INTRODUCTION
Kyphosis is a progressive sagittal spinal deformity caused by congenital vertebrate defect, degeneration, infection, and trauma of the spine [1,2]. Severe kyphosis often causes significant spinal instability, pain, and neurological compromise, which entails surgical correction to address the deformity and mitigate these symptoms. In corrective surgery, one particular concern is the risk of neurological complications. Despite huge efforts to improve surgical techniques and intraoperative neurophysiological monitoring (IONM), the reported risk of neurological complications is still as high as 2.8% [3].
Global kyphosis > 90°, vertebral column resection, cervicothoracic/thoracic osteotomy, blood loss > 3,000 mL, and preoperative neurologic deficits are reportedly associated with an elevated risk for neurological complications [4]. Given the high risk, IONM has now become indispensable for monitoring neurological function during correction surgery [5]. Loss of IONM data is an undesirable event during surgery, with a reported incidence ranging from 3%–27%. Moreover, despite established procedures for tackling IONM events, 3.8% of these events ultimately result in permanent neurological deficits [6,7]. Hence, the investigation into the risk factors for IONM events is still warranted clinically.
The relative spacing of the spinal cord within the canal is a critical determinant for spinal cord compression, and kyphotic spine carries a substantial risk of neurological compromise. In thoracic spinal stenosis caused by ossification of the thoracic ligamentum flavum (OLF), the ossified nodules are close to the dura mater, which increases the risk of intraoperative spinal cord injury [8]. In lumbar spine disease, the presence of a dural sac exhibiting a homogeneous gray signal devoid of cerebrospinal fluid (CSF) signal is related to an increased likelihood of conservative treatment failure [9]. In addition to the encroaching of the spine canal, the distraction of the spinal cord originating from kyphotic deformity potentially precipitate neurological functional impairment [10]. Despite the established link between spinal cord compression and neurological function in degenerative spinal disease, its implications for spinal deformities are not elucidated. Based on the presence or absence of visible CSF signals in patients with scoliosis, Sielatycki et al. [11] presented a risk classification utilizing axial-T2 magnetic resonance imaging (MRI) of the apex of the curve. This classification indicated the 11.7% of patients type 3 spinal cords, characterized by flattening or deformation caused by the apical concave pedicle or vertebral body, and the absence of visible CSF is at risk for IONM [11]. These findings outline a small percentage of patients with coronal deformity with high risk of IONM. But for patient with kyphotic deformity the percentage of severe spinal cord encroachment and distraction can be higher.
Originates from protruded vertebral bodies, discs, and posterior elements in each etiology, the spinal cord compression presents with various forms of compression. In extreme cases, the severe compression can cause deformation of cord and complete loss of CSF flow. Despite established knowledge of the relative location of the spinal cord in coronal deformity, its implications for in kyphotic deformities are poorly understood. Therefore, in this study, we present a novel classification of spinal cord morphology shape based on sagittal MRI to predict the risk of IONM events in patients with kyphosis.
MATERIALS AND METHODS
1. Patients
Patients who underwent surgical correction of cervicothoracic, thoracic, or thoracolumbar kyphosis in our center from July 2005 to December 2020 were recruited (Table 1). Informed consent was obtained from all patients before participation in the study. The inclusion criteria included: (1) patients without obvious scoliosis (Cobb angle < 10°); (2) with preoperative full-spine radiographs and MRIs; and (3) with IONM data including somatosensory evoked potentials (SEPs), motor evoked potentials (MEPs), free running electromyography. Patients with a history of spinal surgery, or with intraspinal lesions such as Chiari malformation, syringomyelia, tethered cord, etc. were excluded. Given the presence of preoperative neurological deficits was identified as an independent risk factor for IONM events [12,13], patients with American Spinal Injury Association (ASIA) A, B, or C were also excluded. Comorbidities were quantified for each patient based on the Charlson Comorbidity Index (CCI) [14]. The study was approved by the Institutional Review Board of Nanjing Drum Tower Hospital (2021-398-01).
2. Radiographic Parameters
The coronal Cobb angle of the main curve and sagittal global kyphosis were measured on preoperative standing whole spinal x-rays at the PACS (picture archiving and communications systems) workstation. The spinal cord compression ratio (CR) was calculated in terms of anteroposterior/laterolateral spinal cord diameter (Fig. 1) [15]. The ossification of the ligamentum flavum is also diagnosed through MRI. Preoperative MRIs were obtained within 6 months of the date of surgery. All radiographic parameters were conducted using Surgimap (v2.3.2.1). Two spinal surgeons (ZJ & JL) who were independent of the operations measured the radiographic assessments, and the mean values were calculated for analysis.
3. IONM Parameters
In our practice, IONM is routinely applied to each case with spine deformity and IONM events are documented in database. The criteria for identifying IONM events were met if one or more of the following conditions occurred: (1) SEP latency increased by more than 10%, (2) SEP amplitude decreased by over 50%, or (3) MEP amplitude decreased by more than 80% [4].
4. Classification System
We devised a simple classification system to describe the morphology of the spinal cord as seen on T2-weighted sagittal MRI (Fig. 2) [11]. Type A cord was defined as a circular/symmetric cord with visible CSF between the cord and the vertebral body. Type B cord was defined as a circular/oval/symmetric cord with no visible CSF between the vertebral body and the cord. Type C cord was defined as a spinal cord that is fattened/deformed by the vertebral body, with no visible CSF between the vertebral body and the cord. Based on type C, given the significantly elevated risk of severe spinal cord deformation or compression leading to potential neurological deficits, the spinal cord CR < 50% was further defined as the subtype C-, while the spinal cord CR ≥ 50% was defined as the subtype C+ [15-17].
5. Statistical Analysis
The Student t-test and analysis of variance were employed to evaluate discrepancies in continuous variable between the types A, B, subtypes C- and C+ spinal cord groups. Pearson test was used to compare the distribution of demographic, radiological, and surgical parameters among those with IONM alerts and those without IONM alerts. Univariate logistic regression analysis was performed to screen for potential variables related to IONM alerts. In order to avoid multicollinearity in the multivariate regression, one variable was eliminated if the Spearman correlation coefficient was > 0.5 [18]. A backward elimination method was used to exclude the nonsignificant variables. A post hoc analysis of the power of logistic regression was performed according to Faul et al. [19] All statistical analyses were performed using IBM SPSS Statistics ver. 21.0 (IBM Co., Armonk, NY, USA). A p-value of < 0.05 was considered to be statistically significant.
RESULTS
A cohort of 294 patients (186 males and 108 females) was enrolled in this study. Table 1 presents the demographic data of the included patients. The age of the participants was 30.2 years (range, 2–79 years). The etiology of kyphosis includes Scheuermann disease (n= 49), congenital kyphosis (n= 79), degenerative kyphosis (n= 17), old fracture (n= 20), spinal tuberculosis (n= 24), and ankylosing spondylitis (n= 105).
The classification of spinal cords revealed that among all cases, 73 (24.8%) were classified as type A, 153 (52.0%) as type B, 53 (18.0%) as subtype C- and 15 (5.1%) as subtype C+ spinal cords. During the corrective surgical procedures, IONM events were observed in a subset of patients. Specifically, 2 patients (2.7%) with type A spinal cords, 13 patients (8.5%) with type B spinal cords, 12 patients (22.6%) with subtype C- spinal cords, and 14 patients (93.3) with subtype C+ spinal cords experienced IONM events (p< 0.001). Notably, only 2 type B patients with OLF exhibited IONM events (Fig. 3). Additionally, 26 patients (35.6%) with type A spinal cords, 31 patients (20.3%) with type B spinal cords, 22 patients (41.5%) with subtype C- spinal cords, and 10 patients (66.7%) preoperative ASIA is D grade (p< 0.001). Moreover, the patients with type A spinal cords were found to be older compared to those with type B, subtypes C- and C+ spinal cords, with mean ages of 39.4 years versus 26.3 years, 31.3 years and 21.3 years (p< 0.001) (Table 2).
Furthermore, the spinal osteotomy grade of patients with types B and C spinal cords was significantly higher than that of patients with type A spinal cords (p< 0.001). Additionally, patients with type C spinal cords displayed a significantly larger sagittal Cobb angle (subtype C-, 83.9°; subtype C+, 93.6°), in comparison to patients with types A and B spinal cords, who had Cobb angles of 69.1° and 75.9° (p< 0.001). Notably, patients with type C spinal cords displayed a significantly larger postoperative changes in Cobb angle (subtype C-, 45.4°; subtype C+, 46.8°), in comparison to patients with types A and B spinal cords, who had 37.7° and 41.9° (p= 0.035) (Table 2).
A standardized operating procedure was implemented in response to IONM events, which included instructions to elevate mean arterial pressure to > 90 mmHg to optimize spinal cord perfusion. Any surgical corrective action corresponding to a specific warning signal was promptly reversed. A thorough assessment was conducted to identify spinal cord compression and manage additional mechanical injuries [20]. Following the resolution of IONM alerts, all patients underwent successful completion of the surgery. Subsequently, 36 of those 41 patients exhibited a return of spinal cord monitoring data to baseline after surgery. Notably, all 4 patients whose spinal cord monitoring data did not revert to baseline had a type C spinal cord. The dorsal aspect ratio (DAR) was significantly larger in type C (subtype C-, 12.8°; subtype C+, 12.7°) vs. types A (8.8°) and B (10.5°) spinal cord patients (p< 0.001) (Table 2).
We further tracked the neurological status of the 14 patients with the subtype C+, none of whom experienced worsened neurological damage postoperatively, with neurological function improving in 4 patients (Table 3). Corrective surgery was indicated in these cases to halt kyphosis correction and prevent further deterioration of neurological function.
The risk factors associated with IONM events are shown in Table 4. Pearson tests showed that sagittal DAR (p < 0.001), neurological impairment (ASIA grade D) (p < 0.001), spinal cord classification (p < 0.001), etiology (p < 0.001), and spinal osteotomy classification (p < 0.001) differed significantly between with IONM events and without IONM events groups. There was no significant association between patient’s sex, age, CCI, body mass index, main lesion site, postoperative changes in Cobb angle (Table 4). Univariate logistic regression analysis showed 4 potential risk factors, including larger sagittal DAR (75%–100%: OR, 4.583; 95% CI, 1.731–12.134, p= 0.002), preoperative neurological impairment (ASIA grade D, p< 0.001), type C spinal cord (subtype C-: OR, 10.390; 95% CI, 2.215–48.735; p = 0.003; subtype C+: OR, 497.000; 95% CI, 42.126–5,863.611; p< 0.001), higher spinal osteotomy grade (grade 4: OR, 6.375; 95% CI, 1.322–30.753; p= 0.021; grade 5: OR, 8.870; 95% CI, 2.668–29.482; p< 0.001; grade 6: OR, 5.667; 95% CI, 1.195–26.874; p= 0.029). Due to the lack of significant differences observed among various etiologies, we have opted not to include them in the multiple regression analysis (Table 4). The 4 variables with were selected for multiple logistic regression with backwards stepwise selection (Table 5). In step 1, the sagittal DAR was observed to have insignificant association with IONM events (OR, 1.204; 95% CI, 0.790–1.835; p= 0.389, multiple logistic regression). In step 2, following the removal of the insignificant variable “sagittal DAR,” spinal cord classification (OR, 5.371; 95% CI, 2.966–9.727; p< 0.001), spinal osteotomy classification (OR, 1.739; 95% CI, 1.304–2.319; p< 0.001), and preoperative ASIA score D (OR, 3.221; 95% CI, 1.376–7.538; p< 0.001) were confirmed as independent risk factors. The Cox and Snell R2 and Nagelkerke R2 of the regression model was 0.296 and 0.534, respectively.
DISCUSSION
In this study, we introduce a novel spinal cord classification system based on sagittal plane MRI for predicting the risk of IONM events in patients with kyphotic deformity. Our findings demonstrate a markedly increased risk of IONM events among patients with subtype C- spinal cord (OR, 10.390), and an even higher risk in subtype C+ (OR, 497.000) during deformity correction procedures, compared to those with a normal spinal cord morphology and CSF presence between the spinal cord and vertebral body (type A). In our multifactorial regression analysis, we have further identified the spinal cord classification as an independent risk factor. This system is a straightforward and effective approach to evaluating the hazard of neuromonitoring events before kyphosis correction. In cases with type C (including subtypes C- and C+) spinal cords, it is of paramount importance to avoid too aggressive correction of deformity. Instead, decompression of the cord and the preservation of neurological function should be prioritized.
On top of all, we identified cases with type C spinal cord had the higher risk of neurological complications. In such cases, the spinal cord is subjected to both the compression of the protruded spinal column and the distraction force that alters the regular shape of the cord. Radiographically, the preoperative radiographic parameter known as the DAR was introduced as a predictor of which patient groups were at higher risk for IONM events [7]. The DAR was determined as the coronal Cobb angle divided by the number of vertebrae encompassed within the curve. An elevated DAR value indicated a more severe, acutely angled curve with an increased likelihood of IONM changes [21-24]. Our findings indicate that patients with a type C spinal cord demonstrate a markedly larger sagittal DAR value, resulting in deformation of the spinal cord and subsequent impairment of neurological function [9,10]. Furthermore, in these cases, the distraction and torsion of the spinal cord may cause paraplegia and hypoxia of the cord [8,11]. Notably, all patients included in this study had a DAR larger than 7, indicating a severe kyphotic deformity [25]. In our multifactorial regression analysis, we have further determined that DAR is not an independent risk factor. In this particular, the relative position and morphology of the spinal cord may serve as a more relevant measure that accounts for the risk of IONM in corrective surgery than the severity of deformity.
Due to the relatively severe spinal cord compression, the incidence of IONM events in the subtype C+ case is as high as 93.3% (Table 2) [19]. Notably, we also observed some unique cases with concurrent IONM events. In 3 patients with congenital chondrodysplasia, the spinal cord was compressed by the vertebral body, with no CSF between the spinal cord and vertebral body or lamina (Fig. 4A). Two patients with ankylosing spondylitis developed idiopathic spinal cord herniation (Fig. 4B). Given that the subtype C+ spinal cord indicates a highly stretched condition, and further elevated risk of IONM based on our analysis, we believe it to be a crucial risk factor for IONM events that require our heightened vigilance.
Our analysis revealed that type B spinal cords (OR, 0.752; p= 0.564) did not exhibit a significantly elevated risk of IONM compared to type A. Our hypothesis suggests that type B spinal cords maintain regular spinal morphology and sufficient blood supply, thus minimizing the risk of injury during correction. However, our investigation revealed that IONM events occurred in only 2 type B spinal cord patients with OLF. Previous study has identified OLF as a significant risk factor for IONM events [26] and can lead to a range of postoperative complications [27-30]. Thus, it is crucial that we remain vigilant in our preparation and proactively take measures to prevent IONM events in patients with OLF.
The primary strength of this classification system is its simplicity, allowing for quick and easy assessment of spinal cord morphology on sagittal MRI preoperatively, without the need for invasive examinations. Furthermore, the identification of type C spinal cords serves as a strong indicator of the increased risk of experiencing an IONM event during deformity correction. Establishing a standardized operating procedure in response to type C spinal cord presence can facilitate prompt management of the issue through direct spinal cord decompression or by accepting a lesser curve correction [20]. Corrective surgery was indicated in these cases to prevent kyphosis worsening and further deterioration of neurological function, suggesting that patients with type C spinal cord conditions are not contraindicated for surgery. Comparatively, type A patients have a lower overall risk of IONM events. For these cases, care should be taken to restore the physiological spinal morphology, with caution paid to cases exhibiting large sagittal DAR.
We believe that this classification system is simple yet informative, providing valuable guidance for alerting the risk of neurological deficit. Furthermore, the classification system presented by Sielatycki et al. [11] could be integrated with our approach to evaluating more complex spinal deformities, thereby enabling a more comprehensive prediction of the risk of neurological complications. However, this study had some limitations, including a relatively multiple etiology and a heterogeneous population. Additionally, the number of patients with OLF was relatively small. Furthermore, the study was conducted in a single surgeon’s practice, working with experienced assistants and an intraoperative neuromonitoring team. Therefore, the results may not be generalizable to all spinal surgery practices.
CONCLUSION
Here we presented a novel sagittal MRI-based spinal cord classification system to predict the risk of IONM event in patients with kyphotic deformity. Specifically, our observations revealed that patients with type C spinal cord, particularly those with the subtype C+, are subject to a significantly elevated risk of experiencing IONM events. These findings have important implications for patients undergoing kyphosis correction, as it is imperative to prepare for potential IONM events by implementing vertebral column resection and/or circumferential spinal cord decompression. Our novel classification system explicitly outlines the different severity and pattern of spinal cord compression in the context of kyphotic deformity, thereby offering a valuable tool for clinicians to identify high-risk patients and implement appropriate surgical correction.
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