Abstract
Study Design
Prospective single institutional cohort study on Degenerative Cervical Myelopathy (DCM) from 2009 to 2022.
Objective
This study aims to assess the relationship between preoperative spinal cord signal change, postoperative signal change evolution, and functional outcome in patients undergoing surgery for DCM.
Summary of Background Data
There is conflicting evidence whether spinal cord signal intensity influences functional outcomes in patients with DCM.
Methods
This prospective study investigated 104 DCM patients that underwent both preoperative and routine postoperative cervical spine MRI as part of a research protocol. Signal intensity/grade, modified Japanese Orthopaedic Association (mJOA) scores, signal resolution, and patient demographics were assessed.
Results
Sixty-eight of the subjects were found to have abnormal T2 spinal cord signal intensity changes on their preoperative MRI. The total mean preoperative mJOA score was 13.6, increasing postoperatively to 16 (p<0.001). The presence or absence of preoperative spinal cord signal change was not associated with change in mJOA score or neurological recovery rate following surgery. Of the 68 patients with preoperative T2 signal change, 36 were found to have improvement in the T2 weighted signal grade after surgery, and 32 had no change in postoperative signal grade. The mean improvement in mJOA score (3.7) and neurological recovery rate (70.3%) was significantly higher in the patients with preoperative signal change whose postoperative MRI signal change grade improved by at least one point compared to those that did not (2.0, 50.5%), (p<0.001, p<0.003)
Conclusions
The presence of preoperative T2 weighted signal change was associated with lower preoperative mJOA scores, but not change in mJOA following surgery or postoperative neurological recovery rate. However, improvement in T2 weighted spinal cord signal grade on postoperative MRI was significantly associated with degree of neurological improvement following surgery.
Keywords: Degenerative, Spine, Myelopathy, Cervical, mJOA, MRI, Decompression
INTRODUCTION
Degenerative Cervical Myelopathy (DCM) is a progressive degenerative spine condition that results in neurological decline and affects the quality of life in up to 5% of the population [1,2]. Some controversy exists regarding the optimal management of DCM patients. Current guidelines suggest that patients with asymptomatic cervical stenosis and mild DCM can be treated nonoperatively, whereas patients with moderate and severe DCM are recommended to undergo surgical intervention [3]. This is supported by a large number of studies that have reported that surgical management improves functional, clinical, and radiographical outcomes in DCM patients [4-12].
The ability to prognosticate surgical outcomes for DCM continues to garner significant attention among spine surgeons. The prognosis can be impacted by different variables, such as age, symptom duration, preoperative symptoms and degree of spinal cord injury [13-16]. The presence of signal change has been viewed as a surrogate for spinal cord injury, and there has been a continued interest in determining the effect of spinal cord signal change and intensity on clinical outcomes and prognosis following surgery [14,15].
Neurological status is optimally assessed using validated outcome measures such as the mJOA to help determine which patients are suitable for surgery [4,11,12]. MRI is a valuable tool because it not only visualizes the magnitude of spinal cord compression, but the presence and intensity of intramedullary spinal cord signal change [15,16]. The relationship between MRI signal intensity and functional outcomes has been examined, however the evidence is conflicting. While some studies have shown that T2-hyperintensity is not a prognostic indicator, other studies have noted a correlation between increased cord signal and reduced functional outcomes [17-21].
This study aims to further evaluate the relationship between spinal cord signal change and clinical outcome, by contrasting preoperative and postoperative signal change evolution following surgery using functional outcome measures.
MATERIALS and METHODS
Study Design & Outcome Measures
A total of 104 DCM patients were prospectively enrolled in a cross-sectional observational study pairing preoperative and postoperative MR imaging with clinical assessment. All patients signed Institutional Review Board-approved consent forms, and all analyses were performed in compliance with the Health Insurance Portability and Accountability Act (HIPAA).
The cohort was comprised of 67 men and 37 women, with a mean age of 65 years (ranging from 39 to 92). The modified Japanese Orthopedic Association (mJOA) score was used to evaluate neurological function. The patient demographic data is summarized in Table 1. Variables of interest include: demographics, preoperative signal grade/intensity, preoperative mJOA scores, as well as any improvement in mJOA score quantitatively or cord signal via resolution postoperatively.
Table 1.
Patient Demographics and Group Outcomes
| Surgical Management of DCM (n=104) |
|
|---|---|
| Average Age (years) | 65 (Min: 39; Max: 92) |
| Gender | Female: 36% (n=37) Male: 64% (n=67) |
| Presence of Cord Signal on T2-weighted MRI | ~65% (n=68) |
| Average preoperative mJOA Score | 13.6 (Min: 8; Max: 18) |
| Average postoperative mJOA | 16 (Min: 11; Max: 18) |
The patients underwent cervical spine MRI and neurological assessment at baseline and three months postoperatively. Signal intensity was graded on MRI based on the Applebaum classification: Grade 0 – no signal change, 1 – slight/fine-point, 2 – moderate/uniform/dull, 3 – intense/bright, 4 – very intense [22]. Subgroup analysis was conducted to assess for improvement in signal grade, evidence signal resolution, and mJOA score alterations postoperatively.
Neurological recovery rate percentage was determined using the formula described by Hirabayshi et al. [23]: postoperative JOA Score – preoperative JOA Score/Full score – preoperative JOA score X 100 (%).
Operative Treatment
The senior author (LTH) performed all of the surgical procedures. The factors that influenced the choice of surgical approach included preoperative spinal alignment, number of levels requiring decompression, patient age, presence of instability on flexion-extension, and the need for motion preservation based on patient occupation or lifestyle. Although each surgical approach was individually decided between the senior author and the patient, several principles were weighed in each case. In general, anterior approaches were utilized for patients with kyphotic spinal alignments or when the anterior compression was so significant that a posterior approach would not allow for adequate decompression. A corpectomy was selected rather than ACDF when the compression extended above or below the disc space, and it was felt that removal of the entire vertebral body was needed to achieve adequate decompression. Posterior approaches were most frequently utilized in cases requiring three levels or more of decompression with straight or lordotic spinal alignments. Of the posterior approaches, laminoplasty was selected in patients when relatively normal preoperative motion was present, and the need for motion preservation due to occupational and lifestyle concerns was a significant priority. Laminectomy without fusion was considered an option in elderly patients with ankylosed spines. Using these general considerations, 64 patients underwent cervical laminectomy and fusion, 24 patients had a laminoplasty performed, 1 had a laminectomy , 11 underwent an anterior cervical discectomy and fusion (ACDF), and 4 had an anterior cervical corpectomy. The mean number of cervical levels involved in surgical decompression was 3 (range: 1-7).
Cervical Spine MRI
Cervical spine MRI without contrast was obtained on a 3T MR scanner (3T Prisma; Siemens Healthcare, Erlangen, Germany). Each of the MRI scans had a formal imaging read by one of our attending neuroradiologists that had at least five years of experience. These neuroradiologists were blinded to study subjects, focusing only on clinical interpretations based on their independent expertise. Additionally, two members of the investigative team reviewed the same images conjointly. Between the team members and the attending neuroradiologist interpretations, the interobserver coefficient was noted to be 0.947.
Statistical Analysis
Chi-squared and t-tests were used for comparative analyses using two-tailed methods for categorical and continuous variables, respectively. Regression analysis was used to explore the functional relationship between cord signal, mJOA scores and the outcomes of interest while controlling for other confounders. Significance was determined as p<0.05. Analyses were carried out using STATA software (StataCorp. 2019. Stata Statistical Software: Release 16. College Station, TX: StataCorp LLC.).
RESULTS
Preoperative Status
The mean mJOA score of the cohort was 13.6 (range of 8 to 18). Sixty-eight patients (65%) had evidence of T2 weighted signal change on their preoperative MRI. Forty-one of the patients had Applebaum Grade 1 signal change, seventeen had Grade 2, eight had Grade 3, and two had Grade 4 (Table 2). Sixty-three patients had the signal intensity at a single level, and 5 had the signal change at multiple levels. Patients with preoperative spinal cord signal change had significantly lower mJOA scores than those that did not (13.1 vs 14, P < 0.0001).
Table 2.
Preoperative Signal Intensity Grading Scale Comparison
| Grade* | Surgical Management of DCM (n=104)* |
|---|---|
| 0 | ~35% (n=36) |
| 1 | ~39% (n=41) |
| 2 | ~16% (n=17) |
| 3 | ~8% (n=8) |
| 4 | ~2% (n=2) |
utilizing the Applebaum grade scale for cord signal intensity on MRI
Postoperative findings
Significant neurological improvement was found following surgery (p < 0.001, Figure 1), as the DCM patients mean postoperative mJOA score was 16 (range of 11 to 18) compared to 13.4 before surgery. The Hirabayashi mJOA Recovery Rate Percentage on average was 63.09% after surgical intervention (Range: 0% to 100%, Median 67%). Of the 68 patients with preoperative T2 weighted spinal cord signal change, 36 patients obtained improvement in their postoperative MRI Applebaum signal change grade (Figure 1). Subgroup analysis in this cohort identified a mean preoperative to postoperative mJOA score improvement of 3.7 (12.7 to 16.4, p <0.001) when signal grade improved by at least one grade following surgery (Table 3). Furthermore, recovery percentage for this group was 70.3%. In contrast, the 32 patients that did not improve their signal grade achieved a mean postoperative mJOA increase of 1.8 (13.5 to 15.3 p<0.001). This change in mJOA score following surgery was significantly lower when compared to the group that improved signal after surgery (2 vs. 3.7, p<0.001) (Table 4). Similarly, neurological recovery rate percentage was also significantly lower in patients that did not obtain improvement in spinal cord signal change compared to those that did. (50.5% vs 70.3%, p=0.003). Twenty patients had resolution of their T2 weighted signal change on postoperative MRI: 19 of these were preoperative Applebaum grade 1, and one was preoperative Applebaum grade 2. Recovery percentage for this group was 70%, with no significant difference noted when compared to the group that improved signal by one grade or more. However, a significant difference was noted in recovery percentage for who did not improve their signal change postoperatively compared to those who resolved the signal change (50.5% vs 70%, p=0.015).
Figure 1: Preoperative to Postoperative Cord Signal Resolution on MRI.
The patient is a 57-year-old male whom underwent a C5-7 laminectomy and fusion. (A) Preoperative T2-weighted sagittal cervical spine MRI noting cord signal intensity (Grade 4). (B) T2-weighted axial image of the same region of the spine. (C) Postoperative T2-weighted image noting cord signal reduction (Grade 2). (D) Same level axial cut notes signal improvement as well. The mJOA score improved from 13 to 18 before and after surgery respectively.
Table 3.
Surgical Subgroup Analysis
| Pre-operative mJOA | Post-operative mJOA |
p-Value | |
|---|---|---|---|
| Preoperative Signal Presence | 13.1 | 15.9 | <0.001 |
| Preoperative Signal Absence | 14 | 16.1 | <0.001 |
| Signal Presence | Signal Absence | p-Value | |
| ΔmJOA | 2.8 | 2.1 | 0.041 |
| Recovery Rate (%) | 61.8 | 65.5 | 0.267 |
| Pre-operative mJOA | Post-operative mJOA |
p-Value | |
| Preoperative Signal Grade 1* | 13 | 15.6 | <0.001 |
| Preoperative Signal Grade 2* | 13.4 | 16.7 | <0.001 |
| Preoperative Signal Grade 3* | 13 | 15.6 | 0.001 |
| Preoperative Signal Grade 4*+ | 12.5 | 16 | 0.232 |
| Signal Resolution After Surgery (n=22) | 13.1 | 16.4 | <0.001 |
| Signal Improvement by 1 Grade Point or more After Surgery (n=36)* | 12.7 | 16.4 | <0.001 |
utilizing the Applebaum grade scale for cord signal intensity on MRI
Total Number (n) is 2
Table 4.
Signal Presence Subgroup Comparisons: Regression Analyses
| Variables of Interest* |
Groups | Values | p-Value |
|---|---|---|---|
| ΔmJOA | Signal Resolution | 3.3 | 0.040 |
| No Signal Resolution | 2.4 | ||
| Signal Improvement 1-Grade Point or more | 3.7 | <0.001 | |
| No Improvement | 2 | ||
| Recovery Rate (%) | Signal Resolution | 69.9 | 0.195 |
| No Signal Resolution | 61.3 | ||
| Signal Improvement 1-Grade Point or more | 70.3 | 0.003 | |
| No Improvement | 50.5 |
All controlling for Age, Gender, and Race.
Regression analyses noted overall consistent findings when controlling for confounders including gender, race/ethnicity, and age. The differences in preoperative mJOA scores in those with preoperative signal change remained lower than those without preoperative signal change (p=0.042). However, postoperative mJOA, ΔmJOA (difference between preoperative and postoperative scores), and recovery rate were not significantly different between those with and without preoperative T2 weighted signal change.
DISCUSSION
The primary purpose of this study was to determine if preoperative T2-weighted spinal cord signal intensity and postoperative signal change evolution can influence prognosis and functional outcomes in those with DCM. To date, the current literature is conflicted on whether signal change should be used as a prognostic indicator or not. We predicted that both mJOA scores and cord signal intensity could be used to predict prognosis. We subsequently identified clinically significant relationships between mJOA and signal intensity noted on T2-weighted MR imaging.
Of the 104 patients included in this study, an average preoperative mJOA score of 13.6 signficantly improved to 16 following decompressive surgery. Of the 68 patients with preoperative signal change, 36 patients improved signal grade by at least one point, with an average improved mJOA score postoperatively by 3.7. Furthermore, mJOA improved postoperatively, independently from preoperative signal presence and grade; supporting the current state of the literature [1-13]. Commonly, mJOA scores serve to gauge the necessity of surgical intervention [8,9,11]. Several studies have noted that cord signal change and intensity influence the need for surgical intervention [13-16]. However, some believe that there is no merit to this argument, stating that signal change is not a prognostic indicator nor surgical determinant [17].
Our study noted significant differences in signal intensity presence and grade, supporting the majority of evidence presented in the literature. Those managed operatively were noted to have preoperative signal change in the spinal cord 65% of the time. In addition, the findings above, increases in postoperative mJOA scores were significantly influenced by cord signal T2 resolution and signal improvement by one graded level. The presence or absence of T2 signal change was associated with a change in mJOA after surgery. This is likely due to the fact that patients with preoperative signal presence had a lower preoperative mJOA score; rather than the presence or absence of signal acting as an independent predictor of improvement postoperatively. This is evidenced by the fact that recovery rate was not significantly different, which takes into consideration the preoperative mJOA score when calculating the degree of improvement. Moreover, on regression analysis, the presence or absence of T2 signal change was not associated with a change in mJOA score postoperatively, further supporting the finding that preoperative signal presence was not a predictor. This could be due to the fact that patients recovered to similar levels of functionality postoperatively, while starting more debilitated on average preoperatively. Nonetheless, spinal cord signal presence/intensity can be used to predict surgical outcome in patients with DCM as signal regression predicts improved postoperative functional outcomes.
As for prognostic applicability of cord signal presence and intensity on T2-weighted imaging, regression analysis was conducted. (1) With respect to preoperative mJOA score, differences between cohorts those with signal and without signal change held true. (2) Improvements in spinal cord signal postoperatively are clinically important as the majority of subjects with DCM have graded signal intensity and could benefit from intervention. (3) Complete resolution of signal change and improvement of signal change were both associated with better neurological recovery following surgery than patients that did not have any improvement in spinal cord signal change. In fact, the improvement in mJOA score was more than twice as high in those who improved their signal grade postoperatively and the patients that did not. Interestingly, there was no difference in outcome between patients that simply improved their spinal cord signal change compared to those that had complete resolution. Thus, it appears that any improvement in signal change is more critical to prognosis than the actual magnitude. These critical findings were not influenced by age, sex or race/ethnicity. Given that mJOA can be used as a prognostic indicator, this correlation suggests that spinal cord signal intensity and presence noted on T2-weighted MR imaging can be utilized similarly in clinical practice.
There are several noteworthy limitations in the study. (1) The single-center prospective cross-sectional observational nature of this study is a limitation itself, not only limiting sample size/demographics, but also power analysis. (2) No standardized quantitative methodology exists to grade signal change intensity. The Applebaum classification was utilized in this study [22]. This system is subject to observer bias.
Conclusion
The presence of preoperative T2 weighted signal change was associated with lower preoperative mJOA scores, but not change in mJOA following surgery or postoperative neurological recovery rate. However, improvement in T2 weighted spinal cord signal grade on postoperative MRI was significantly associated with degree of neurological improvement following surgery.
Acknowledgements
We would like to acknowledge the contributions of author GKF. We hope that this posthumous study is well received and a contribution to his legacy. We would also like to thank the Departments of Neurosurgery, Orthopaedic Surgery, and Radiology at the David Geffen School of Medicine at the University of California Los Angeles.
Funding
NIH Research Grants:
R21 NS065419
R01 NS078494
Footnotes
Institutional Review Board Statement
Ethical review and approval were obtained via an expedited review. IRB#16-000409
Informed Consent
Informed consent was obtained from all subjects involved in the study.
Conflicts of Interest
The authors state that there are no conflicts of interest nor disclosures pertaining to this study.
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