Ce rv i c a l spondylosis is a progressive disease that is

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1 J Neurosurg Spine 11: , 2009 Effect of spinal cord signal intensity changes on clinical outcome after surgery for cervical spondylotic myelopathy Clinical article An o o j Ch a t l e y, M.S., M.Ch., Ra j Ku m a r, M.S., M.Ch., Vi j e n d r a K. Ja i n, M.Ch., Sanjay Behari, M.Ch., and Rabi Narayan Sahu, M.Ch. Department of Neurosurgery, Sanjay Gandhi Institute of Postgraduate Medical Sciences, Lucknow, India Object. The presence of intramedullary T2 high signal intensity changes in patients with cervical spondylotic myelopathy (CSM) indicates the existence of a chronic spinal cord compressive lesion. However, the prognostic significance of signal intensity changes remains controversial. The purpose of this study was to evaluate the effect of spinal cord T2 signal intensity changes on the outcome after surgery for CSM. Method. In a prospective study, 64 patients with CSM who underwent surgical treatment between October 2006 and April 2008 using an anterior approach were included. Based on the clinical symptoms and signs present, the severity of neurological deficits of all patients was scored according to a modified Japanese Orthopaedic Association scale score for CSM just before the surgery and at 6 months follow-up. Recovery rates were calculated at 6 months. Results. There were 22 patients who did not have spinal cord intensity changes on MR imaging and 44 who demonstrated high-intensity signal changes on T2-weighted images (focal or segmental). No statistically significant differences were found in recovery rates between cases with T2 signal intensity changes and those with no signal intensity changes. However, the postoperative modified Japanese Orthopaedic Association scale scores and the recovery rates were much lower in patients with multisegmental signal intensity changes compared with those without these changes or those with focal signal intensity change, and ANOVA demonstrated this difference to be statistically significant (p < 0.05). Conclusion. Multisegmental spinal cord signal intensity changes on T2-weighted MR imaging are predictors of a poor outcome in terms of functional recovery rate in patients undergoing operations for CSM. (DOI: / SPINE091) Ke y Wo r d s cervical spine cervical spondylotic myelopathy spinal cord signal intensity Abbreviations used in this paper: CSM = cervical spondylotic myelopathy; mjoa = modified Japanese Orthopaedic Association. Ce rv i c a l spondylosis is a progressive disease that is a frequent cause of cervical myelopathy, especially in patients > 50 years of age. The natural history of CSM is frequently one of slow, progressive neurological deterioration. The sequences of degenerative changes that constitute cervical spondylosis include intervertebral disc degeneration, disc space collapse, osteophyte formation, and hypertrophy of the ligamentum flavum, lamina, and facets. These changes, when occurring in conjunction with a narrow canal, predispose the aging patient to CSM. 25 Spinal cord injury may occur due to mechanical compression and vascular compromise, with resultant lesions in the dorsal and lateral columns and degeneration of the ascending and descending tracts. 18 In the past, the radiological diagnosis of CSM was dependent on myelography, CT, and CT myelography. At present, MR imaging is the preferred radiological diagnostic tool that can not only depict spinal cord compression, but also reflect the pathological changes in the spinal cord. 15,31 The neurological outcome of decompressive surgery for CSM is influenced by several factors. Although each factor may have an independent effect, it is more likely that the outcome is influenced by more than 1 factor. Many authors 15,28,29,31 have reported intramedullary high signal intensity changes on T2-weighted MR imaging in patients with compressive spondylotic lesions of the cervical spinal cord. Such intramedullary high signal intensity abnormality is presumed to be myelomalacia or cord gliosis secondary to a long standing compressive effect on the spinal cord. 29 Therefore, the presence of intramedullary high signal intensity in patients with CSM indicates the existence of a chronic spinal cord compressive lesion. However, the prognostic significance of signal intensity changes remains controversial. The purpose of this study was to evaluate the effect of spinal cord signal intensity 562 J Neurosurg: Spine / Volume 11 / November 2009

2 Spinal cord intensity changes in cervical spondylotic myelopathy changes on outcome following surgery for CSM, and to identify other factors associated with these cord intensity changes that may affect the outcome. Methods J Neurosurg: Spine / Volume 11 / November 2009 TABLE 1: Clinical features of the 64 patients included in the study Clinical Features No. of Cases (%) symptoms weakness 50 (78.1) all 4 limbs 31 (48.4) both upper limbs 10 (15.6) both lower limbs 2 (3.1) right-sided limbs 1 (1.6) 1 upper limb 6 (9.4) stiffness 51 (79.7) numbness radicular myelopathic radiculo-myelopathic paraesthesia radicular myelopathic radiculo-myelopathic pain neck pain radicular funicular sphincteric dysfunction bladder bowel 12 (18.8) 33 (51.6) 1 (1.6) 15 (23.4) 19 (29.7) 6 (9.4) 25 (39.1) 17 (26.6) 3 (4.7) 27 (42.2) 21 (32.9) walking difficulty 55 (86.0) clumsiness of hands 47 (73.4) Lhermitte phenomenon 1 (1.6) respiratory difficulty 1 (1.6) signs increased tone 59 (92.2) wasting 9 (14.1) weakness 54 (84.4) Hoffman sign 33 (51.6) sensory loss 46 (71.9) loss of proprioception 20 (31.3) spinal tenderness 13 (20.3) Patient Population In a prospective study, 64 of 137 consecutive patients who underwent operations for symptomatic CSM/radiculomyelopathy using the anterior approach between October 2006 and April 2008 at Sanjay Gandhi Postgraduate Institute of Medical Sciences in Lucknow, India, were included for the purpose of the study. The inclusion criteria for the study were those patients with CSM/radiculomyelopathy who underwent an operation using an anterior approach with follow-up > 6 months. The study exclusion criteria were: 1) the presence of an ossified posterior longitudinal ligament; 2) history of trauma; 3) cervical radiculopathy with no features of myelopathy; 4) undergoing an operation using the posterior approach; 5) previous surgery for CSM; 6) associated disorders such as atlantoaxial dislocation, basilar invagination, rheumatoid arthritis, and ankylosing spondylitis; and 7) follow-up < 6 months. Cervical laminectomy for treatment of CSM may lead to late instability with progressive kyphotic deformity or swan neck deformity. This procedure does not directly address the ventral compression or correct the dynamic component. To address these shortcomings, fusion following laminectomy or laminoplasty may be performed. However, we prefer using the anterior approach for all patients with ventral compression, except for older patients with significant comorbid conditions, a lordotic spine, and compression at > 3 levels. Therefore, these cases were not included in the study because they were very few in number and included other significant factors such as very old age and significant comorbid conditions that adversely affect prognosis. Of the 137 patients, 73 were excluded because they did not fulfill the inclusion criteria. There were 19 patients with ossified posterior longitudinal ligaments, 12 with a history of trauma, 11 who underwent surgery using a posterior approach, 15 with previous surgery for CSM, 8 with associated disorders (as noted in the exclusion criteria), and another 8 patients with follow-up < 6 months. All of these patients were excluded from the study. Among the 64 patients, 57 were men and 7 were women. The mean age of the patients was 47.1 years (range years). Duration of symptoms ranged from 1 to 84 months (mean months). The diagnosis of CSM was made on the basis of clinical and radiological findings. Clinical symptoms and signs of the patient population are summarized in Table 1. All patients showed neurological findings compatible with CSM/radiculomyelopathy. Based on the clinical symptoms and signs, the severity of neurological deficits of all patients was scored according to an mjoa scale score 2,7 for CSM (Table 2) just before surgery and at 6 months follow-up. The range of this score is 0 17, in which 0 represents maximal neurological deficits and 17 represents no neurological deficits. All patients were followed up for a minimum of 6 months. The mean follow-up period was months (range 6 20 months). The recovery rate after treatment was calculated using the Hirabayashi 6 method as follows: (postoperative mjoa scale score preoperative mjoa scale score / 17 preoperative mjoa scale score) 100 Imaging Studies Radiological investigations included plain radiographs of the cervical spine in the anteroposterior and lateral flexion-extension views, and MR imaging of the cervical spine. The curvature of the spine, reduced disc space height, and presence of osteophytes, spondylolisthesis, and vertebral fusion were examined using plain radiographs of the cervical spine. The MR imaging protocol 563

3 A. Chatley et al. TABLE 2: Neurological outcome for anterior spondylectomy and laminoplasty* Parameter Anterior Spondylectomy Laminoplasty p Value preop JOA score 11.6 ± ± postop (4 6 weeks) JOA score 14.7 ± ± follow-up JOA score 14.5 ± ± neurological improvement rate at follow-up (%) 67.5 ± ± * Data expressed as the mean ± SD. Mann-Whitney U-test. included sagittal and axial T1- and T2-weighted images, using a slice thickness of 5 mm to detect the level and type of disc protrusion. Attention was mainly directed to the sagittal T2-weighted images, to examine increased signal intensity resulting from spinal cord compression. Intensity changes in the spinal cord on T1-weighted images were not taken into consideration. The T2 hyperintensity changes were further quantified and divided into 2 groups: focal (< 2 segments) and multisegmental ( 2 segments). Radiological findings are summarized in Table 3. The disc level at which MR imaging showed either an intrinsic signal intensity change of the spinal cord or a maximal compression of the spinal cord was considered the intervertebral disc level responsible for cervical compressive myelopathy. Surgical Procedures All patients underwent surgery using an anterior approach. The surgical procedures performed are summarized in Table 4. The decision to perform surgery was made on the basis of clinical-radiological correlation. Mild disc herniations, without any compression of the thecal sac, were not targeted. In all cases, postoperative radiographs of the cervical spine were performed on the 1st postoperative day. Operative complications in these patients included graft extrusion in 3 cases, CSF leak in 2, hoarseness of voice in 2, and donor site infection in 2 cases. Statistical Analysis Statistical analysis was conducted using SPSS statistical software version 15 for Windows (SPSS, Inc.). The primary variable analyzed as an indicator of surgical outcome was the recovery rate; other factors taken into account were duration of symptoms, age at surgery, and the pre- and postoperative mjoa scale scores. Initially the entire population was divided into 2 groups: one in which high-intensity signal changes were present on T2-weighted images, and one in which they were absent. The group in which these signal changes were present was then divided into 2 subgroups according to the extension of the lesion: focal (lesion spanning < 2 segments) and multisegmental (lesion spanning 2 segments). To compare the recovery rate between groups, we used the independent sample t-test when data were continuous and normally distributed. The Mann-Whitney U-test was used when these conditions were not fulfilled. A linear regression model was performed to verify whether signal intensity changes could be used to predict outcome. Probability values < 0.05 were considered statistically significant. Results For the entire population the mean preoperative and postoperative (at 6 months) mjoa scale scores were ± 2.86 and ± 2.71, respectively. The mean followup duration was months (range 6 20 months). The mean recovery rate was ± 36.92%. There were 22 patients who did not have cord signal intensity changes on MR imaging and 44 who demonstrated high-intensity signal changes on T2-weighted images. Differences in mean values between patients with and without high-intensity signal changes on T2-weighted images are shown in Table 5 for the following variables: age at surgery, duration of symptoms, pre- and postoperative mjoa scale scores, and postoperative recovery rates. The Student t- test revealed no statistically significant differences in recovery rates between cases of T2 signal intensity change and those with no signal change, and none of the other variables was shown to exhibit any significant intergroup differences. A summary of the data obtained in the subgroups of patients (focal and segmental intensity changes) in whom the T2-weighted imaging revealed high-intensity signals is provided in Table 6. The postoperative mjoa scale scores and the recovery rates were much lower in patients with multisegmental signal intensity change as compared with those without this change or those with focal signal intensity change; ANOVA demonstrated this difference to be statistically significant (p < 0.05). All other variables (age at surgery, duration of symptoms, preoperative mjoa scale scores) did not exhibit any significant differences between the 2 groups. However, there were no statistically significant differences in recovery rates between cases of focal T2 signal intensity change and those with no signal change. All other variables (age at surgery, duration of symptoms, pre- and postoperative mjoa scale scores) also did not exhibit any significant differences. Discussion The role of MR imaging signal intensity changes in patients with cervical spine disorders has been widely studied. Abnormal T2-weighted signal intensity has been described in numerous disorders of the cervical spine. Different authors have speculated on both the histolopatho- 564 J Neurosurg: Spine / Volume 11 / November 2009

4 Spinal cord intensity changes in cervical spondylotic myelopathy TABLE 3: Radiological findings Cervical Spine Characteristic No. of Cases (%) plain radiograph prominent osteophytes 41 (64.1) configuration lordotic straightening kyphotic reduced height of disc space single level multiple level 45 (70.3) 17 (26.6) 2 (3.1) 35 (54.7) 15 (23.4) vertebral fusion 5 (7.8) subluxation 4 (6.3) MR imaging level of disc bulge C2 3 1 (1.6) C3 4 7 (10.9) C4 5 5 (7.8) C (26.6) C6 7 7 (10.9) C2 3, C3 4 1 (1.6) C3 4, C4 5 3 (4.7) C3 4, C5 6 2 (3.1) C3 4, C5 6, C6 7 1 (1.6) C4 5, C5 6 7 (10.9) C4 5, C6 7 2 (3.1) C4 5, C5 6, C6 7 1 (1.6) C5 6, C (15.6) spinal cord intensity changes absent focal multisegmental 22 (34.4) 31 (48.4) 11 (17.2) logical 1,12,16,17,21,28 and prognostic significance 12,17,19,22,29,35 of these signal intensity changes. In 1987, Takahashi et al. 28 originally proposed that the T2 high-intensity signal changes represented myelomalacia from gliosis, edema, demyelination, and microcavity formation. However, controversy persisted with respect to the specific pathological mechanism involved. Ramanauskas et al. 24 divided myelomalacia into 3 stages. They proposed that in the early stage, a change in the signal intensity of the spinal cord observed on MR imaging reflected cord edema, and that in the intermediate stage, a change reflected cystic necrosis of the central gray matter after prolonged cord edema. These authors also reported that in the early and intermediate stages, the spinal cord demonstrated high signal intensity on T2-weighted sequences, and that in the late stage, low signal intensity on T1-weighted images and high signal intensity on T2-weighted sequences were noted. It was proposed by Al Mefty et al. 1 that the high-intensity signal on T2-weighted images is secondary to myelomalacia, with cystic cord necrosis and syrinx formation evidenced by low T1/high T2 signal characteristics. Haupts and Haan 5 observed that there can be extension of T2 signal changes above and below the regions of stenosis and proposed a shearing mechanism as the underlying pathological process. Mehalic et al. 15 proposed that T2 high-intensity signal changes were nonspecific and may represent a variety of pathological processes including edema, inflammation, vascular ischemia, gliosis, or myelomalacia. In acute spinal cord trauma, hyperintense T2-weighted changes have been assumed to be secondary to cord edema or small, petechial intramedullary hemorrhage. Larger hemorrhage, with proportionally greater deoxyhemoglobin, appears as hypointense lesions on T2-weighted images. 4,8,10 Eventual cyst formation may present with hypointensity on T1-weighted images and hyperintensity on T2-weighted sections. 23,33,34 Matsuda et al. 12 proposed that reversible signal changes may be secondary to vascular pathology and irreversible lesions could represent chronic cord damage, with ensuing gliosis, demyelination, and microcavity formation. Similarly, Taneichi et al. 30 proposed that reversible T2-weighted hyperintensity correlates with simple edema, whereas gliosis presents with irreversible signal changes, based on serial MR imaging results and correlation with patient clinical status. Based on the results reported in the literature, high-intensity signal changes on T2-weighted images indicate edema and gliosis (which may be reversible), whereas low-intensity signal changes on T1-weighted images can represent myelomalacia and necrosis (which are considered irreversible). 21 Correlation between MR imaging findings and clinical presentation/recovery after therapy remain unclear. TABLE 4: Summary of the surgical procedures performed Surgical Procedure No. of Cases (%) discoidectomy without bone grafting 9 (14.1) Smith-Robinson procedure 25 (39.1) Cloward procedure 2 (3.1) corpectomy with grafting 22 (34.4) corpectomy with grafting and plating 4 (6.3) Smith-Robinson at upper level and corpectomy with grafting at lower level 1 (1.6) 2 consecutive-level corpectomy with grafting and plating 1 (1.6) J Neurosurg: Spine / Volume 11 / November

5 A. Chatley et al. TABLE 5: Comparison between patients with no signal intensity change and those with signal intensity change on T2-weighted images* Variable Signal Intensity Change Absent (22 Patients) Present (44 Patients) age (yrs) ± ± duration of symptoms (mos) 6.16 ± ± preop mjoa scale score ± ± 2.65 postop mjoa scale score ± ± 2.86 recovery rate (%) ± ± * All values given as mean ± SD; p > 0.05 for all comparisons. TABLE 6: Comparison between patients with focal signal intensity change and those with multisegmental signal intensity change on T2-weighted images* Variable Signal Intensity Change Focal (31 Patients) Multisegmental (11 Patients) p Value age (yrs) ± ± >0.05 duration of symptoms (mos) ± ± >0.05 preop mjoa scale score ± ± 2.58 >0.05 postop mjoa scale score ± ± 3.64 <0.05 recovery rate (%) ± ± <0.05 * All values given as mean ± SD. Several studies have confirmed that patients with lowintensity signal changes on T1-weighted images have a poor prognosis. 14,17,27 However, the prognostic value of high-intensity signal changes on T2-weighted images remains controversial. Therefore, we limited our study to the changes on T2-weighted images. Some authors attest to increased severity of neurological deficit concomitant with an increased T2 signal, 9,12,20,29,34 whereas others note no correlation between the two factors. 21,31 Matsumoto et al. 13 and other authors 11,19,35 have observed that altered signal intensity on T2-weighted images was not related to poor outcome in patients with CSM. Singh et al. 26 reported that patients with worse signal changes on MR imaging subsequently experienced greater benefits from surgery as measured by improvement in walking parameters and other rating scales (myelopathy disability index, Nurick scale, and Ranawat classification). In some other studies, 3,32 although it appeared that there was a tendency toward a poorer outcome in patients with T2 high-intensity signal changes, statistical significance was reached only after quantifying these images. In our study, patients were initially divided into 2 groups: those without T2 high-intensity signal change and those with T2 high-intensity signal change. The recovery rate, although higher in patients without these signal changes (58.53 ± 32.45% vs ± 38.38%, respectively), did not differ significantly between the 2 groups. The other parameters (age at surgery, duration of symptoms, preand postoperative mjoa scale scores) also did not exhibit statistically significant intergroup differences. On further quantification of the T2 spinal cord signal-intensity changes (focal/multisegmental), it was observed that the recovery rate of the 11 patients in whom T2-weighted images revealed signal intensity changes spanning multiple levels was significantly worse (17.33 ± 38.74%) than that in patients with focal (52.35 ± 34.36%) or no signal changes (58.53 ± 32.45%) on T2-weighted images. The postoperative mjoa scale scores were also significantly lower in these patients (11.27 ± 3.64) as compared with the patients with focal (13.90 ± 2.21) or no signal changes (14.45 ± 2.24). Although patients with multisegmental changes were older and were symptomatic for a longer duration as compared with patients in the other 2 groups, these differences were not statistically significant (Tables 5 and 6). Similarly, there were no significant differences in the 3 groups regarding preoperative mjoa scale scores. The regression model confirmed the value of multisegmental T2 spinal cord signal intensity changes as predictors of a poor outcome in terms of recovery rate. Conclusions Based on our study, we conclude that patients with CSM and high-intensity signal changes on T2-weighted images do not necessarily have a poorer prognosis when compared with patients with no signal intensity changes. Multisegmental T2 cord intensity changes, however, are predictors of a poor outcome in terms of functional recovery rate in patients who undergo operations for CSM. Finally, focal high-intensity changes on T2-weighted images do not indicate a poor functional recovery rate. Disclaimer The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Acknowledgment The authors gratefully acknowledge the kind help provided by Professor Uttam Singh of the Department of Biostatistics, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, India, in the statistical analysis conducted in this paper. References 1. Al-Mefty O, Harkey LH, Middleton TH, Smith RR, Fox JL: Myelopathic cervical spondylotic lesions demonstrated by magnetic resonance imaging. J Neurosurg 68: , Benzel EC, Lancon J, Kesterson L, Hadden T: Cervical laminectomy and dentate ligament section for cervical spondylotic myelopathy. J Spinal Disord 4: , Fernández de Rota JJ, Meschian S, Fernández de Rota A, Urbano V, Baron M: Cervical spondylotic myelopathy due to chronic compression: the role of signal intensity changes in magnetic resonance images. J Neurosurg Spine 6:17 22, Flanders AE, Schaefer DM, Doan HT, Mishkin MM, Gonzalez CF, Northrup BE: Acute cervical spine trauma: correlation of MR imaging findings with degree of neurologic deficit. 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6 Spinal cord intensity changes in cervical spondylotic myelopathy 5. Haupts M, Haan J: Further aspects of MR-signal enhancements in stenosis of the cervical spinal canal. MRI investigations in correlation to clinical and CSF findings. Neuroradiology 30: , Hirabayashi K, Miyakawa J, Satomi K, Maruyama T, Wakano K: Operative results and postoperative progression of ossification among patients with ossification of cervical posterior longitudinal ligament. Spine 6: , Hukuda S, Mochizuki T, Ogata M, Shichikawa K, Shimomura Y: Operations for cervical spondylotic myelopathy: A comparison of the results of anterior and posterior procedures. J Bone Joint Surg Br 67: , Kadoya S, Nakamura T, Kobayashi S, Yamamoto I: Magnetic resonance imaging of acute spinal cord injury. Report of three cases. Neuroradiology 29: , Kohno K, Kumon Y, Oka Y, Matsui S, Ohue S, Sakaki S: Evaluation of prognostic factors following expansive laminoplasty for cervical spinal stenotic myelopathy. 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Spine 20: , Wada E, Yonenobu K, Suzuki S, Kanazawa A, Ochi T: Can intramedullary signal change on magnetic resonance imaging predict surgical outcome in cervical spondylotic myelopathy? Spine 24: , Yamashita Y, Takahashi M, Matsuno Y, Kojima R, Sakamoto Y, Oguni T, et al: Acute spinal cord injury: magnetic resonance imaging correlated with myelopathy. Br J Radiol 64: , Yamashita Y, Takahashi M, Matsuno Y, Sakamoto Y, Oguni T, Sakae T, et al: Chronic injuries of the spinal cord: assessment with MR imaging. Radiology 175: , Yone K, Sakou T, Yanase M, Ijiri K: Preoperative and postoperative magnetic resonance image evaluations of the spinal cord in cervical myelopathy. Spine 17 (10 Suppl):S388 S392, 1992 Manuscript submitted January 1, Accepted June 23, Address correspondence to: Raj Kumar, M.S., M.Ch., Department of Neurosurgery, Sanjay Gandhi Postgraduate Institute of Medical Sciences, Lucknow, UP, India rajkumar@sgpgi. ac.in. J Neurosurg: Spine / Volume 11 / November