Eur Spine J DOI 10.1007/s00586-015-4109-5
ORIGINAL ARTICLE
Predictors of surgical outcome in cervical spondylotic myelopathy: focusing on the quantitative signal intensity Jing Tao Zhang1 • Fan Tao Meng1 • Shuai Wang1 • Lin Feng Wang1 Yong Shen1
•
Received: 15 May 2015 / Revised: 1 July 2015 / Accepted: 1 July 2015 Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose The association between intramedullary increased signal intensity (ISI) on T2-weighted magnetic resonance imaging and surgical outcome in cervical spondylotic myelopathy (CSM) remains controversial. The purpose of this study is to assess the impact of quantitative signal change ratio (SCR) on the surgical outcome for CSM. Methods The prospective study included 108 consecutive patients who underwent surgical treatment for CSM. The Japanese Orthopaedic Association (JOA) score and recovery rate were used to evaluate clinical outcomes. JOA recovery rate less than 50 % was defined as a poor clinical result. The SCR was defined as the signal intensity at the level of ISI or severely compressed cord (in cases with no ISI) divided by the signal intensity at the C7–T1 disc level. Age, sex, body mass index, duration of symptoms, surgical technique, preoperative JOA score, levels of compression, preoperative SCR, preoperative C2–7 angle, preoperative C2–7 range of motion were assessed. Results Forty patients (37.0 %) had a recovery rate of less than 50 %. Multivariate logistic regression analysis revealed that a higher preoperative SCR and a longer duration of symptoms were significant risk factors for a poor clinical outcome. Receiver operating characteristic
J. T. Zhang and F. T. Meng contributed equally to this work. J. T. Zhang and F. T. Meng should be considered co-first authors. & Yong Shen [email protected] 1
Department of Spinal Surgery, The Third Hospital of Hebei Medical University, No. 139 Ziqiang Road, Shijiazhuang 050051, Hebei, People’s Republic of China
(ROC) curve analysis showed that the optimal preoperative SCR cutoff value as a predictor of poor clinical result was 1.46. The area under the ROC curve of preoperative SCR for predicting a poor surgical outcome was 0.844. Conclusions Preoperative SCR significantly reflected the surgical outcome in patients with CSM. Patients with SCR greater than or equal to 1.46 can experience poor recovery after surgery. Keywords Cervical spondylotic myelopathy Intramedullary spinal cord signal intensity Magnetic resonance imaging Prognosis Quantitative analysis
Introduction Cervical spondylotic myelopathy (CSM) is one of the most common causes of spinal cord dysfunction in the elderly population. The disease usually has an insidious course and a slow stepwise deterioration in neurological function [1]. However, approximately 5 % of patients present with a dramatic and rapid functional decline [2]. In case of severe spinal cord compression or a progressive course, operative decompression is the accepted treatment for CSM. Although there is emerging evidence that most patients improve after surgical treatment, the key clinical and imaging factors that predict the surgical outcome remain uncertain. Magnetic resonance imaging (MRI) is a valuable tool before surgical decompression because it visualizes not only the magnitude of cervical spinal cord compression but also intramedullary signal intensity. The presence of intramedullary high signal intensity on T2-weighted MRI in patients with CSM reflects chronic spinal cord compression lesion. However, the significance of increased
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Eur Spine J
signal intensity (ISI) on T2-weighted imaging (WI) for prognosis remains controversial [3–12]. Definitive information is not available because most descriptions of signal changes are qualitative in nature. Based on the previous studies [13, 14], we used signal change ratio (SCR) to quantitatively assess the changes of signal intensity. The aim of this study is to assess the risk factors associated with poor recovery outcome, particularly the predictive value of quantitative SCR, after surgical treatment for CSM and ascertain the crucial determinants of surgical outcome using statistical analyses.
Materials and methods Patient population The research protocol was approved by the Research and Ethics Committee of The Third Hospital of Hebei Medical University, and all patients gave written informed consent for their information to be stored in the hospital database and used for research. A total of 178 consecutive patients with CSM were prospectively enrolled from January 2011 to January 2012. Sixty-two patients who had asymptomatic cervical cord compression, active infection, trauma, neoplastic disease, rheumatoid arthritis, previous surgery for CSM, cervical ossification of the posterior longitudinal ligament, and concomitant symptomatic lumbar spinal stenosis, or other neurological disorders were excluded from this study. An additional of 8 patients were lost to follow-up within the 12 months after surgery because of various reasons unrelated to their CSM. The remaining 108 patients who could be tracked for more than 12 months after surgery were included in this study. Diagnoses were confirmed by neurological examinations and imaging studies such as X-rays radiographs and MRI. Neurological assessment The preoperative and postoperative neurological function 12 months after surgery was assessed using Japanese Orthopaedic Association (JOA) score. The recovery ratio of JOA score was calculated using Hirabayashi’s method [15] and was based on the following formula: recovery rate = (postoperative JOA score-preoperative JOA score/ 17-preoperative JOA score) 9 100 %. The 12-month time frame was chosen because it represents a typical time period of optimum recovery after operation for CSM [16, 17]. Recent study-reported clinical results were divided into 4 groups as follows: 75 % or higher (excellent), 50–74 % (good), 25–49 % (fair), and less than 25 % (poor) [18]. Therefore, we defined a poor clinical outcome as a recovery rate less than 50 % in this study.
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Radiographic assessment The C2–7 angle was measured between the posterior border of the C2 vertebral body and posterior border of the C7 vertebral body on lateral radiographs with patients in a neutral position. The Cobb method was used to measure the C2–7 ROM through the change in the maximal flexion and extension by lateral radiographic view. All patients underwent high-resolution MRI with a 1.5-T system (Siemens Magnetom Symphony) before surgery. MRI of the cervical spinal cord were obtained using a spin echo sequence system for T1-weighted images (T1WIs) and a fast spin echo sequence system for T2-weighted images (T2WIs). A surface coil was used. The slice width was 4 mm, and the acquisition matrix was 512 9 256. The sequence parameters for T1WIs were a repetition time (TR) of 612 ms and an echo time (TE) of 13 ms; for T2WIs, a TR of 2400 ms and a TE of 114 ms was used. The high signal intensity values of the cervical spinal cord on sagittal T2WIs were obtained, and the regions of interest (ROIs) were taken by 0.05 cm2. The normal spinal cord signal intensity values on sagittal T2WIs were obtained at C7–T1 disc levels, and the ROIs were taken by 0.3 cm2. If no intramedullary high-signal intensity on T2WIs was noted, the ROIs will be taken by 0.05 cm2 of the severely compressed cord. The SCR was defined as the signal intensity at the level of ISI or severely compressed cord (in cases with no ISI) divided by the signal intensity at the C7–T1 disc level. Signal intensity value was measured on the MRI workstation and the SCR was calculated. Choosing ROIs is due to a balance of a number of factors. For instance, extremely large area would not hold all patients in the group; whereas extremely small area would jeopardize the accuracy of the signal intensity value. Statistical analysis Descriptive analysis for the patient population was conducted using means and standard deviations (SD) for continuous variables and frequencies and percentages for categorical variables. Inferential statistics were performed to assess the association between the independent risk factors and recovery status using independent Student t tests for continuous variables and Chi squared or Fisher’s exact tests to analyses categorical variables. Multivariate logistic regression analysis was also performed to control for potential confounding variables with the end point of ‘poor recovery after surgery’. Adjusted odds ratios (OR) with 95 % confidence intervals (CI) were presented with their respective p values. Factors with a p value of less than 0.20 in univariate analysis were entered into the multivariate logistic model. Receiver operating characteristic (ROC) curve was constructed to evaluate the sensitivity
Eur Spine J
and specificity of SCR in predicting poor clinical result after surgery. p \ 0.05 was considered to represent a statistically significant difference. All analyses were performed using SPSS software (version 21.0; SPSS Inc, Chicago, IL).
Results The patient characteristics were shown in Table 1. There were 65 men and 43 women; mean age at surgery was 66.0 years (range 38–84 year). The average JOA score was 10.0 points (range 6–15) before surgery and 13.7 points (range 6–17) 12 months after surgery. The JOA recovery rate averaged 53.9 % (range 0–100 %); 68 patients had good clinical outcomes, with recovery rates greater than or equal to 50 %, while 40 patients had poor clinical outcomes with recovery rates less than 50 %. Twenty-eight patients had diabetes mellitus. The average preoperative JOA scores for the good recovery group and poor recovery group were not significantly different (10.2 vs 9.7, p = 0.292). The postoperative JOA score was significantly improved in the good recovery group compared with the poor recovery group at 12 months after surgery (14.7 vs 11.9, p \ 0.001). There were no significant differences between the two groups regarding the sex, BMI, diabetes mellitus. The anterior approach (discectomy or corpectomy with fusion) for decompressive surgery was performed in 70 patients, posterior approach (either laminectomy and fusion or laminoplasty) was performed in 29 patients, and combination of both anterior and posterior approaches was Table 1 Comparison of patient characteristics between good and poor recovery groups
performed in 9 patients. All patients had adequate cervical spinal cord decompression as confirmed by MRI at 6 months after surgery. None of them required revision surgery for inadequate cervical spinal cord decompression. There were no significant differences in the type of surgical procedure and levels involved between the two groups (p = 0.208, p = 0.515, respectively). The age at operation in the poor recovery group was significantly older than in the good recovery group (68.6 vs 64.5 year, p = 0.021). The duration of symptoms was significantly longer in the poor recovery group compared with the good recovery group (20.9 vs 10.2 mo, p \ 0.001). The preoperative C2–7 angle was similar in the two groups (16.2° vs 15.7°, p = 0.668). Regarding dynamic factors of the cervical spine, there was no significant difference in the preoperative C2–7 ROM between the two groups (16.9° vs 17.3°, p = 0.807). The SCR was significantly greater in the poor recovery group than in the good recovery group (1.65 vs 1.30, p \ 0.001). From univariate analysis, three variables were selected for multivariate regression: age, duration of symptoms and SCR. The multivariate logistic regression analysis revealed that the odds of a poor clinical outcome were greater when the patient had a higher preoperative SCR (OR 6.02, p = 0.001) and had a longer duration of symptoms (OR 3.63, p \ 0.001, Table 2). The ROC analysis showed that the optimal cutoff value of preoperative SCR as a predictor of poor clinical result was 1.46, which maximized the sum of the sensitivity and specificity (Fig. 1). The area under the ROC curve of preoperative SCR for predicting poor clinical outcome was 0.844 (95 % CI 0.771–0.917; p \ 0.001).
Variable
Good (n = 68)
Poor (n = 40)
p value
Age at operation (year)
64.5 ± 9.5
68.6 ± 7.6
0.021
Female sex (n, %)
28 (41.2 %)
15 (37.5 %)
0.706
BMI (kg/m2)
25.7 ± 3.0
25.0 ± 4.4
0.342
Diabetes mellitus (n, %) Duration of symptoms (mo)
20 (29.4 %) 10.2 ± 7.5
8 (20.0 %) 20.9 ± 15.8
Preoperative JOA score
10.2 ± 2.5
9.7 ± 2.2
JOA score at 12-month follow-up
14.7 ± 1.1
11.9 ± 2.4
\0.001
Recovery rate (%)
66.8 ± 10.5
32.0 ± 11.9
\0.001 \0.001
0.281 \0.001 0.292
SCR
1.30 ± 0.16
1.65 ± 0.37
C2–7 angle (°)
16.2 ± 5.7
15.7 ± 6.5
0.668
C2–7 ROM (°)
16.9 ± 10.0
17.3 ± 6.2
0.807
Levels involved
2.1 ± 1.0
1.9 ± 1.1
0.515
Anterior
40
30
0.208
Posterior
22
7
Combined anterior/posterior
6
3
Surgical approach
BMI body mass index, JOA Japanese Orthopaedic Association, SCR signal change ratio, ROM range of motion
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Eur Spine J Table 2 Risk factors for poor outcome after operation: multiple logistic regression analysis Variablea
OR (95 % CI)
p value
Age at operation (year)
1.05 (0.98–1.12)
0.134
Duration of symptoms (mo)
3.63 (1.82–7.19)
0.000
SCR
6.02 (2.19–16.54)
0.001
SCR signal change ratio, CI confidence interval a
Duration of symptoms: 1, B3 mo; 2, [3 but B6 mo; 3, [6 but B12 mo; 4, [12 but B24 mo; 5, [24 mo. SCR: 1, [1.00 but B1.50; 2, [1.50 but B2.00; 3, [2.00 but B2.50; 4, [2.50
Fig. 1 ROC curves showed that optimal cutoff value of SCR for prediction of a poor clinical outcome
Discussion The elucidation of factors that contribute to prognosis of patients with CSM has been investigated by several groups [10, 19–22]. Recognition of the best timing for surgery to ensure neurological recovery is an important clinical issue. Up to now, numerous factors have been reported to affect postoperative outcomes in patients with CSM. Age [20], duration of myelopathic symptoms [4, 10, 20, 21, 23], signal intensity changes on preoperative MRI [5, 7, 8, 24], and preoperative JOA score have been considered key predictors. However, the list of predictive factors differs according to researchers, and the prognostic significance of these factors remains controversial. ISI of the cervical spinal cord on T2-weighted MRI is often observed in patients with CSM, and various authors have speculated on its histopathologic significance and impact on surgical outcome. ISI on T2WI indicates local
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pathologic changes in the spinal cord, and patients with CSM and high signal intensity on T2WI usually have a poor prognosis even after surgical intervention [3–7]. AlMefty et al. [25] reported that high signal change on T2WI reflected myelomalacia, and that low signal change on T1WI indicated cystic necrosis or secondary syrinx. Yukawa et al. [26] indicated that preoperative ISI in T2WI was correlated with age, duration of symptoms, postoperative JOA score, and recovery rates, and predicted a poor outcome, especially intense ISI. Despite such evidence, many studies found no correlation between surgical outcome and intramedullary ISI on T2WI [8–12, 27, 28]. What is the reason for this observation? The following may explain this phenomenon. Although MRI provides high specificity in the assessment of morphologic changes and intramedullary changes of the cervical spinal cord, it is almost impossible to estimate potential recovery of the cervical spinal cord on preoperative MRI without appropriate quantitative analysis. We consider that ISI is a variant with large range and it usually covers a huge range of actual severity. If only focusing on the patients with ISI or not, it will bias the result due to possible judgment errors by each investigator. Considering these factors, in this study, signal change was evaluated with a focus on quantitative approaches. SCR was a quantitative method to assess the changes of signal intensity, which was described in previous studies [13, 14]. We found that preoperative SCR was an independent predictor of surgical outcome. In the statistic analysis, we categorized SCR into four groups: 1.50 or less, more than 1.50–2.00, more than 2.00–2.50, and more than 2.50. Specifically, the odds of a poor outcome were 6.02 times of greater for every half-point increase in the preoperative SCR. Then, we calculated that the optimal cutoff value of SCR as a predictor of poor outcome after surgery was 1.46. As far as we know, this study first reported that patients with SCR greater than or equal to 1.46 can predict poor recovery after surgical treatment for CSM. Therefore, recognition of SCR contributes significantly to the determination of the most appropriate timing for surgery. Moreover, duration of symptoms was another independent predictive factor affecting clinical outcome after surgery. The odds of a poor outcome were 3.63 times greater for patients with more than 3–6 months of symptoms than for those with 3 months or less of symptoms. The rationale is that long-standing and chronic compression of the spinal cord may lead to irreversible damage due to demyelination and necrosis of the gray matter. The current study demonstrated that patients age in the poor outcome group was significantly older than that in the good recovery group (p = 0.021). Age was also selected to multivariate logistic analysis. However, after adjustments for SCR and duration of symptoms, age showed a trend toward mild, but not significant, association with poor outcome. Although most surgeons will not discriminate on the basis of age, they
Eur Spine J
should be aware that elderly patients may translate a poor neurological recovery. However, patient demographic variables, such as gender, BMI and diabetes mellitus did not influence the improvement with surgical intervention. The C2–7 angle, C2–7 ROM, levels of compression and surgical approach did not correlate with clinical outcome. There are several limitations need to be considered in our study. First, this study was a single-center design and involved only a limited number of patients. Second, each high-resolution MRI system has different characteristic and working parameter. Therefore, these limitations suggest that further study of these questions is needed.
Conclusions Quantification of signal intensity in patients with CSM was used in the present study to assess the impact of intramedullary signal change on the surgical outcome. Preoperative SCR on MRI could be potentially useful for prediction of the surgical outcome in patients with CSM. Patients with SCR greater than or equal to 1.46 can experience poor recovery after surgery. Acknowledgments statistical analysis.
We thank Dr. Jie Li for his assistance in the
Conflict of interest The authors declare that they have no conflicts of interest concerning this article.
References 1. Clark CR (1988) Cervical spondylotic myelopathy: history and physical findings. Spine 13:847–849 2. Clarke E, Robinson PK (1956) Cervical myelopathy: a complication of cervical spondylosis. Brain 79:483–510 3. Mehalic TF, Pezzuti RT, Applebaum BI (1990) Magnetic resonance imaging and cervical spondylotic myelopathy. Neurosurgery 26:217–226 4. Okada Y, Ikata T, Yamada H et al (1993) Magnetic resonance imaging study on the results of surgery for cervical compression myelopathy. Spine 18:2024–2029 5. Matsuda Y, Miyazaki K, Tada K et al (1991) Increased MR signal intensity due to cervical myelopathy. Analysis of 29 surgical cases. J Neurosurg 74:887–892 6. Suri A, Chabbra RP, Mehta VS et al (2003) Effect of intramedullary signal changes on the surgical outcome of patients with cervical spondylotic myelopathy. Spine J 3:33–45 7. Takahashi M, Yamashita Y, Sakamoto Y et al (1989) Chronic cervical cord compression: clinical significance of increased signal intensity on MR images. Radiology 173:219–224 8. Morio Y, Teshima R, Nagashima H et al (2001) Correlation between operative outcomes of cervical compression myelopathy and mri of the spinal cord. Spine 26:1238–1245 9. Yone K, Sakou T, Yanase M et al (1992) Preoperative and postoperative magnetic resonance image evaluations of the spinal cord in cervical myelopathy. Spine 17:S388–S392 10. Wada E, Yonenobu K, Suzuki S et al (1999) Can intramedullary signal change on magnetic resonance imaging predict surgical outcome in cervical spondylotic myelopathy? Spine 24:455–461
11. Alafifi T, Kern R, Fehlings M (2007) Clinical and MRI predictors of outcome after surgical intervention for cervical spondylotic myelopathy. J Neuroimaging 17:315–322 12. Mastronardi L, Elsawaf A, Roperto R et al (2007) Prognostic relevance of the postoperative evolution of intramedullary spinal cord changes in signal intensity on magnetic resonance imaging after anterior decompression for cervical spondylotic myelopathy. J Neurosurg Spine 7:615–622 13. Zhang YZ, Shen Y, Wang LF et al (2010) Magnetic resonance T2 image signal intensity ratio and clinical manifestation predict prognosis after surgical intervention for cervical spondylotic myelopathy. Spine 35:E396–E399 14. Wang LF, Zhang YZ, Shen Y et al (2010) Using the T2-weighted magnetic resonance imaging signal intensity ratio and clinical manifestations to assess the prognosis of patients with cervical ossification of the posterior longitudinal ligament. J Neurosurg Spine 13:319–323 15. Hirabayashi K, Miyakawa J, Satomi K et al (1981) Operative results and postoperative progression of ossification among patients with ossification of posterior longitudinal ligament. Spine 6:354–364 16. Furlan JC, Kalsi-Ryan S, Kailaya-Vasan A et al (2011) Functional and clinical outcomes following surgical treatment in patients with cervical spondylotic myelopathy: a prospective study of 81 cases. J Neurosurg Spine 14:348–355 17. Cheung WY, Arvinte D, Wong YW et al (2008) Neurological recovery after surgical decompression in patients with cervical spondylotic myelopathy—a prospective study. Int Orthop 32:273–278 18. Tani T, Ushida T, Ishida K et al (2002) Relative safety of anterior microsurgical decompression versus laminoplasty for cervical myelopathy with a massive ossified posterior longitudinal ligament. Spine 27:2491–2498 19. Uchida K, Nakajima H, Sato R et al (2005) Multivariate analysis of the neurological outcome of surgery for cervical compressive myelopathy. J Orthop Sci 10:564–573 20. Fujiwara K, Yonenobu K, Ebara S et al (1989) The prognosis of surgery for cervical compression myelopathy. An analysis of the factors involved. J Bone Joint Surg Br 71:393–398 21. Koyanagi T, Hirabayashi K, Satomi K et al (1993) Predictability of operative results of cervical compression myelopathy based on preoperative computed tomographic myelography. Spine 18:1958–1963 22. Singh A, Crockard HA, Platts A et al (2001) Clinical and radiological correlates of severity and surgery-related outcome in cervical spondylosis. J Neurosurg 94:189–198 23. Matsuyama Y, Kawakami N, Mimatsu K (1995) Spinal cord expansion after decompression in cervical myelopathy. Investigation by computed tomography myelography and ultrasonography. Spine 20:1657–1663 24. Takahashi M, Sakamoto Y, Miyawaki M et al (1987) Increased MR signal intensity secondary to chronic cervical cord compression. Neuroradiology 29:550–556 25. Al-Mefty O, Harkey LH, Middleton TH et al (1988) Myelopathic cervical spondylotic lesions demonstrated by magnetic resonance imaging. J Neurosurg 68:217–222 26. Yukawa Y, Kato F, Yoshihara H et al (2007) MR T2 image classification in cervical compression myelopathy: predictor of surgical outcomes. Spine 32:1675–1678 27. Chen CJ, Lyu RK, Lee ST et al (2001) Intramedullary high signal intensity on T2-weighted MR images in cervical spondylotic myelopathy: prediction of prognosis with type of intensity. Radiology 221:789–794 28. Okais N, Moussa R, Hage P (1997) Value of increased MRI signal intensity in cervical arthrosis in myelopathies. Neurochirurgie 43:285–290
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ORIGINAL ARTICLE
Predictors of surgical outcome in cervical spondylotic myelopathy: focusing on the quantitative signal intensity Jing Tao Zhang1 • Fan Tao Meng1 • Shuai Wang1 • Lin Feng Wang1 Yong Shen1
•
Received: 15 May 2015 / Revised: 1 July 2015 / Accepted: 1 July 2015 Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose The association between intramedullary increased signal intensity (ISI) on T2-weighted magnetic resonance imaging and surgical outcome in cervical spondylotic myelopathy (CSM) remains controversial. The purpose of this study is to assess the impact of quantitative signal change ratio (SCR) on the surgical outcome for CSM. Methods The prospective study included 108 consecutive patients who underwent surgical treatment for CSM. The Japanese Orthopaedic Association (JOA) score and recovery rate were used to evaluate clinical outcomes. JOA recovery rate less than 50 % was defined as a poor clinical result. The SCR was defined as the signal intensity at the level of ISI or severely compressed cord (in cases with no ISI) divided by the signal intensity at the C7–T1 disc level. Age, sex, body mass index, duration of symptoms, surgical technique, preoperative JOA score, levels of compression, preoperative SCR, preoperative C2–7 angle, preoperative C2–7 range of motion were assessed. Results Forty patients (37.0 %) had a recovery rate of less than 50 %. Multivariate logistic regression analysis revealed that a higher preoperative SCR and a longer duration of symptoms were significant risk factors for a poor clinical outcome. Receiver operating characteristic
J. T. Zhang and F. T. Meng contributed equally to this work. J. T. Zhang and F. T. Meng should be considered co-first authors. & Yong Shen [email protected] 1
Department of Spinal Surgery, The Third Hospital of Hebei Medical University, No. 139 Ziqiang Road, Shijiazhuang 050051, Hebei, People’s Republic of China
(ROC) curve analysis showed that the optimal preoperative SCR cutoff value as a predictor of poor clinical result was 1.46. The area under the ROC curve of preoperative SCR for predicting a poor surgical outcome was 0.844. Conclusions Preoperative SCR significantly reflected the surgical outcome in patients with CSM. Patients with SCR greater than or equal to 1.46 can experience poor recovery after surgery. Keywords Cervical spondylotic myelopathy Intramedullary spinal cord signal intensity Magnetic resonance imaging Prognosis Quantitative analysis
Introduction Cervical spondylotic myelopathy (CSM) is one of the most common causes of spinal cord dysfunction in the elderly population. The disease usually has an insidious course and a slow stepwise deterioration in neurological function [1]. However, approximately 5 % of patients present with a dramatic and rapid functional decline [2]. In case of severe spinal cord compression or a progressive course, operative decompression is the accepted treatment for CSM. Although there is emerging evidence that most patients improve after surgical treatment, the key clinical and imaging factors that predict the surgical outcome remain uncertain. Magnetic resonance imaging (MRI) is a valuable tool before surgical decompression because it visualizes not only the magnitude of cervical spinal cord compression but also intramedullary signal intensity. The presence of intramedullary high signal intensity on T2-weighted MRI in patients with CSM reflects chronic spinal cord compression lesion. However, the significance of increased
123
Eur Spine J
signal intensity (ISI) on T2-weighted imaging (WI) for prognosis remains controversial [3–12]. Definitive information is not available because most descriptions of signal changes are qualitative in nature. Based on the previous studies [13, 14], we used signal change ratio (SCR) to quantitatively assess the changes of signal intensity. The aim of this study is to assess the risk factors associated with poor recovery outcome, particularly the predictive value of quantitative SCR, after surgical treatment for CSM and ascertain the crucial determinants of surgical outcome using statistical analyses.
Materials and methods Patient population The research protocol was approved by the Research and Ethics Committee of The Third Hospital of Hebei Medical University, and all patients gave written informed consent for their information to be stored in the hospital database and used for research. A total of 178 consecutive patients with CSM were prospectively enrolled from January 2011 to January 2012. Sixty-two patients who had asymptomatic cervical cord compression, active infection, trauma, neoplastic disease, rheumatoid arthritis, previous surgery for CSM, cervical ossification of the posterior longitudinal ligament, and concomitant symptomatic lumbar spinal stenosis, or other neurological disorders were excluded from this study. An additional of 8 patients were lost to follow-up within the 12 months after surgery because of various reasons unrelated to their CSM. The remaining 108 patients who could be tracked for more than 12 months after surgery were included in this study. Diagnoses were confirmed by neurological examinations and imaging studies such as X-rays radiographs and MRI. Neurological assessment The preoperative and postoperative neurological function 12 months after surgery was assessed using Japanese Orthopaedic Association (JOA) score. The recovery ratio of JOA score was calculated using Hirabayashi’s method [15] and was based on the following formula: recovery rate = (postoperative JOA score-preoperative JOA score/ 17-preoperative JOA score) 9 100 %. The 12-month time frame was chosen because it represents a typical time period of optimum recovery after operation for CSM [16, 17]. Recent study-reported clinical results were divided into 4 groups as follows: 75 % or higher (excellent), 50–74 % (good), 25–49 % (fair), and less than 25 % (poor) [18]. Therefore, we defined a poor clinical outcome as a recovery rate less than 50 % in this study.
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Radiographic assessment The C2–7 angle was measured between the posterior border of the C2 vertebral body and posterior border of the C7 vertebral body on lateral radiographs with patients in a neutral position. The Cobb method was used to measure the C2–7 ROM through the change in the maximal flexion and extension by lateral radiographic view. All patients underwent high-resolution MRI with a 1.5-T system (Siemens Magnetom Symphony) before surgery. MRI of the cervical spinal cord were obtained using a spin echo sequence system for T1-weighted images (T1WIs) and a fast spin echo sequence system for T2-weighted images (T2WIs). A surface coil was used. The slice width was 4 mm, and the acquisition matrix was 512 9 256. The sequence parameters for T1WIs were a repetition time (TR) of 612 ms and an echo time (TE) of 13 ms; for T2WIs, a TR of 2400 ms and a TE of 114 ms was used. The high signal intensity values of the cervical spinal cord on sagittal T2WIs were obtained, and the regions of interest (ROIs) were taken by 0.05 cm2. The normal spinal cord signal intensity values on sagittal T2WIs were obtained at C7–T1 disc levels, and the ROIs were taken by 0.3 cm2. If no intramedullary high-signal intensity on T2WIs was noted, the ROIs will be taken by 0.05 cm2 of the severely compressed cord. The SCR was defined as the signal intensity at the level of ISI or severely compressed cord (in cases with no ISI) divided by the signal intensity at the C7–T1 disc level. Signal intensity value was measured on the MRI workstation and the SCR was calculated. Choosing ROIs is due to a balance of a number of factors. For instance, extremely large area would not hold all patients in the group; whereas extremely small area would jeopardize the accuracy of the signal intensity value. Statistical analysis Descriptive analysis for the patient population was conducted using means and standard deviations (SD) for continuous variables and frequencies and percentages for categorical variables. Inferential statistics were performed to assess the association between the independent risk factors and recovery status using independent Student t tests for continuous variables and Chi squared or Fisher’s exact tests to analyses categorical variables. Multivariate logistic regression analysis was also performed to control for potential confounding variables with the end point of ‘poor recovery after surgery’. Adjusted odds ratios (OR) with 95 % confidence intervals (CI) were presented with their respective p values. Factors with a p value of less than 0.20 in univariate analysis were entered into the multivariate logistic model. Receiver operating characteristic (ROC) curve was constructed to evaluate the sensitivity
Eur Spine J
and specificity of SCR in predicting poor clinical result after surgery. p \ 0.05 was considered to represent a statistically significant difference. All analyses were performed using SPSS software (version 21.0; SPSS Inc, Chicago, IL).
Results The patient characteristics were shown in Table 1. There were 65 men and 43 women; mean age at surgery was 66.0 years (range 38–84 year). The average JOA score was 10.0 points (range 6–15) before surgery and 13.7 points (range 6–17) 12 months after surgery. The JOA recovery rate averaged 53.9 % (range 0–100 %); 68 patients had good clinical outcomes, with recovery rates greater than or equal to 50 %, while 40 patients had poor clinical outcomes with recovery rates less than 50 %. Twenty-eight patients had diabetes mellitus. The average preoperative JOA scores for the good recovery group and poor recovery group were not significantly different (10.2 vs 9.7, p = 0.292). The postoperative JOA score was significantly improved in the good recovery group compared with the poor recovery group at 12 months after surgery (14.7 vs 11.9, p \ 0.001). There were no significant differences between the two groups regarding the sex, BMI, diabetes mellitus. The anterior approach (discectomy or corpectomy with fusion) for decompressive surgery was performed in 70 patients, posterior approach (either laminectomy and fusion or laminoplasty) was performed in 29 patients, and combination of both anterior and posterior approaches was Table 1 Comparison of patient characteristics between good and poor recovery groups
performed in 9 patients. All patients had adequate cervical spinal cord decompression as confirmed by MRI at 6 months after surgery. None of them required revision surgery for inadequate cervical spinal cord decompression. There were no significant differences in the type of surgical procedure and levels involved between the two groups (p = 0.208, p = 0.515, respectively). The age at operation in the poor recovery group was significantly older than in the good recovery group (68.6 vs 64.5 year, p = 0.021). The duration of symptoms was significantly longer in the poor recovery group compared with the good recovery group (20.9 vs 10.2 mo, p \ 0.001). The preoperative C2–7 angle was similar in the two groups (16.2° vs 15.7°, p = 0.668). Regarding dynamic factors of the cervical spine, there was no significant difference in the preoperative C2–7 ROM between the two groups (16.9° vs 17.3°, p = 0.807). The SCR was significantly greater in the poor recovery group than in the good recovery group (1.65 vs 1.30, p \ 0.001). From univariate analysis, three variables were selected for multivariate regression: age, duration of symptoms and SCR. The multivariate logistic regression analysis revealed that the odds of a poor clinical outcome were greater when the patient had a higher preoperative SCR (OR 6.02, p = 0.001) and had a longer duration of symptoms (OR 3.63, p \ 0.001, Table 2). The ROC analysis showed that the optimal cutoff value of preoperative SCR as a predictor of poor clinical result was 1.46, which maximized the sum of the sensitivity and specificity (Fig. 1). The area under the ROC curve of preoperative SCR for predicting poor clinical outcome was 0.844 (95 % CI 0.771–0.917; p \ 0.001).
Variable
Good (n = 68)
Poor (n = 40)
p value
Age at operation (year)
64.5 ± 9.5
68.6 ± 7.6
0.021
Female sex (n, %)
28 (41.2 %)
15 (37.5 %)
0.706
BMI (kg/m2)
25.7 ± 3.0
25.0 ± 4.4
0.342
Diabetes mellitus (n, %) Duration of symptoms (mo)
20 (29.4 %) 10.2 ± 7.5
8 (20.0 %) 20.9 ± 15.8
Preoperative JOA score
10.2 ± 2.5
9.7 ± 2.2
JOA score at 12-month follow-up
14.7 ± 1.1
11.9 ± 2.4
\0.001
Recovery rate (%)
66.8 ± 10.5
32.0 ± 11.9
\0.001 \0.001
0.281 \0.001 0.292
SCR
1.30 ± 0.16
1.65 ± 0.37
C2–7 angle (°)
16.2 ± 5.7
15.7 ± 6.5
0.668
C2–7 ROM (°)
16.9 ± 10.0
17.3 ± 6.2
0.807
Levels involved
2.1 ± 1.0
1.9 ± 1.1
0.515
Anterior
40
30
0.208
Posterior
22
7
Combined anterior/posterior
6
3
Surgical approach
BMI body mass index, JOA Japanese Orthopaedic Association, SCR signal change ratio, ROM range of motion
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Eur Spine J Table 2 Risk factors for poor outcome after operation: multiple logistic regression analysis Variablea
OR (95 % CI)
p value
Age at operation (year)
1.05 (0.98–1.12)
0.134
Duration of symptoms (mo)
3.63 (1.82–7.19)
0.000
SCR
6.02 (2.19–16.54)
0.001
SCR signal change ratio, CI confidence interval a
Duration of symptoms: 1, B3 mo; 2, [3 but B6 mo; 3, [6 but B12 mo; 4, [12 but B24 mo; 5, [24 mo. SCR: 1, [1.00 but B1.50; 2, [1.50 but B2.00; 3, [2.00 but B2.50; 4, [2.50
Fig. 1 ROC curves showed that optimal cutoff value of SCR for prediction of a poor clinical outcome
Discussion The elucidation of factors that contribute to prognosis of patients with CSM has been investigated by several groups [10, 19–22]. Recognition of the best timing for surgery to ensure neurological recovery is an important clinical issue. Up to now, numerous factors have been reported to affect postoperative outcomes in patients with CSM. Age [20], duration of myelopathic symptoms [4, 10, 20, 21, 23], signal intensity changes on preoperative MRI [5, 7, 8, 24], and preoperative JOA score have been considered key predictors. However, the list of predictive factors differs according to researchers, and the prognostic significance of these factors remains controversial. ISI of the cervical spinal cord on T2-weighted MRI is often observed in patients with CSM, and various authors have speculated on its histopathologic significance and impact on surgical outcome. ISI on T2WI indicates local
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pathologic changes in the spinal cord, and patients with CSM and high signal intensity on T2WI usually have a poor prognosis even after surgical intervention [3–7]. AlMefty et al. [25] reported that high signal change on T2WI reflected myelomalacia, and that low signal change on T1WI indicated cystic necrosis or secondary syrinx. Yukawa et al. [26] indicated that preoperative ISI in T2WI was correlated with age, duration of symptoms, postoperative JOA score, and recovery rates, and predicted a poor outcome, especially intense ISI. Despite such evidence, many studies found no correlation between surgical outcome and intramedullary ISI on T2WI [8–12, 27, 28]. What is the reason for this observation? The following may explain this phenomenon. Although MRI provides high specificity in the assessment of morphologic changes and intramedullary changes of the cervical spinal cord, it is almost impossible to estimate potential recovery of the cervical spinal cord on preoperative MRI without appropriate quantitative analysis. We consider that ISI is a variant with large range and it usually covers a huge range of actual severity. If only focusing on the patients with ISI or not, it will bias the result due to possible judgment errors by each investigator. Considering these factors, in this study, signal change was evaluated with a focus on quantitative approaches. SCR was a quantitative method to assess the changes of signal intensity, which was described in previous studies [13, 14]. We found that preoperative SCR was an independent predictor of surgical outcome. In the statistic analysis, we categorized SCR into four groups: 1.50 or less, more than 1.50–2.00, more than 2.00–2.50, and more than 2.50. Specifically, the odds of a poor outcome were 6.02 times of greater for every half-point increase in the preoperative SCR. Then, we calculated that the optimal cutoff value of SCR as a predictor of poor outcome after surgery was 1.46. As far as we know, this study first reported that patients with SCR greater than or equal to 1.46 can predict poor recovery after surgical treatment for CSM. Therefore, recognition of SCR contributes significantly to the determination of the most appropriate timing for surgery. Moreover, duration of symptoms was another independent predictive factor affecting clinical outcome after surgery. The odds of a poor outcome were 3.63 times greater for patients with more than 3–6 months of symptoms than for those with 3 months or less of symptoms. The rationale is that long-standing and chronic compression of the spinal cord may lead to irreversible damage due to demyelination and necrosis of the gray matter. The current study demonstrated that patients age in the poor outcome group was significantly older than that in the good recovery group (p = 0.021). Age was also selected to multivariate logistic analysis. However, after adjustments for SCR and duration of symptoms, age showed a trend toward mild, but not significant, association with poor outcome. Although most surgeons will not discriminate on the basis of age, they
Eur Spine J
should be aware that elderly patients may translate a poor neurological recovery. However, patient demographic variables, such as gender, BMI and diabetes mellitus did not influence the improvement with surgical intervention. The C2–7 angle, C2–7 ROM, levels of compression and surgical approach did not correlate with clinical outcome. There are several limitations need to be considered in our study. First, this study was a single-center design and involved only a limited number of patients. Second, each high-resolution MRI system has different characteristic and working parameter. Therefore, these limitations suggest that further study of these questions is needed.
Conclusions Quantification of signal intensity in patients with CSM was used in the present study to assess the impact of intramedullary signal change on the surgical outcome. Preoperative SCR on MRI could be potentially useful for prediction of the surgical outcome in patients with CSM. Patients with SCR greater than or equal to 1.46 can experience poor recovery after surgery. Acknowledgments statistical analysis.
We thank Dr. Jie Li for his assistance in the
Conflict of interest The authors declare that they have no conflicts of interest concerning this article.
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