Cervical spondylotic myelopathy (CSM) is the most common cause of spinal cord dysfunction worldwide.1,2 It is a progressive disease caused by the degeneration of various components of the spinal axis, including the vertebral body, the intervertebral disc, the supporting ligaments, and the facet joints. Various static factors and anatomical changes to the spine, including the development of osteophytes, disc herniation, ossification of the posterior longitudinal ligament (OPLL), hypertrophy of the ligament flavum, and vertebral subluxation, can result in stenosis of the spinal canal and lead to compression of the cervical spinal cord.3
Patients are diagnosed with CSM through clinical assessment of symptoms, which may include impaired gait and numb and clumsy hands, as well as through detection of various clinical signs such as hyper-reflexia, atrophy of intrinsic hand muscles, positive Hoffman sign, and upgoing plantar responses.4 This diagnosis is confirmed and others excluded through the use of numerous imaging tests, including plain radiographies,5 magnetic resonance imaging (MRI),6 computed tomography, and electrophysiological modalities such as electromyography or somatosensory-evoked potentials.7,8 For purposes of directing diagnosis and surgical management, MRI is generally considered the preferred method of radiological evaluation, because it can be used to determine the severity of degenerative changes, the diameter of the spinal canal, the degree of cord compression, and also to detect the presence of intrinsic spinal cord abnormalities through signal intensity (SI) changes.2
Although the diagnostic use of MRI in the setting of CSM is well accepted, its role as a prognostic tool in this context is largely unknown. It is unclear whether certain MRI characteristics can predict patient deterioration during longitudinal nonoperative treatment. Duration of symptoms has been clearly identified as an important negative predictor of surgical outcome, and, accordingly, it is essential to preselect patients who have a high probability of progressive clinical deterioration during trials of conservative therapy to ensure optimal clinical outcome.9–17
Two previous systematic reviews of the literature were conducted to evaluate important clinical predictors of outcome, including age, baseline severity score, duration of symptoms, smoking status, and various signs, symptoms and comorbidities.18,19 With respect to MRI characteristics, there is conflicting evidence as to whether anatomic dimensions of the spinal canal or cord properties are more valuable in predicting surgical outcome. It is important to synthesize results from previous studies on the basis of level of evidence in order to draw relevant conclusions as to the most significant predictors of surgical outcome.
The purpose of this study was to conduct a thorough systematic review to address 3 key questions. In adult patients diagnosed with CSM, are there characteristics of the MRI that
- can be used to direct treatment (surgery or conservative care) to improve outcomes?
- predict postsurgical patient outcome?
- predict adverse events?
MATERIALS AND METHODS
Electronic Literature Search
We conducted a systematic search of PubMed/MEDLINE and the Cochrane Collaboration Library for literature published through November 20, 2012. Only studies on humans, written in English and containing abstracts were considered for inclusion, but no limits were placed on the search. Search strategies used for each key question are listed in the Supplemental Digital Content Tables, available at http://links.lww.com/BRS/A827. Reference lists of key articles were also systematically checked to identify additional eligible articles. For key question 1, we sought studies that directly assessed outcomes comparing operative with nonoperative care stratified by MRI characteristics in patients with CSM or OPLL. Having found none, we expanded our search to include indirect evidence from articles that assessed MRI characteristics that predicted poor outcomes in patients with the same diagnosis but undergoing nonoperative care. Identified MRI characteristics predicting a poor outcome in these studies may suggest a need for consideration of surgical intervention.
For key questions 2 and 3, we focused on identifying studies explicitly designed to evaluate preoperative MRI factors affecting outcome after surgery for CSM or OPLL. We included cohort studies evaluating as prognostic factors either MRI-specific characteristics (e.g., SI) or anatomical characteristics assessed by MRI (e.g., spinal canal diameter or number of compressed intervertebral discs). We limited study selection to those that used multivariate analyses that controlled for at least 2 of the following 3 covariates: age, duration of symptoms, and severity of myelopathy. We also limited our search to cohort studies with at least 10 patients in each comparison group. Case reports, meeting abstracts/proceedings, white papers, and editorials were also excluded. Table 1 provides a summary of inclusion and exclusion criteria for each key question. Two investigators (L.T., J.R.D.) reviewed the full texts of potential articles meeting the inclusion criteria to obtain the final collection of included studies (Figure 1).
From the included articles, the following data were extracted: study design; patient characteristics, including diagnosis and treatment administered; follow-up duration and the rate of follow-up; MRI and non-MRI prognostic factors evaluated; outcome measures; and results of association as reported by the authors. Detailed tables containing these results can be found in the Supplemental Digital Content, available at http://links.lww.com/BRS/A827.
Study Quality and Overall Strength of Body of Literature
Class of evidence ratings were assigned to each article independently by 2 reviewers (J.R.D., E.D.B.) using criteria set by The Journal of Bone & Joint Surgery20 for prognostic studies and modified to delineate criteria associated with methodological quality and risk of bias described elsewhere in this issue (Skelly et al).21
After individual article evaluation, the overall body of evidence with respect to each outcome was determined on the basis of precepts outlined by the Grading of Recommendation Assessment, Development and Evaluation Working Group,22 and recommendations made by the Agency for Healthcare Research and Quality.23 Qualitative analysis was performed considering the following Agency for Healthcare Research and Quality–required and additional domains.24
The initial strength of the overall body of evidence was considered high if the majority of the studies were class I or II and low if the majority of the studies were class III or IV. The body of evidence may be downgraded 1 or 2 levels on the basis of the following criteria: (1) inconsistency of results, (2) indirectness of evidence, (3) imprecision of the effect estimates (e.g., wide confidence intervals [CIs]), or (4) non-a priori statement of subgroup analyses. The body of evidence may be upgraded 1 or 2 levels on the basis of the following criteria: (1) large magnitude of effect or (2) dose-response gradient. The final overall strength of the body of literature expresses our confidence in the estimate of effect and the impact that further research may have on the results. An overall strength of “high” means we have high confidence that the evidence reflects the true effect. Further research is very unlikely to change our confidence in the estimate of effect. The overall strength of “moderate” means we have moderate confidence that the evidence reflects the true effect. Further research may change our confidence in the estimate of effect and may change the estimate. A grade of “low” means we have low confidence that the evidence reflects the true effect. Further research is likely to change the confidence in the estimate of effect and likely to change the estimate. Finally, a grade of “insufficient” means that evidence either is unavailable or does not permit a conclusion. The Supplemental Digital Content Tables, available at http://links.lww.com/BRS/A827, contain the details of how we arrived at the strength of evidence for each key question.
Data Analysis and Synthesis
We attempted to collect effect measures (relative risks, hazard ratios, or odds ratios [ORs]) in order to assess the magnitude of the association between predictive characteristic and outcome. However, reporting of these was rare. Instead, most authors reported a correlation or a regression coefficient or simply a P value while stating whether there was a significant association with an outcome. Therefore, we report whether an MRI characteristic was associated with a specific outcome (no association, negative association, or positive association), grouped by MRI characteristic and by outcome.
Clinical Recommendations and Consensus Statements
Clinical recommendations or consensus statements were made through a modified Delphi approach by applying the Grading of Recommendation Assessment, Development and Evaluation/Agency for Healthcare Research and Quality criteria that impart a deliberate separation between the strength of the evidence (i.e., high, moderate, low, or insufficient) and the strength of the recommendation. When appropriate, recommendations or statements “for” or “against” were given “strong” or “weak” designations on the basis of the quality of the evidence, the balance of benefits/harms, and values and patient preferences. In some instances, costs may have been considered. A more thorough description of this process can be found in the focus issue Methods article.
For key question 1, we identified 3 studies that met inclusion criteria from 84 that were obtained from our search strategy (Figure 1). Two were retrospective25,26 and 1 was prospective.27 We excluded 69 by reviewing the abstracts and titles and another 12 after full text review. Sample sizes in these 3 studies ranged from 45 to 70 patients, with mean ages ranging from 55 to 67 years. Mean follow-up varied widely (29–78 mo). For key questions 2 and 3, a total of 17 cohort studies (2 prospective, 15 retrospective) met our inclusion. We excluded 137 by reviewing the abstracts and titles and another 31 after reviewing the full text. Most were excluded because of the absence of a multivariate analysis (see Supplemental Digital Content Tables, available at http://links.lww.com/BRS/A827, for a list of excluded studies and reason for exclusion). Sample sizes ranged from 50 to 197 patients, with mean ages ranging from 44 to 65 years. Mean follow-up varied widely (3 mo to 8 yr). All studies investigated preoperative SI change on MRI, and 7 studies considered anatomic characteristics seen on MRI as prognostic factors for outcome after several types of decompression surgery. Various outcome measures were used across the studies, with the Japanese Orthopaedic Association (JOA) recovery rate reported most consistently, followed by the Nurick grade. All studies controlled for age and the majority also controlled for symptom duration and disease severity. Tables 2 and 3 provide a summary of the sample characteristics, MRI factors assessed, and outcome measures used in the nonoperative and operative studies, respectively.
Are There MRI Characteristics That Can be Used to Direct Treatment (Surgery or Conservative Care) to Improve Outcomes?
Three studies analyzed MRI predictors of functional deterioration during conservative treatment (Table 4).
In the study by Shimomura et al,27 70 patients with mild CSM were enrolled to determine important factors related to successful conservative treatment. Of the 56 patients who completed a final follow-up assessment, 11 showed signs of deterioration from mild to moderate or severe CSM and were recommended surgery. The most significant and only prognostic MRI characteristic was circumferential spinal cord compression on an axial MR image. In this form of compression, the circumferential surface of the spinal cord is deformed by osteophytes, disc bulging, and ligamentum flavum infolding such that the dorsal subarachnoid space cannot be seen on the image. Patients with circumferential compression were at a 26.624 (CI: 1.682–421.541, P = 0.0199) higher risk of symptom deterioration on the JOA scale than those with partial compression, using multivariate logistic regression. Specifically, 10 of 33 patients (30.3%) with this type of cord compression deteriorated, 9 of whom were subsequently treated surgically. Neither partial cord compression on axial MR image, nor high SI on T2-weighted image (WI) (OR: 1.317, CI: 0.161–10.801; P = 0.793, multivariate) was significantly associated with outcome as measured by deterioration in JOA scale.
A second study by Oshima et al25 also examined factors prognostic of outcome in 45 patients with mild CSM treated conservatively. Sixteen of these patients deteriorated on the JOA score and went on to receive surgical treatment. Spinal cord diameter, measured by the ratio at the narrowest part of the canal to the C1 level, was the only MRI characteristic studied and was not significantly related to conservative treatment failure (P = 0.09). The Cox proportional hazard analysis yielded a hazard ratio of 2.24 for a patient with a ratio of less than 50% compared with one with a ratio of 50% or more. The CI, however, did span 1 (CI: 0.83–6.06), indicating insignificance.
Finally, Yoshimatsu et al26 studied 69 patients to determine the limitations of nonsurgical intervention and to analyze important predictors of failed conservative treatment. Forty-three of these patients showed functional deterioration, assessed by a decrease in JOA score. MRI characteristics analyzed as predictors in this study included the number of intervertebral discs compressing the spinal cord and the presence of high SI on a T2WI; neither of these demonstrated significant value in predicting deterioration.
Are There Characteristics of the MRI That Predict Postsurgical Patient Outcome?
This review analyzed the predictive value of both anatomic features and spinal cord properties. The anatomic characteristics considered were cervical curvature, transverse area at the level of maximum compression, spinal canal diameter, number of compressed segments, and rate of cord flattening (Table 5 and Figure 2). Cord properties assessed included high SI on T2WI, low SI on T1WI, combined T1/T2 signal change, SI ratio, number of SI segments, and length on T2WI (Table 6).
In a study by Chen et al,29 abnormal curvature was defined as a configuration of the cervical spine in which any part of the dorsal aspect of the C3 to C6 vertebral bodies crossed the line drawn to and from the dorsocaudal aspects of C2 and C7. There was no significant difference in JOA recovery rate between patients with abnormal and normal cervical curvature (R = −0.768; P = 0.901).
Okada et al28 analyzed the importance of transverse area in predicting outcome assessed by the JOA recovery rate. A larger transverse area was predictive of a higher JOA recovery rate in patients with OPLL and CSM but not in those with disc herniation. This factor was included in the multiple regression equations formulated to predict outcome in all 3 forms of cervical myelopathy.
The predictive value of the compression ratio, calculated by dividing the sagittal diameter by the transverse diameter (×100%), was assessed by 3 studies.28–30 All studies reported a nonsignificant association between cord compression ratio and recovery rate.
The diameter of the spinal canal was assessed as a prognostic factor by a single prospective study.31 Multivariate logistic analysis yielded a nonsignificant association between diameter and final modified Japanese Orthopaedic Association (mJOA).
The greatest number of studies (n = 4) evaluated the relationship between number of compressed segments and outcome assessed by JOA recovery rate,32 Neurosurgical Cervical Spine Scale recovery rate,33 mJOA score,31 Nurick grade, or improvement of motor, sensory, and autonomic symptoms.13 In the study by Park et al,33 correlation analysis revealed no significant association between Neurosurgical Cervical Spine Scale recovery rate and number of compressed segments (R = −0.0427; P = 0.7259). Setzer et al31 observed no differences between an “unchanged,” “improvement,” and “deterioration” group when examining the number of affected segments. Multivariate analysis, conducted by Uchida et al,32 however, revealed that the outcome in spondylotic patients undergoing either laminoplasty (n = 45) or anterior surgery (n = 32) is significantly impacted by involvement of 3 or more intervertebral levels (P = 0.0084; P = 0.0293). Poor outcome in patients with OPLL, on the contrary, is highly associated to 2-vertebra involvement in anterior surgery (P = 0.0388) and laminoplasty (P = 0.0076) and to 3 or more vertebrae in laminoplasty (P = 0.0029). Finally, Suri et al13 reported a nonsignificant association between the number of prolapsed intervertebral discs and motor, sensory, or autonomic outcome. When looking at disability outcome, evaluated by Nurick grade, however, patients with single (P < 0.001, OR: 2.91, 95% CI: 0.7–10.4) or 2-level (P < 0.001, OR: 2.61, 95% CI 0.4–8.9) involvement had better outcome than patients with multilevel prolapsed intervertebral discs.
The rate of flattening of the cord as a prognostic factor was examined by a single study.32 This rate is calculated by dividing the anteroposterior axis of the spinal cord by the spinal cord width (×100%). A rate of flattening less than 50% was significantly associated with a worse JOA recovery rate after anterior surgery and laminoplasty in patients with spondylosis (P = 0.0381; P = 0.0116). In patients with OPLL, a flattening rate of 50% or more was predictive of a better outcome in both surgical groups (P = 0.0457; P = 0.0298).
There were more studies that analyzed important MRI SI characteristics than anatomic properties. Figure 3 is a summary figure illustrating various cord signal change properties.
Six studies considered the prognostic value of high SI changes on T2WI.13,31,34–37 Chibbaro et al34 and Setzer et al31 evaluated the relationship between SI changes on T2WI and postoperative mJOA score. Setzer et al31 found no significant differences between the “unchanged,” “improvement,” and “deterioration” groups when exploring the impact of T2WI SI. Chibbaro et al,34 on the contrary, concluded using multivariate analysis that a high SI on a T2WI was significantly correlated with a higher postoperative mJOA (P < 0.01). Three studies examined the impact of T2WI SI changes on outcome assessed by JOA recovery rate.35–37 In a study by Yamazaki et al,35 T2WI SI changes were not significantly different between the “excellent” and “fair” recovery outcome groups in the younger (P = 0.848) or elderly population (P = 0.051). Both Wada et al36 and Nakashima et al37 confirmed this nonsignificant association between T2WI SI and outcome using multivariate analysis. Nakashima et al37 also considered the effect of T2WI SI change on a second outcome measure, lower limb function section of the JOA Cervical Myelopathy Evaluation Questionnaire (JOACMEQ-L). Neither univariate (OR: 0.5, CI: 0.19–1.33; P = 0.164) analysis nor multivariate (OR: 0.39, CI: 0.13–1.18; P = 0.98) analysis yielded a significant association. Finally, in a study by Suri et al,13 there was no significant difference in the motor (OR: 1.26, 0.82–9.81; P = NS), sensory, autonomic, or disability outcome (OR: 0.79, CI: 1.79–7.61; P = NS) in patients with T2WI SI change and those without.13
High SI grade on T2WI was also examined as a prognostic factor by 4 studies.29,30,32,38 A grade of 0 was defined as no intramedullary high SI, grade 1 as predominantly faint and indistinct border, and grade 2 as predominantly intense and well-defined border. Uchida et al32 also included a fourth grade in their definition: cystic formation. In the study by Chen et al,29 patients with grade 2 had the worst outcome (P < 0.001, R = −33.302), and no significant difference was detected between grade 0 and grade 1. The study by Shin et al30 observed a statistically significant difference in recovery rate among these 3 signal change groups (P = 0.002). Vedantam et al38 determined that the presence of grade 2 signal change was associated with a decreased probability of cure (Nurick grade of 0 or 1, OR: 0.48, CI: 0.2–0.9; P = 0.04). Grade 1 signal, on the contrary, was not predictive of either improvement in Nurick grade (OR: 0.7, CI: 0.3–1.5, P = 0.41) or cure (OR: 1.4, CI: 0.7–2.7; P = 0.23). Uchida et al32 did not find any relationship between SI grade and postoperative JOA score in patients with spondylosis or OPLL.
Low SI change on a T1WI was analyzed as a prognostic factor by Chibbaro et al.34 This study reported that patients with a low SI change on a T1WI had a lower postoperative mJOA (P < 0.05).
Four studies further examined the predictive value of SI characteristics by looking at a combined T1/T2 signal change.13,38–40 Kim et al39 identified this predictor as an important risk factor for poor outcome on JOA using both univariate (OR: 3.02, CI: 1.56–5.32) and multivariate (OR: 2.53, CI: 1.67–5.95) logistic regression analysis. Suda et al40 also identified combined T1/T2 signal change as a risk factor for poor outcome, defined as a JOA recovery rate of less than 50% (univariate: OR: 3.25, CI: 1.34–7.91, P < 0.01; multivariate: OR: 4.10, CI: 1.51–11.12, P < 0.01). Suri et al13 reported that patients without SI changes had a significantly better outcome with respect to motor improvement than patients with a combined T1/T2 SI (OR: 5.1, CI: 1.87–25.1; P < 0.001). This was not the case when assessing disability outcome on the Nurick grade. When examining predictors of a Nurick grade of 0 or 1, however, Vedantam et al38 reported that patients with T1/T2 SI had a lower probability of achieving this Nurick outcome.
Okada et al,28 Wang et al,41 and Zhang et al16,17 explored the predictive value of SI ratio on surgical outcome. Okada et al28 defined SI ratio by dividing the SI at the site of maximal compression on a T2WI by readings at adjacent noncompressed sites. JOA recovery rate was highly correlated with SI ratio in the OPLL (r = 0.53) and CSM (r = 0.426) groups and was included in the final multiple regression equation for all 3 degenerative diseases. Wang et al41 and Zhang et al,16 on the contrary compared T2WI SI at sites of compression with SI at C7–T1 levels. In both studies, patients were divided into groups according to their SI ratio: group 1, low SI ratio; group 2, middle SI ratio; and group 3, high SI ratio. Recovery rates in group 1, group 2, and group 3 were significantly different (P < 0.0001). SI ratio was identified as an important predictor and included in the final regression equations in both studies. Finally, Zhang et al17 analyzed the prognostic value of SI ratio by comparing the SI on T2WI with the T1WI at the same spinal cord level and over a similar area. Patients were split into 2 groups on the basis of the media T2:T1 ratio: group 2 (1.18–1.74, n = 18) and group 3 (1.79–2.77, n = 18). There was a significant difference between these 2 groups with respect to the recovery rate (32.6 ± 14.4 vs. 21.9 ± 8.3, P < 0.001) and postoperative JOA score (12.3 ± 1.6 vs. 10.8 ± 1.5, P < 0.001). T2:T1 ratio was also included in the final regression equation.
The length of the SI on a T2WI was assessed by a single study.30 This variable was not identified as a significant prognostic factor (P = 0.0961) of outcome evaluated by the JOA recovery rate.
Park et al33 reported that number of high-intensity segments was negatively correlated with recovery rate (R = −0.289; P = 0.0063) and included it in the multivariate regression model. Wada et al36 confirmed this finding by observing that patients in the focal group had better recovery rate and postoperative JOA score (56.1 ± 22.2, 14.3 ± 1.0) than the multisegmental group (38.8 ± 14.7, 12.6 ± 18) (P < 0.01).
Are There Characteristics of the MRI That Predict Adverse Events?
This review found no studies commenting on predictors of adverse events.
There is no direct evidence suggesting that MRI characteristics can be used to direct treatment and improve outcomes. Indirect evidence from studies identifying MRI characteristics that are predictive of poor outcome in patients treated conservatively is insufficient. There is, however, low evidence suggesting that high SI grade on T2WI is not associated with patient deterioration throughout conservative treatment.
There is insufficient evidence identifying MRI anatomic characteristics, including cervical curvature, transverse area, number of compressed segments, and flattening rate, as important predictors of surgical outcome. Compression ratio and diameter of the canal were not associated with surgical outcome (low evidence).
There is low evidence suggesting that high SI on T2WI is not an important prognostic factor. A combined T1/T2 signal change, SI ratio, and a greater number of SI segments on T2WI were found to be negatively associated with outcome assessed by a wide range of measures. The strength of evidence for these findings was low. Conclusions could not be drawn on the predictive value of SI grade on T2WI, low SI changes on T1WI, and length of SI on T2WI (Table 7).
MRI is a noninvasive technique routinely used to confirm the diagnosis of CSM, evaluate cord compression because of canal stenosis, and identify any intramedullary signal changes.6,42 It is also a valuable tool to exclude differential diagnoses, because it can visualize parenchymal abnormalities including neoplasms, demyelinating plaques, and syringomyelia.44 It should be noted, however, that patients with metallic foreign body in their eye, aneurysm clips, embedded wires, stimulators or batteries, nitroglycerin patches, pacemakers, or severe claustrophobia cannot be examined by MRI. Computed tomographic myelography is the preferred alternative diagnostic modality for patients with contraindications to MRI.2
The major objective of this study was to determine the value of MRI as a prognostic tool for both conservative and operative treatment approaches. It is essential to define reliable predictors of patient deterioration, particularly in mild cases, in order to delineate the patient cohort that should be considered for upfront surgical intervention versus those that could be safely subjected to longitudinal clinical follow-up and thus avoid surgery. In a prospective analysis of important clinical predictors, the odds of a successful outcome (mJOA ≥16) decreased by 22% when a patient moved from a shorter to a longer duration of symptoms group (<3, 3–6, 6–12, 12–24, and >24 mo). Given the importance of surgical timing, it is thus valuable to determine any objective evidence that may classify which patients will likely require surgery in the future.25–27 From our review, we can only conclude that high SI on a T2WI is not predictive of failure of conservative treatment. Patients may tolerate spinal cord compression differently; some may have high SI on a T2WI but be completely asymptomatic.45 There are discrepancies between MRI findings and the presentation of signs and symptoms, thereby making it difficult to predict deterioration using imaging characteristics.
There is controversy in the literature surrounding the ability of MRI to predict surgical outcome and whether it is canal dimensions or cord properties that are more significant. In a preliminary survey of 325 members of the AOSpine International community, 87.66% answered that the MRI is indeed a prognostic tool and 83.33% responded that cord characteristics are more important than canal measurements. These results support the findings from our review as no anatomic factor was found to be associated with outcome.
A high SI on T2WI reflects a broad spectrum of compressive pathologies and a wide range of recuperative potentials.13,17,38,41,46 T2WI SI is nonspecific and may indicate either reversible damage including edema and ischemia or irreversible changes similar to T1WI, such as necrosis, myelomalacia, and cavitation.13,33,36,38,41,46,47 If the SI reflects more minor pathological changes that will likely diminish postsurgery, then it is not an important prognostic factor. Chen et al29 and Vedantam et al38 recognized the need to separate T2 signal changes into grades: type 1 or “faint, fuzzy, indistinct borders” was more representative of reversible changes whereas type 2 or “intense, well-defined borders” signified irreversible histological damage. These definitions were based on a histopathologic spinal cord study that reported that severe changes (microcavitation, spongiform changes, and necrosis) have a higher water content, resulting in more intense borders. Milder histological damage, such as edema, demyelination, and Wallerian degeneration, on the contrary, produces fainter borders. Both studies demonstrated improvements in SI in type 1 postsurgically, confirming that milder signal changes are reversible. Grading of the T2WI SI allows for an assessment of the amount of irreversible damage. Unfortunately, there is no standard method of classifying these changes or an approach to quantify the degree of signal change.
Based on this review, patients with a greater number of segments with high SI on T2WI had a poor prognosis. The recovery rate of patients with focal SI did not differ from those without SI.17,46 Patients with multisegmental involvement, however, had a recovery rate similar to patients with a T1-signal change and a worse recovery rate than the focal group. Wada et al36 also noted a correlation between multisegmental areas on T2WI and low SI on T1WI.36 Histologically, a greater number of segments with signal change reflect more severe and irreversible damage than a focal signal change.13,36
Although less prevalent, combined T1/T2 signal change was an important predictor of outcome. This type of SI is indicative of severe histological damage including cystic necrosis, secondary syrinx, and cavitation.13,17,33,36,38 SI at the site of compression as well as at an unaffected level, however, differs from patient to patient. Three studies addressed this issue by creating a ratio comparing SI at compressed and noncompressed sites or by comparing SI on T2WI and T1WI.16,17,41 SI ratio was found to be an important prognostic factor.
It is clear from this review that there is a lack of evidence in the form of high-quality prospective studies using validated outcome measures. Other studies have neglected to control for important confounders when assessing the relationship between predictor and outcome. It is also important to note that the definitions of CSM varied from study to study: 8 studies enrolled only patients with CSM; 5 studies included patients with OPLL or CSM; 2 studies specified cervical myelopathy as the diagnosis and did not provide further explanation; 1 study explored patients only with OPLL; and 1 study examined patients with OPLL, CSM, and disc herniation separately. In addition, approximately 40% of the studies were conducted in Japan, where the prevalence of OPLL is higher than in Western populations. These studies may be considered flawed because of a heterogeneous patient population.
Unfortunately, the scaling of SI changes has not been universally quantified or agreed upon. From the studies that have assessed high SI on T2WI, it does seem that the type of methodology impacted the ability to establish a relationship to prognosis. Although T2WI SI changes may not relate to prognosis when measured simply for presence/absence, or subjectively as has been done by previous authors,29,32 more modern and objective approaches that have stratified SI into grades on the basis of calculated SI ratios have been effective in providing prognostic insights. Accordingly, further research, in the form of prospective data and with larger patient groups are necessary to determine the role of T2WI SI changes more conclusively. No further systematic reviews should be conducted until a reliable and valid method to quantify SI changes is devised.
A major issue is that most of the tools used to evaluate outcome in these studies are too crude and may not be able to detect all functional improvements, especially in milder patients. Results often differ depending on the outcome measure: this was the case in a systematic review of important clinical factors.18 For example, baseline severity score was found to be significantly associated with outcome on both the mJOA and Nurick scores. Outcome was positively correlated with baseline mJOA but the direction of the association was unclear on the Nurick score. The mJOA has also not been validated, thus reducing the overall level of evidence of studies using this scale. Traditional measures such as the mJOA and Nurick scores should be used in combination with more sensitive and specific measures, including the walking test, grip strength, and the Berg Balance Scale. The use of a wider range of functional and impairment tests may help better define the prognostic value of certain MRI characteristics.
Diffusion tensor imaging (DTI) is a relatively new neuroimaging technique based on magnetic resonance. It assesses the structural integrity of white matter tracts by evaluating diffusion rates of extracellular water molecules through tissue.45,48–50 DTI measures 2 key parameters: the apparent diffusion coefficient (ADC) and the fractional anisotropy (FA).50 Several studies reported significant differences in these 2 measurements between a control and myelopathic group: the FA at the level of compression was significantly lower and the ADC was significantly higher in the patient group.45,48–50 This form of imaging seems to be more sensitive and specific than the MRI and can detect damage to the white matter tracts before a high signal lesion appears on T2WI.45,51 For example, in a study by Lee et al,50 4 patients who had no abnormal signal changes on the MR image also had lower FA values and higher ADC values. Another one of the possible advantages of the DTI is that it may be able to distinguish between a symptomatic and asymptomatic group of patients.45 In a study by Kerkovsky et al,45 the FA values were significantly lower and the ADC values were significantly higher in a symptomatic group than in an asymptomatic spondylotic cervical cord encroachment subgroup.
With respect to outcome prediction, Jones et al52 and Nakamura et al53 assessed the correlation between various DTI parameters and postsurgical outcome. Jones et al52 reported a significant positive association between baseline FA measures and outcome evaluated by NDI but not by Nurick grade or mJOA. When stratifying the patient population on the basis of mJOA scores, the results were slightly different. For patients with a mJOA score of 8, lower FA values were predictive of a worse outcome: for every 0.1-point increase in FA, the odds of improving were 1.5 times greater. In a second study by Nakamura et al,53 the fiber tract ratio, calculated by dividing the number of fibers at the compressed level by the number of fibers at the C2-level, was correlated with the JOA recovery rate (r = 0.6066, P = 0.0046). Patients with a fiber tract ratio below 60% typically had a poor recovery rate of less than 40%. Further studies are required to evaluate the prognostic value of the DTI.
This study attempted to identify important MRI predictors of failed conservative treatment and surgical outcome by synthesizing evidence from the literature. Based on low evidence, patients with high SI changes on T2WI combined with low SI changes on T1WI, a high SI ratio (compressed vs. noncompressed C7–T1) on T2WI, high SI ratio on T2/T1WI, and a greater number of high SI segments on T2WI are likely to have poorer neurological outcomes after surgery.
Evidence-Based Clinical Recommendations.
Recommendation 1. We suggest that when clinically feasible, surgeons rely on MRI to confirm the diagnosis of CSM and rely on clinical history and examination to determine progression and severity of disease.
Overall Strength of Evidence. Low
Strength of Recommendation. Weak
Recommendation 2. T2 signal may be a useful prognostic indicator when used in combination with low SI change on T1WI, or as a ratio comparing compressed versus non-compressed segments, or as a ratio of T2 compared with T1WI. We suggest that if surgeons use MRI signal intensity to estimate the risk of a poor outcome following surgery, they use high SI change on T2WI in combination with other signal intensity parameters, and not in isolation.
Overall Strength of Evidence. Low
Strength of Recommendation. Weak
- Cervical spondylotic myelopathy is the most common cause of spinal cord dysfunction worldwide. MRI is routinely used to confirm its diagnosis and assess the degree of stenosis and cord compression.
- A systematic review was conducted to determine whether there are any MRI characteristics that affect treatment decisions or predict postsurgical outcomes or adverse events.
- A high SI grade on a T2WI is not associated with patient deterioration during conservative treatment. This conclusion, however, was only based on low-level evidence.
- Preoperative compression ratio and canal diameter were not associated with surgical outcome, based on low-level evidence.
- High SI on a T2WI is not an important prognostic factor. A combined T1/T2 signal change, SI ratio, and a greater number of SI segments on a T2WI were found to be negatively associated with outcome.
Author contributions are as follows: L.T.: Study design, data analysis and interpretation, manuscript preparation, and manuscript revision; J.R.W.: Data interpretation, clinical guidance, and manuscript revision; A.S.: Data interpretation and manuscript revision; M.G.F.: Data interpretation, clinical guidance, and manuscript revision; A.N.: Manuscript preparation and revision; E.D.B.: Data analysis and synthesis, manuscript preparation, and manuscript revision; J.R.D.: Study design, data analysis and interpretation, manuscript preparation, and manuscript revision; and W.B.J.: Study design, data analysis and interpretation, clinical guidance manuscript preparation, and manuscript revision.
Supplemental digital content is available for this article. Direct URL citations appearing in the printed text are provided in the HTML and PDF version of this article on the journal's web site (www.spinejournal.com).
1. Young WF. Cervical spondylotic myelopathy: a common cause of spinal cord dysfunction in older persons. Am Fam Phys 2000;62:1064–70, 1073.
2. Tracy JA, Bartleson JD. Cervical spondylotic myelopathy. Neurolog 2010;16:176–87.
3. Baptiste DC, Fehlings MG. Pathophysiology of cervical myelopathy. Spine J 2006;6:S190–7. doi: http://dx.doi.org/10.1016/j.spinee.2006.04.024
4. Kalsi-Ryan S, Karadimas SK, Fehlings MG. Cervical spondylotic myelopathy: the clinical phenomenon and the current pathobiology of an increasingly prevalent and devastating disorder [November 30, 2012]. Neuroscientist 2013;19:409–21. doi:10.1177/1073858412467377.
5. Yue WM, Tan SB, Tan MH, et al. The Torg–Pavlov ratio in cervical spondylotic myelopathy: a comparative study between patients with cervical spondylotic myelopathy and a nonspondylotic, nonmyelopathic population. Spine 2001;26:1760–4.
6. Nagata K, Kiyonaga K, Ohashi T, et al. Clinical value of magnetic resonance imaging for cervical myelopathy. Spine 1990;15:1088–96.
7. Tanaka N, Fujimoto Y, Yasunaga Y, et al. Functional diagnosis using multimodal spinal cord evoked potentials in cervical myelopathy. J Orthop Sci 2005;10:3–7.
8. Lo YL. The role of electrophysiology in the diagnosis and management of cervical spondylotic myelopathy. Ann Acad Med Singapore 2007;36:886–93.
9. Ebersold MJ, Pare MC, Quast LM. Surgical treatment for cervical spondylitic myelopathy. J Neurosurg 1995;82:745–751.
10. King JT Jr, Moossy JJ, Tsevat J, et al. Multimodal assessment after surgery for cervical spondylotic myelopathy. J Neurosurg Spine 2005;2:526–34.
11. Morio Y, Teshima R, Nagashima H, et al. Correlation between operative outcomes of cervical compression myelopathy and MRI of the spinal cord. Spine 2001;26:1238–1245. doi:http://dx.doi.org/10.1097/00007632-200106010-00012
12. Rajshekhar V, Kumar CSS. Functional outcome after central corpectomy in poor-grade patients with cervical spondylotic myelopathy or ossified posterior longitudinal ligament. Neurosurgery 2005;56:1279–84. doi:http://dx.doi.org/10.1227/01.NEU.0000159713.20597.0F
13. Suri A, Chabbra RPS, Mehta VS, et al. Effect of intramedullary signal changes on the surgical outcome of patients with cervical spondylotic myelopathy. Spine J 2003;3:33–45.
14. Suzuki A, Misawa H, Simogata M, et al. Recovery process following cervical laminoplasty in patients with cervical compression myelopathy: prospective cohort study. Spine 2009;34:2874–9. doi:http://dx.doi.org/10.1097/BRS.0b013e3181bb0e33
15. Tanaka J, Seki N, Tokimura F, et al. Operative results of canal-expansive laminoplasty for cervical spondylotic myelopathy in elderly patients. Spine 1999;24:2308–12.
16. Zhang Y-Z, Shen Y, Wang L-F, et al. Magnetic resonance T2 image signal intensity ratio and clinical manifestation predict prognosis after surgical intervention for cervical spondylotic myelopathy. Spine 2010;35:E396–9.
17. Zhang P, Shen Y, Zhang Y-Z, et al. Significance of increased signal intensity on MRI in prognosis after surgical intervention for cervical spondylotic myelopathy. J Clin Neurosci 2011;18:1080–3.
18. Tetreault LA, Karpova A, Fehlings MG. Predictors of outcome in patients with degenerative cervical spondylotic myelopathy undergoing surgical treatment: results of a systematic review. Eur Spine J 2013. doi:10.1007/s00586-013-2658-z.
19. Holly LT, Matz PG, Anderson PA, et al. Clinical prognostic indicators of surgical outcome in cervical spondylotic myelopathy. J Neurosurg Spine 2009;11:112–8. doi:10.3171/2009.1.spine08718.
20. Wright JG, Swiontkowski MF, Heckman JD. Introducing levels of evidence to the journal. J Bone Joint Surg Am 2003;85-A:1–3.
21. Skelly AC, Hashimoto RE, Norvell DC, et al. Cervical Spondylotic Myelopathy: Methodological Approaches to Evaluate the Literature and Establish Best Evidence. Spine 2013;38:S9–18.
22. Atkins D, Best D, Briss PA, et al. Grading quality of evidence and strength of recommendations. BMJ 2004;328:1490.
23. West S, King V, Carey TS, et al. Systems to Rate the Strength of Scientific Evidence. Rockville, MD: Agency for Healthcare Research and Quality; 2002. Evidence Report/Technology Assessment No. 47 (Prepared by the Research Triangle Institute-University of North Carolina Evidence-based Practice Center, Contract No. 290-97-0011).
24. Owens DK, Lohr KN, Atkins D, et al. AHRQ series paper 5: grading the strength of a body of evidence when comparing medical interventions—Agency for Healthcare Research and Quality and the effective health-care program. J Clin Epidemiol 2010;63:513–23.
25. Oshima Y, Seichi A, Takeshita K, et al. Natural course and prognostic factors in patients with mild cervical spondylotic myelopathy with increased signal intensity on T2-weighted magnetic resonance imaging. Spine (Phila Pa 1976) 2012;37:1909–13.
26. Yoshimatsu H, Nagata K, Goto H, et al. Conservative treatment for cervical spondylotic myelopathy. Prediction of treatment effects by multivariate analysis. Spine J 2001;1:269–73.
27. Shimomura T, Sumi M, Nishida K, et al. Prognostic factors for deterioration of patients with cervical spondylotic myelopathy after nonsurgical treatment. Spine 2007;32:2474–9.
28. Okada Y, Ikata T, Yamada H, et al. Magnetic resonance imaging study on the results of surgery for cervical compression myelopathy. Spine 1993;18:2024–9.
29. Chen CJ, Lyu RK, Lee ST, et al. Intramedullary high signal intensity on T2-weighted MR images in cervical spondylotic myelopathy:prediction of prognosis with type of intensity. Radiology 2001;221:789–94.
30. Shin JJ, Jin BH, Kim KS, et al. Intramedullary high signal intensity and neurological status as prognostic factors in cervical spondylotic myelopathy. Acta Neurochir (Wien) 2010;152:1687–94.
31. Setzer M, Vrionis FD, Hermann EJ, et al. Effect of apolipoprotein E genotype on the outcome after anterior cervical decompression and fusion in patients with cervical spondylotic myelopathy: Clinical article. J Neurosurg Spine 2009;11:659–66. doi:http://dx.doi.org/10.3171/2009.7.SPINE08667
32. Uchida K, Nakajima H, Sato R, et al. Multivariate analysis of the neurological outcome of surgery for cervical compressive myelopathy. J Orthop Sci 2005;10:564–73.
33. Park Y-S, Nakase H, Kawaguchi S, et al. Predictors of outcome of surgery for cervical compressive myelopathy: retrospective analysis and prospective study. Neurol Med Chir (Tokyo) 2006;46:231–8; discussion 238–9.
34. Chibbaro S, Benvenuti L, Carnesecchi S, et al. Anterior cervical corpectomy for cervical spondylotic myelopathy: experience and surgical results in a series of 70 consecutive patients. J Clin Neurosci 2006;13:233–38. doi:http://dx.doi.org/10.1016/j.jocn.2005.04.011
35. Yamazaki T, Yanaka K, Sato H, et al. Cervical spondylotic myelopathy: surgical results and factors affecting outcome with special reference to age differences. Neurosurgery 2003;52:122–6.
36. Wada E, Yonenobu K, Suzuki S, et al. Can intramedullary signal change on magnetic resonance imaging predict surgical outcome in cervical spondylotic myelopathy? Spine 1999;24:455–62. doi:http://dx.doi.org/10.1097/00007632-199903010-00009
37. Nakashima H, Yukawa Y, Ito K, et al. Prediction of lower limb functional recovery after laminoplasty for cervical myelopathy: focusing on the 10-s step test. Eur Spine J 2012;21:1389–95. doi:http://dx.doi.org/10.1007/s00586-012-2241-z
38. Vedantam A, Jonathan A, Rajshekhar V. Association of magnetic resonance imaging signal changes and outcome prediction after surgery for cervical spondylotic myelopathy. J Neurosurg Spine 2011;15:660–66. doi:http://dx.doi.org/10.3171/2011.8.SPINE11452
39. Kim HJ, Moon SH, Kim HS, et al. Diabetes and smoking as prognostic factors after cervical laminoplasty. J Bone Joint Surg Br 2008;90:1468–72. doi:http://dx.doi.org/10.1302/0301-620X.90B11.20632
40. Suda K, Abumi K, Ito M, et al. Local kyphosis reduces surgical outcomes of expansive open-door laminoplasty for cervical spondylotic myelopathy. Spine 2003;28:1258–62.
41. Wang L-F, Zhang Y-Z, Shen Y, et al. 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 2010;13:319–23. doi:http://dx.doi.org/10.3171/2010.3.SPINE09887
42. Zhang L, Zeitoun D, Rangel A, et al. Preoperative evaluation of the cervical spondylotic myelopathy with flexion-extension magnetic resonance imaging: about a prospective study of fifty patients. Spine 2011;36:E1134–9. doi:http://dx.doi.org/10.1097/BRS.0b013e3181f822c7
43. Benzel EC, Lancon J, Kesterson L, et al. Cervical laminectomy and dentate ligament section for cervical spondylotic myelopathy. J Spinal Disord 1991;4:286–295.
44. Harrop JS, Naroji S, Maltenfort M, et al. Cervical myelopathy: a clinical and radiographic evaluation and correlation to cervical spondylotic myelopathy. Spine 2010;35:620–4. doi:http://dx.doi.org/10.1097/BRS.0b013e3181b723af
45. Kerkovsky M, Bednarik J, Dusek L, et al. Magnetic resonance diffusion tensor imaging in patients with cervical spondylotic spinal cord compression: correlations between clinical and electrophysiological findings. Spine 2012;37:48–56. doi:http://dx.doi.org/10.1097/BRS.0b013e31820e6c35
46. Fernandez de Rota JJ, Meschian S, Fernandez de Rota A, et al. Cervical spondylotic myelopathy due to chronic compression: the role of signal intensity changes in magnetic resonance images. J Neurosurg Spine 2007;6:17–22.
47. Yagi M, Ninomiya K, Kihara M, et al. Long-term surgical outcome and risk factors in patients with cervical myelopathy and a change in signal intensity of intramedullary spinal cord on magnetic resonance imaging: clinical article. J Neurosurg Spine 2010;12:59–65. doi:http://dx.doi.org/10.3171/2009.5.SPINE08940
48. Budzik J-F, Balbi V, Le Thuc V, et al. Diffusion tensor imaging and fibre tracking in cervical spondylotic myelopathy. Eur Radiol 2011;21:426–33. doi:http://dx.doi.org/10.1007/s00330-010-1927-z
49. Kara B, Celik A, Karadereler S, et al. The role of DTI in early detection of cervical spondylotic myelopathy: a preliminary study with 3-T MRI. Neuroradiology 2011;53:609–16. doi:http://dx.doi.org/10.1007/s00234-011-0844-4
50. Lee JW, Kim JH, Park JB, et al. Diffusion tensor imaging and fiber tractography in cervical compressive myelopathy: preliminary results. Skeletal Radiol 2011;40:1543–51. doi:http://dx.doi.org/10.1007/s00256-011-1161-z
51. Demir A, Ries M, Moonen CTW, et al. Diffusion-weighted MR imaging with apparent diffusion coefficient and apparent diffusion tensor maps in cervical spondylotic myelopathy. Radiology 2003;229:37–43.
52. Jones JG, Cen SY, Lebel RM, et al. Diffusion tensor imaging correlates with the clinical assessment of disease severity in cervical spondylotic myelopathy and predicts outcome following surgery. AJNR Am J Neuroradiol 2013;34:471–78. doi:10.3174/ajnr.A3199.
53. Nakamura M, Fujiyoshi K, Tsuji O, et al. Clinical significance of diffusion tensor tractography as a predictor of functional recovery after laminoplasty in patients with cervical compressive myelopathy. J Neurosurg Spine 2012;17:147–52. doi:10.3171/2012.5.spine1196.