective study was conducted based on medical records and test results. Among these, patients whose neurological outcome worsened or whose hospitalization period was prolonged due to non-neurological causes such as pneumonia or bedsores were excluded, and patients who had neurological sequelae due to cerebral palsy or other stroke history before surgery were also excluded. In addition, in order to exclude cases where the hospitalization period is prolonged due to rehabilitation treatment or insurance-related matters, and to exclude cases where the hospitalization period is prolonged due to treatment for other concomitant diseases, the time of discharge for patients transferred to the rehabilitation department or other departments was taken at the point when he was transferred from the surgery department. The requirement for informed consent from individual patients was omitted because of the retrospective design of this study.

A total of 146 patients were classified according to age, sex, previous medical disease, presence and change of pain, pre- and postoperative changes in the Medical Research Council (MRC) muscle strength grade, and changes in IONM results.

Monitoring

The IONM device used in the study was NIM ECLIPSE IONM system (version 3.5.350; Medtronics). Preoperative tests used NICOLET EDX EMG/NCV/EP 8ch (2020; Natus) for evoked potential and EMG. The method of each test and the interpretation of the results followed clinical practice guideline of Korean Society of Intraoperative Neurophysiological monitoring and guidelines for neurophysiologic procedures of The Korean Society of Clinical Neurophysiology.

SSEPs

SSEPs were performed by stimulating the median nerve in the upper extremity and the posterior tibial nerve in the lower extremity. During surgery, stimulation was performed using a constant current method at 5 to 30 mA, with a stimulation width of 0.1 to 0.3 ms and a stimulation frequency of 2 to 5 Hz. This was usually done by stimulating the limbs alternately rather than performing them simultaneously and analyzing the waveforms. Cortical potentials are recorded from the C3’ or C4’ electrode and the Cz’ electrode located 2 cm posterior to the C3 and C4 electrodes of the international 10-20 system, and in addition, C2S and C5S above the second and fifth cervical vertebrae to confirm subcortical potentials. Recording electrodes may be added or placed at Erb’s point or popliteal fossa to evaluate whether stimulation is being delivered properly. Among the waveforms formed in this way, the negative waveform (N20) with a latency of 20 ms was observed for the median nerve SSEP, and the positive waveform (P37) with a latency of 37 ms was observed for the posterior tibial nerve SSEP. Alarm criteria were 50% reduction in the amplitude or 10% increase in the latency.

MEPs

In the case of MEP, there are two methods: transcranial electrical stimulation muscle recording MEP (TES-MEP) and epidural electrical stimulation MEP (D wave). In this study, the transcranial electrical stimulation method was used. The stimulating electrode was installed 1 to 2 cm in front of C1/2 or C3/4 in the international 10-20 system, and both constant voltage stimulation and constant current stimulation were possible. In our study, we used a constant-voltage stimulation method and repeated 3 to 7 consecutive pulses of 500 V stimulation, with pulse intervals of 1 to 5 ms and pulse duration of 0.05 to 0.20 ms. The recording method was usually performed on distal muscles that can obtain large waveforms due to the large number of innervating nerve fibers, such as abductor pollicis brevis, abductor digiti quinti, abductor hallucis, and tibialis anterior. Two needle electrodes were inserted into one muscle to record compound muscle action potential. A decrease of more than 80% in amplitude between peak points was considered a significant criterion, and an increase of latency of more than 10% or an increase of more than 3 ms was also used as an additional criterion.

Free-run and stimulus induced EMG

Free-run EMG uses the principle that when there is mechanical stimulation that occurs during surgery, an electrical signal is generated in the nerve fibers, which excites the muscles and generates an EMG signal. However, these signals do not necessarily mean nerve damage. The sensitivity of free-running EMG in predicting morbidity after lumbar spinal surgery is very high (99%), but the specificity is known to be very low at around 24% [7]. Stimulus induced EMG was usually performed in surgeries that go under the dura. Electrical stimulation was applied to identify the type of nerve observed during the surgery, and the type of muscle connected to this nerve or the location of instruments such as screws inserted during surgery were too close. A high frequency filter of 10-30 kHz and a low frequency filter of 2-30 Hz were used, and the EMG signal was observed by stimulating less than 8 mA with a time base of 200 ms to 5 seconds.

Statistical analysis

Sex, presence of chronic medical disease, pre- and postoperative changes in MRC grade, and changes in IONM results were classified as categorical variables. Chronic medical diseases included hypertension, diabetes, heart disease, pulmonary disease, and renal disease that can change the pre- and postsurgical prognosis and hospitalization period, and included patients taking medications at the time of surgery. In MRC grade, if there was improvement after surgery or if the strength grade after surgery was the same, the patient was classified into improved or maintained group. If the strength grade after surgery worsened, he or she was classified as exacerbated group. In IONM, it was classified as non-alarmed group if there was no change, and as alarmed group if there was a loss or change in the waveform. Patients with proven spinal cord injury clinically, through imaging, or electrophysiological tests and patients without injury were classified separately. Age was classified as the first group for patients aged 30 to 49 years, the second group for patients aged 50 to 69 years, and the third group for patients over 70 years of age. This was to reduce statistical errors by keeping the number of patients in each group similar. In pain, a score of 0 to 10 was assessed on the NRS (numeric rating scale) at the time of hospitalization before surgery. Patients with a score of 0 to 4, a group that does not require pharmacological intervention, were classified as mild pain group, and patients with a score of 5 to 6 were classified as moderate pain group, and patients with a score of 7 or more were classified as severe pain group.

The relationship between the patient groups classified and the groups according to changes in IONM was analyzed using the chi-square test. Differences in the length of hospital days between groups according to changes in IONM were compared in survival analysis graphs according to Kaplan–Meier curve analysis. Additionally, the Cox proportional hazards model was used to analyze other independent variables that could affect the length of hospital days. Statistical significance was expressed as a p-value, and if it was less than 0.05, it was expressed as a significant difference. Statistical analysis was performed using IBM SPSS Statistics 23 (IBM Corp.).

RESULTS

Characteristics of patients

Among the total 146 patients included in the study, 18 patients (12.3%) showed significant abnormalities in IONM, and 128 patients (87.7%) showed no significant changes (Table 1). At demographic characteristics, there were 106 male (72.6%) and 40 female (27.4%). Age was divided into three groups: 24 patients aged 30 to 49, 85 patients aged 50 to 69, and 37 patients aged 70 or older. Additionally, age and sex had no statistically significant relationship with changes during IONM. The presence or absence of a medical history was not related to changes during IONM. On the MRC grade, 42 patients (28.8%) worsened compared to before surgery, and 104 patients (71.2%) improved or maintained their strength. There was a difference, but it did not produce statistically significant results (p = 0.364). Patients were divided into three groups according to the degree of preoperative pain, with 111 patients (76.1%) in the mild pain group, which was more than those with moderate pain (15.1%) or severe pain (8.9%). However, there was no statistical correlation between changes in IONM and the three groups (p = 0.389). There were more cases without postoperative spinal cord injury (86.3%) than those with (13.7%), but there was no statistical correlation with the results of IONM (p = 0.253).

Table 1 . Baseline characteristics of enrolled patients

CharacteristicIONM non-alarmed (n = 128)IONM alarmed (n = 18)Total (n = 146)p-value
Sex0.186
Female33 (25.8)7 (38.9)40 (27.4)
Male95 (74.2)11 (61.1)106 (72.6)
Age (yr)0.882
30-4922 (17.2)2 (11.1)24 (16.4)
50-6974 (57.8)11 (61.1)85 (58.2)
≥7032 (25.0)5 (27.8)37 (25.3)
Past medical history0.104
Presence74 (57.8)7 (38.9)81 (55.5)
None54 (42.2)11 (61.1)65 (44.5)
Change of MRC grade after surgery0.364
Exacerbated38 (29.7)4 (22.2)42 (28.8)
Improved or maintained90 (70.3)14 (77.8)104 (71.2)
Pain (NRS)0.389
Mild (0-4)100 (78.1)11 (61.1)111 (76.1)
Moderate (5-6)15 (11.7)7 (38.9)22 (15.1)
Severe (≥7)13 (10.2)013 (8.9)
Spinal cord injury0.253
Presence19 (14.8)1 (5.6)20 (13.7)
None109 (85.2)17 (94.4)126 (86.3)

Values are presented as number (%).

IONM, intraoperative neurophysiological monitoring; MRC, Medical Research Council; NRS, numeric rating scale.



Comparison of hospital days between non-alarmed and alarmed patients

In terms of IONM detecting complications that may occur after surgery, the survival analysis graph showed a significant difference when comparing the hospital days between non-alarmed and alarmed group (p = 0.047; Fig. 1). The average hospital days for the non-alarmed group was 9.734 ± 0.443, while the average hospital days for the alarmed group was 13.278 ± 1.834 days (Table 2). Therefore, compared to other factors, it can be said that IONM played a role to some extent in reducing the length of hospital stay. Other risk factors that affect the hospital days were analyzed using the Cox proportional hazards model. Sex, age, degree of pain, and presence of spinal cord injury did not all show significant values. However, it was analyzed that the presence or absence of a past medical disease history had an effect on the hospital days (p = 0.009), and the proportional risk of lengthening the hospital days increased by 1.627 times in the group with a past medical disease history compared to the group without (Table 3).

Table 2 . Average and median value of hospital days between non-alarmed and alarmed patients in intraoperative neurophysiological monitoring (IONM) according to Kaplan–Meier curve

IONM changeAverage ± standard deviation95% Confidence interval

Lower limitUpper limit
Non-alarmed9.734 ± 0.4438.86510.604
Alarmed13.278 ± 1.8349.68316.873
Median10.171 ± 0.4579.27511.067


Table 3 . Variables associated with postoperative hospital days by Cox proportional hazards model

β coefficientHR (95% CI)p-value
Sex
Male0.2371.268 (0.86, 1.868)0.231
Female (ref)
Age (yr)
30-49 (ref)
50-69–0.4260.653 (0.409, 1.043)0.074
≥70–0.4950.609 (0.352, 1.055)0.077
Past medical history
Presence0.4871.627 (1.128, 2.349)0.009
None (ref)
MRC change
Improved or maintained–0.0460.955 (0.658, 1.387)0.810
Exacerbated (ref)
Pain (NRS)
Mild (0-4) (ref)
Moderate (5-6)0.1411.151 (0.699, 1.895)0.580
Severe (≥7)–0.4450.641 (0.339, 1.211)0.171
Spinal cord injury
Presence–0.3530.702 (0.421, 1.172)0.176
None (ref)
IONM change
Alarmed0.4711.601 (0.966, 2.654)0.014
Non-alarmed (ref)

HR, hazard ratio; 95% CI, 95% confidence interval; ref, reference; MRC, Medical Research Council; NRS, numeric rating scale; IONM, intraoperative neurophysiological monitoring.



Figure 1. Comparison of hospital days between non-alarmed and alarmed patients in intraoperative neurophysiological monitoring (IONM) by Kaplan–Meier curve (p = 0.047).
DISCUSSION

In this study, the difference in the presence or absence of abnormalities in IONM among patients who underwent spinal surgery played a role in influencing the patient’s length of hospital days from surgery to discharge, and other factors affecting the length of hospital days included the patient’s medical condition. However, it was found that the patient’s age, sex, presence of pain, presence of spinal cord injury, change in MRC grade, and presence of past medical history did not affect the results of intraoperative nervous system monitoring itself.

First of all, age and sex are known to be important factors affecting spinal degeneration. However, it is known that this varies greatly from person to person and other factors also have an effect [8]. Furthermore, in IONM, the principle of notifying abnormalities by measuring relative changes in the waveform during surgery does not evaluate abnormalities in absolute numbers, so it is not greatly affected by the condition of the spine before surgery due to sex or age.

The reason for the lack of correlation between the presence of pain and IONM can be found in the anatomical factors of the spinal cord. The SSEP of the IONM is a device that mainly tests sensory tracts located in the dorsal column of the spinal cord [1]. Somatic pain is mainly transmitted along the ascending lateral spinothalamic tract, which is not significantly affected by SSEP [9]. There is currently no quantitative method to objectively evaluate a patient’s paresthesia or hypoesthesia, such as tingling and numbness, so there is a limitation in accurately analyzing the clinical correlation between neuropathic pain and IONM results [10].

Unlike pain, motor weakness is a dysfunction of the corticospinal tract, the same pathway as the MEP study [9]. However, this study did not reveal a correlation between IONM results and MRC grade, and Sala et al. [11,12] reported that this was due to the timing of the investigation. The postoperative muscle strength grade of the patients in our study was assessed at the time of discharge or transfer, and the average length of stay for the patients was 10.171 ± 0.457 days. Another study showed that IONM protocol significantly improves motor outcome at a follow-up of at least 3 months. However, that study also showed that short-term evaluation, early after surgery, did not show an advantage for the monitored versus non-monitored group, and the authors assumed that these results were likely due to the transient paraplegia phenomenon that would mask the beneficial role of monitoring, when patients are evaluated in the early postoperative stage [11]. Transient weakness caused by compression of spinal nerves does not immediately recover even after surgery. This is because it takes some time for the swelling around the nerves to disappear after surgery [13,14].

When spinal cord injury occurs due to compression from the vertebral body or spinal stenosis, various symptoms such as ipsilateral spastic paralysis and contralateral paresthesia occur as in Brown-Séquard syndrome [9]. However, if the degree is mild, the correlation between IONM, which monitors motor and sensory pathways, and spinal cord injury may be less relevant because the degree of injury varies depending on the spinal pathway involved. In our study, there was also no statistical significance between spinal cord injury and IONM results.

There was no statistical correlation between past medical history and the results of IONM. However, it has been found to have an effect on the patient’s hospital days. Delayed recovery of the surgical wounds due to diabetes, postoperative management of high blood pressure, and the occurrence of other postoperative complications are believed to have influenced the hospital days. Another study also reported similar results [6].

The most characteristic feature of this study is that it revealed the relationship between the hospital days after surgery and the results of IONM. When a patient is discharged from the hospital after surgery, in addition to pain and motor strength grades, which the authors consider variables, the degree of recovery from the wound at the surgical site and whether the patient is active enough to lead daily life also affect discharge. During surgery, spinal nerves can be operated on more selectively through stimulus induced EMG, which can help with recovery after surgery by minimizing the surgical area and iatrogenic damage. In addition, although statistical significance was not revealed in this study, Fehlings et al. [15] showed that IONM reduces perioperative neurologic deficits. It is believed that IONM alert will have the effect of reducing hospital days by preventing permanent and serious nerve damage. Therefore, hospital days can also be used as an indicator of the patient’s prognosis.

However, this study has several limitations. First of all, as it is a retrospective study, there is a lack of detailed records. In addition, in spine surgery, there are clear differences between cervical spine surgery and lumbar surgery depending on the surgical site, and there are also differences depending on the type of surgery, such as tumor surgery and degenerative disease surgery. Therefore, for accurate research, future study is needed to determine the surgical site and surgical method. It should be classified according to each category. Lastly, a prospective study including a larger number of cases will be needed.

IONM is widely used as a device to detect neurologic deficits that occur during surgery, but even after more than 30 years since its development, large-scale randomized controlled trials have not been conducted [15,16]. Howick et al. [16] reported on IONM-related clinical trials conducted until recently and revealed the limitations of clinical trials. First, they said that creating a control group itself when designing a prospective randomized trial could be ethically problematic. Therefore, from the perspective of evidence-based medicine, it was reported that the external validity of clinical trials was lacking. Additionally, there have been ongoing discussions about the effectiveness of IONM and whether it should be used for diagnostic test or interventional purposes [15,16].

In conclusion, this study showed that IONM during spinal surgery plays a role in helping patients quickly return to their daily lives and reducing the length of hospital days by early detecting and preventing nerve damage that may occur during surgery. In addition, the correlation between the alarm signs of IONM and hospital days showed that it could be used as a postoperative prognostic factor. However, the correlation between IONM results and neurological symptoms such as pain and motor weakness observed in a short period of time could not be revealed. Nevertheless, since the clear benefits of IONM have been revealed, it is believed that surveillance through the adoption of appropriate IONM tests should be performed in spinal surgery with a risk of intraoperative nervous system damage.

SUPPLEMENTARY MATERIALS

None.

ACKNOWLEDGEMENTS

This article is based on the master’s thesis of the second author (Seung Hoon Yun) from Dankook University.

AUTHOR CONTRIBUTIONS

Conceptualization: JYK, SHY, CML. Data curation: SHY, JYK. Formal analysis: SHY, CML. Investigation: SHY. Methodology: SHY, CML. Project administration: CML. Software: SHY. Validation: JYK, SHY, CML. Visualization: SHY. Writing–original draft: JYK. Writing–review & editing: all authors.

CONFLICT OF INTEREST

No potential conflict of interest relevant to this article was reported.

FUNDING

None.

DATA AVAILABILITY

Contact the corresponding author for data availability.

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