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Differences in clinical outcomes between traumatic cervical myelopathy and degenerative cervical myelopathy: A comparative study of cervical spinal cord injury without major bone injury and cervical spondylotic myelopathy
Journal of Clinical Neuroscience 70 (2019) 127–131
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Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical study
Differences in clinical outcomes between traumatic cervical myelopathy and degenerative cervical myelopathy: A comparative study of cervical spinal cord injury without major bone injury and cervical spondylotic myelopathy Masaaki Machino a, Kei Ando a, Kazuyoshi Kobayashi a, Masayoshi Morozumi a, Satoshi Tanaka a, Keigo Ito b, Fumihiko Kato b, Naoki Ishiguro a, Shiro Imagama a,⇑ a b
Department of Orthopedic Surgery, Nagoya University Graduate School of Medicine, Nagoya, Japan Department of Orthopedic Surgery, Chubu Rosai Hospital, Japan Organization of Occupational Health and Safety, Nagoya, Japan
a r t i c l e
i n f o
Article history: Received 11 June 2019 Accepted 6 August 2019
Keywords: Clinical outcomes Traumatic cervical myelopathy Degenerative cervical myelopathy Comparative study Cervical spinal cord injury without major bone injury Cervical spondylotic myelopathy
a b s t r a c t A comparative study to examine the surgical outcomes of traumatic cervical myelopathy (TCM) patients was designed. The study aim was to compare the surgical outcomes between TCM and degenerative cervical myelopathy (DCM) and to characterize the preoperative symptoms and postoperative residual symptoms in TCM patients. One hundred consecutive patients with TCM (81 men, 19 women; mean age, 57.7 years; range, 31–79 years) and 100 consecutive patients with DCM (88 men, 12 women; mean age, 58.4 years; range, 36–78 years) were included in this study. All patients were treated by laminoplasty. The pre- and postoperative neurological statuses were evaluated according to the Japanese Orthopaedic Association (JOA) scoring system for cervical myelopathy. The recovery rate (RR) of each function was compared between the two groups. The mean preoperative JOA scores of motor function of the upper extremity in the TCM and DCM groups were 1.9 and 2.3, respectively (P < 0.01). After surgery, the mean RRs of motor function of the upper extremity in the TDM and DCM groups were 36.4% and 55.7%, respectively (P < 0.01) and in the lower extremity were 32.3% and 46.5%, respectively (P < 0.05). The RR for sensory function of the lower extremity was significantly lower in TCM patients than in DCM patients (39.6 vs 68.2, respectively; P < 0.0001). Motor function impairments of the upper and lower extremities and sensory function impairments of the lower extremities after surgery were more persistent in the TCM group than in the DCM group. Ó 2019 Elsevier Ltd. All rights reserved.
1. Introduction Over the last decades, population aging has caused the incidence of spinal stenosis to rise, which has led to a consequent increase in cases of traumatic cervical myelopathy (TCM) caused by minor trauma [1]. TCM is a syndrome that involves spinal cord injury without evidence of spinal fracture or dislocation on plain radiography or computed tomography (CT) [2]. Surgical treatment of cervical myelopathy is aimed at decompressing the spinal cord to prevent further damage [3]. Although some neurological function can be recovered after surgery, a degree of irreversible neurological damage is unavoidable [4,5]. ⇑ Corresponding author at: Department of Orthopaedic Surgery, Nagoya University Graduate School of Medicine, 65, Tsurumai, Showa-ku, Nagoya, Aichi 466-8550, Japan. E-mail address: [email protected] (S. Imagama). https://doi.org/10.1016/j.jocn.2019.08.054 0967-5868/Ó 2019 Elsevier Ltd. All rights reserved.
Traumatic damage of the spinal cord might reflect poor outcomes with a lower recuperative potential [6]. The surgical outcome of laminoplasty might be worse in TCM patients than in degenerative cervical myelopathy (DCM) patients. Recovery of spinal cord function may be insufficient in TCM because of increased vulnerability of the spinal cord; therefore, surgical treatment of TCM patients has become a great concern [7–9]. To determine the best treatment for TCM, it is important to understand the differences in the characteristics of preoperative impairments and postoperative residual symptoms between TCM and DCM patients. However, no report has described the particular residual symptoms following surgery in TCM patients. We hypothesized that patients with TCM that occurs rapidly have more severe symptoms preoperatively and poorer outcomes postoperatively than those of patients with DCM that occurs slowly. Therefore, we designed a prospective comparative study
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MRI and myelography findings were consistent with myelopathy secondary to multisegmental cervical spondylotic stenosis. All patients exhibited myelopathy, which was confirmed by a physical examination, and cord compression was present between C2/C3 and C7/T1 disk levels (Fig. 1). Differences in the following parameters were evaluated among the two groups: age, sex, prevalence of diabetes, prevalence of hypertension, smoking history, and postoperative follow-up duration. This study was approved by the Institutional Review Board, and written informed consent was obtained from each patient prior to study participation or surgery. 2.2. Surgical technique for modified double-door laminoplasty
Fig. 1. Representative sagittal views in T2-weighted MRI before surgery of traumatic cervical myelopathy (TCM) and degenerative cervical myelopathy (DCM).
to examine the surgical outcomes of TCM patients from a single surgery. The purpose of this study was to compare the surgical outcomes between TCM and DCM and to characterize the preoperative symptoms and postoperative residual symptoms in TCM patients. 2. Material and methods 2.1. Study population 2.1.1. Patients with TCM One hundred consecutive TCM patients with cervical spinal cord injury (SCI) without major bone injury (81 men and 19 women; mean age, 57.7 years; range, 31–79 years) were enrolled. All patients underwent preoperative functional X-ray in the acute phase. The exclusion criteria were as follows: (1) presence of ossification of the posterior longitudinal ligament (OPLL); (2) history of rheumatoid arthritis, cerebral palsy, or tumors; (3) fracture or traumatic instability, such as dislocation/subluxation; (4) destructive spondyloarthritis due to hemodialysis; (5) previous cervical surgery; (6) spinal fusion with instrumentation; (7) thoracic spondylotic myelopathy; and (8) lumbar spinal canal stenosis. All patients presented symptoms of TCM and magnetic resonance imaging (MRI) findings consistent with symptoms secondary to cervical spinal canal stenosis. For each patient, TCM was confirmed by physical examination and MRI-confirmed cord compression between the C2/C3 and C7/T1 disk levels. Patients with profound neurological deficits and persistent spinal cord compression due to cervical spinal canal stenosis were indicated for surgery. The mean period from injury to operation was 18.4 ± 3.5 days. 2.1.2. DCM (Controls) One hundred consecutive DCM patients with cervical spondylotic myelopathy (CSM) (88 men and 12 women; mean age, 58.4 years; range, 36–78 years) were included in this study. The exclusion criteria were as follows: (1) presence of OPLL; (2) history of rheumatoid arthritis, cerebral palsy, or tumors; (3) spinal injuries; (4) destructive spondyloarthritis due to hemodialysis; (5) previous cervical surgery; (6) spinal fusion with instrumentation; (7) thoracic spondylotic myelopathy; and (8) lumbar spinal canal stenosis. All patients presented with symptoms of myelopathy.
All patients were treated by double-door laminoplasty, as described by Kurokawa, with some modifications [10,11]. The muscles attached to the C2 spinous process were preserved without detachment. Surgical exposure was limited as much as possible. The spinous processes between C3 and C7 were resected at their bases, and the laminae were cut at the center by using a high-speed drill. Bilateral gutters were created as hinges at the border between the laminae and facets in a manner that was slightly more medial than originally described, thus minimizing the invasion of facets [12]. After elevating the halves of the laminae (similar to opening a French door), bone graft struts (16–18 mm long) created from the C6 or C7 spinous process were tied to bridge the bilateral edges of the laminae. 2.3. Postoperative considerations All patients were allowed to sit up and walk on postoperative day 1 while wearing a Philadelphia collar. The collars were fitted for all patients, but they were allowed to remove them at their discretion. The cervical range of motion exercises were performed as soon as possible during the rehabilitation program. The ideal spinal alignment was explained to all patients after surgery. 2.4. Clinical outcome Operative time and blood loss were assessed. The pre- and postoperative severities of myelopathy were evaluated according to a scoring system proposed by the Japanese Orthopaedic Association (JOA) for cervical myelopathy [13]. The postoperative JOA score was assessed during the final follow-up. The JOA score quantifies neurological impairment by evaluating motor function in the upper and lower extremities (four points each), sensory function in the upper and lower extremities as well as in the trunk sensibility (two points each, total six), and urinary bladder function (three points). Thus, a perfect JOA score for cervical myelopathy is 17 points (Table 1). The recovery rate (RR) of the JOA score was calculated by using the formula suggested by Hirabayashi et al (Table 1) [14]. [RR = postoperative preoperative JOA scores)/(17 preoperative JOA score) 100%]. In addition, the achieved JOA score (postoperative JOA score preoperative JOA score) was also evaluated [15]. Each functional improvement was also expressed by a RR (sub-score RRs), and they were compared between the two groups [16]. 2.5. Statistical analysis Data were analyzed by using SPSS statistical software (version 18.0; SPSS, Inc., Chicago, IL, USA). All values are expressed as a mean ± standard deviation. The Mann–Whitney U test was used to analyze the differences between the two groups. Repeated measures analyses of variance in the same group were performed by using the Wilcoxon test. The chi-square test was used to analyze
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M. Machino et al. / Journal of Clinical Neuroscience 70 (2019) 127–131 Table 1 Evaluation of cervical myelopathy using the scoring system proposed by the Japanese Orthopedic Association (JOA score) and recovery rate of the JOA score. JOA score
Follow-up period (months) Surgery time (minutes) Blood loss (ml) Preoperative JOA score (points) Postoperative JOA score at final follow-up (points) Achieved JOA score (points) Recovery rate of the JOA score (%)
I. Motor function of the upper extremity 0. Impossible to eat with chopsticks or spoon 1. Possible to eat with spoon, but not with chopsticks 2. Possible to eat with chopsticks, but inadequate 3. Possible to eat with chopsticks, awkward 4. Normal II. Motor function of the lower extremity 0. Impossible to walk 1. Needs cane or aid on flat ground 2. Needs cane or aid only on stairs 3. Possible to walk without cane or aid but slowly 4. Normal
TCM
DCM
P value
24.9 ± 18.4 82.6 ± 23.4 62.7 ± 70.0 8.4 ± 3.6 11.5 ± 3.5
25.6 ± 12.5 82.4 ± 26.1 56.6 ± 51.2 8.8 ± 2.0 13.2 ± 2.5
0.7706 0.5949 0.2428 0.2613 <0.001***
3.1 ± 2.3 40.0 ± 26.0
4.3 ± 2.3 53.5 ± 26.2
<0.001*** <0.001***
Values given are mean ± SD unless otherwise specified. JOA score indicates Japanese Orthopaedic Association score for cervical myelopathy; SD, standard deviation; TCM, traumatic cervical myelopathy; DCM, degenerative cervical myelopathy. *Statistically significant values. *p < 0.05, **p < 0.01, ***p < 0.001.
III. Sensory function A. Upper extremity 0. Apparent sensory loss 1. Minimal sensory loss 2. Normal B. Lower extremity (same as A) C. Trunk (same as A) IV. Bladder function 0. Complete retention 1. Severe disturbance (sense of retention, dribbling, incomplete continence) 2. Mild disturbance (urinary frequency, urinary hesitancy) 3. Normal Recovery rate of the JOA score (Hirabayashi method). Recovery rate (%) = [Postoperative score Preoperative score]/[Full score (17) Preoperative score] 100. Achieved JOA score. Achieved score (points) = Postoperative score Preoperative score.
differences between groups. P < 0.05 was considered to be indicative of statistical significance.
3. Results There were no significant differences in the patient demographic data (age, sex). No significant intergroup differences were observed in the prevalence of diabetes, hypertension, and smoking history between both groups (Table 2). The TCM patients underwent expansive laminoplasty, which was performed on C3–C7 in 90 patients and on C3–C6 in 10 patients. In the DCM patients, laminoplasty was performed at the following disk levels: C3–C7 (n = 86) and C3–C6 (n = 14). There were no statistically significant differences in the follow-up period, operation time, or blood loss between the two groups (Table 3). The mean JOA scores in the TCM and DCM groups were 8.4 ± 3.6 and 8.8 ± 2.0 points before surgery and 11.6 ± 3.5 and 13.2 ± 2.5 points at the final postoperative follow-up, respectively. The postoperative JOA scores at the final follow-up were significantly lower in the TCM group than in the DCM group (P < 0.001). The TCM
Table 2 Patient demographics and comorbidities between two groups.
Number of patients Age (years) Gender (Males/Female) Diabetes Hypertension Smoking history
Table 3 Clinical outcomes between two groups.
TCM
DCM
P value
100 57.7 ± 11.0 81/19 15 (15%) 24 (24%) 23 (23%)
100 58.4 ± 9.3 88/12 18 (18%) 28 (28%) 20 (20%)
0.4677 0.2411 0.7037 0.5247 0.7310
Values given are mean ± SD unless otherwise specified. SD indicates standard deviation; TCM, traumatic cervical myelopathy; DCM, degenerative cervical myelopathy.
group showed significantly lower RRs of JOA scores than those of the DCM group (40.1% ± 26.1% vs. 53.5% ± 26.2%, respectively; P < 0.001). The mean achieved JOA scores in the TCM and DCM groups were 3.2 ± 2.4 and 4.4 ± 2.3 points, respectively, with significant difference between the two groups (P < 0.001, Table 3). Before surgery, the mean preoperative JOA scores of motor function in the upper extremity in the TCM and DCM groups were 1.9 ± 1.2 and 2.3 ± 0.9 points, respectively (P = 0.0016). Adversely, the JOA scores of sensory function of the trunk were significantly lower in the DCM group than in the TCM group (1.0 ± 0.9 vs. 1.4 ± 0.8, respectively, P = 0.0016, Table 4). After surgery, the motor function scores for the upper extremity were 2.7 ± 1.1 points (TCM) and 3.3 ± 0.7 points (DCM) at final follow-up (P < 0.0001). The scores of motor and sensory function for the lower extremities were lower in the TCM group than in the DCM group after surgery (P = 0.0039, P = 0.0012, respectively, Table 4). The mean RRs of motor function of the upper extremity in the TDM and DCM groups were 36.4% and 55.7%, respectively (P = 0.005). The RR of lower extremity motor function was significantly lower in the TCM group than in the DCM group (32.3% vs. 46.5%, respectively; P = 0.0108). The TCM patients showed significantly lower RR for sensory function of the lower extremity than that of the DCM patients (39.6% vs. 68.2%, respectively; P < 0.0001, Table 5). 4. Discussion Damage to the spinal cord caused by traumatic injury may influence the surgical outcome. However, the preoperative symptoms and postoperative residual symptoms have not been fully evaluated in TCM patients. This study aimed to compare the surgical outcomes between TCM and DCM and to characterize the preoperative symptoms and postoperative residual symptoms in TCM patients. The TCM patients showed significantly lower JOA scores for motor function of the upper extremity than those of the DCM patients before surgery. After surgery, upper extremity motor function impairments and lower extremity motor and sensory function impairments persisted more than other symptoms in the TCM patients than in the DCM patients. Such findings should be included in the preoperative discussions on the risks and benefits of surgery. The pathophysiology of SCI is best described as biphasic, consisting of a primary and secondary phase of injury [6]. The primary phase involves the initial mechanical injury that directly imparts force to the spinal cord and disrupts axons, blood vessels, and cell membranes. This is followed by the delayed onset of a secondary injury phase involving vascular dysfunction, edema, ischemia, excitotoxicity, electrolyte shifts, free radical production, inflammation, and delayed apoptotic cell death. Whereas neurological defi-
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Table 4 Preoperative and postoperative Japanese Orthopaedic Association scores for each function in the two groups. TCM
DCM
P value
Preoperative JOA score Motor function of the Upper extremity (points) Motor function of the Lower extremity (points) Sensory function of the Upper extremity (points) Sensory function of the Lower extremity (points) Sensory function of the Trunk (points) Bladder function (points)
1.9 ± 1.2 1.9 ± 1.3 0.09 ± 0.3 0.82 ± 0.9 1.4 ± 0.8 2.4 ± 0.9
2.3 ± 0.9 2.1 ± 0.8 0.18 ± 0.4 0.83 ± 0.8 1.0 ± 0.9 2.4 ± 0.6
0.0016** 0.1070 0.0899 0.9346 0.0016** 0.9240
Postoperative JOA score Motor function of the Upper extremity (points) Motor function of the Lower extremity (points) Sensory function of the Upper extremity (points) Sensory function of the Lower extremity (points) Sensory function of the Trunk (points) Bladder function (points)
2.7 ± 1.1 2.6 ± 1.1 0.8 ± 0.7 1.3 ± 0.8 1.7 ± 0.6 2.5 ± 0.8
3.3 ± 0.7 3.0 ± 0.9 1.0 ± 0.8 1.6 ± 0.7 1.6 ± 0.6 2.7 ± 0.5
<0.0001*** 0.0039** 0.1465 0.0012** 0.9675 0.0528
Values given are mean ± SD unless otherwise specified. JOA score indicates Japanese Orthopaedic Association score for cervical myelopathy; SD, standard deviation; TCM, traumatic cervical myelopathy; DCM, degenerative cervical myelopathy. *Statistically significant values. *p < 0.05, **p < 0.01, ***p < 0.001.
Table 5 Recovery rate of the Japanese Orthopaedic Association (JOA) score for each function in the two groups.
Motor function of the Upper extremity (%) Motor function of the Lower extremity (%) Sensory function of the Upper extremity (%) Sensory function of the Lower extremity (%) Sensory function of the Trunk (%) Bladder function (%)
TCM
DCM
P value
36.4 ± 51.1 32.3 ± 34.2 37.0 ± 38.0 39.6 ± 40.4 59.5 ± 47.2 44.2 ± 45.4
55.7 ± 43.9 46.5 ± 41.8 42.9 ± 41.7 68.2 ± 41.9 67.7 ± 38.5 60.2 ± 48.9
0.0050** 0.0108* 0.2654 <0.0001*** 0.2564 0.0753
Values given are mean ± SD unless otherwise specified. SD, standard deviation. *Statistically significant values. *p < 0.05, **p < 0.01, ***p < 0.001.
cits are present immediately following the initial injury, the secondary injury phase results in a protracted period of tissue destruction. TCM is associated with hyperextension injury of the cervical spine and is commonly observed in patients with minor trauma without bony injury and in patients with a pre-existing pathology, such as canal stenosis [13]. The most common of the incomplete SCI syndromes, central cord syndrome, usually results from neck hyperextension in older people with spinal stenosis [17]. In a hyperextension injury, the cord is compressed between the enfolded ligamentum flavum and the vertebral osteophyte [18]. Before surgery, the TCM patients in the present study had a significantly lower JOA score for motor function of the upper extremity than that of the DCM patients. Generally, in patients with TCM, motor function impairments of the upper extremity are caused by central cord syndrome [19]. Because central cord syndrome is usually caused by damage to the cervical spinal cord, it is characterized by weakness in the arms with lesser weakness of the legs and less loss of sensation in regions in which the nerves branch from the sacral segments [20]. There is loss of sensation of pain, temperature, light touch, and pressure below the level of injury. The spinal tracts that serve the arms are more affected because of their central location in the spinal cord, whereas the corticospinal fibers that serve the legs are spared because of their more external location. The pathophysiology of DCM involves static factors, which lead to acquired or developmental stenosis of the cervical canal and dynamic factors that involve repetitive damage to the cervical cord [21]. These mechanical factors in turn result in direct damage to neurons and glia as well as a secondary cascade of events, includ-
ing ischemia, excitotoxicity, and apoptosis [22]. DCM is a common degenerative disease of the spine that is the direct result of spinal cord compression. With age, the spine undergoes natural degenerative changes that can affect its basic anatomy and lead to stenosis of the spinal canal. In the current study, motor function impairments of the upper extremity and motor and sensory function impairments of the lower extremity after surgery were more persistent than other symptoms in the TCM patients than in the DCM patients. TCM causes irreversible paralysis and sensory damage, and it remains controversial as to whether conservative or surgical treatment strategies are best for adult patients with TCM [23,24]. When considering surgery, associated risks should be fully disclosed and explained, and the patient’s general condition should be thoroughly ascertained. To date, no definitive management protocol has been established for TCM. In our institution, we perform radiography and CT to identify cervical spine fractures or dislocations, and when instability is not evident on extension-flexion radiographs, patients are allowed to sit up and walk while wearing a Philadelphia collar. Rehabilitation is then started immediately after injury. Moreover, the role of surgery in TCM patients remains controversial. In our institution, patients with spinal cord compression in delayed MRI are offered cervical laminoplasty to achieve a more favorable outcome and prevent symptom deterioration. On the basis of the results of this study, we speculate that the spinal cord relatively resists chronic pressure to progress slowly by degenerative change. In contrast, the spinal cord might be vulnerable to a sudden on-set contusion because of an injury caused by an external force. A better understanding of both the biological and mechanical mechanisms that cause TCM will significantly
M. Machino et al. / Journal of Clinical Neuroscience 70 (2019) 127–131
improve physicians’ ability to treat patients diagnosed with this disease and decrease the prevalence of patients suffering from spinal cord impairment. There were some limitations in our study. The follow-up duration was relatively brief, and patient-based objective outcomes, such as quality of life determined by using the Short-Form Health Survey 36, subjective satisfaction, and axial back pain measured by using the visual analog scale, were not assessed. Objective measures should be added in future studies. In this study, we used only the JOA scores for to assess neurological function. However, many previous investigators have used the JOA scoring system and its RR to evaluate outcomes [12–14]. We did not compare the surgical outcomes in the patients who underwent double-door laminoplasty and those who underwent either anterior or posterior surgery. Despite these limitations, these findings provide baseline data that may help clinicians accurately assess preoperative impairments and postoperative outcomes in patients with TCM. 5. Conclusion This study investigated the surgical outcomes between TCM and DCM and characterized the preoperative symptoms and postoperative residual symptoms of TCM patients. Symptoms of motor function impairments of the upper and lower extremities and sensory function impairments of the lower extremities after surgery were more persistent in TCM patients than in DCM patients. Funding No funds were received in support of this work. No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. The Institutional Review Board in our institution approved this study, and written informed consent was obtained from each patient before study participation or surgery. The authors declare no conflict of interest. Declaration of Competing Interest The authors have no financial conflicts of interest. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.jocn.2019.08.054. References [1] Ouchida J, Yukawa Y, Ito K, Katayama Y, Matsumoto T, Machino M, et al. Delayed magnetic resonance imaging in patients with cervical spinal cord injury without radiographic abnormality. Spine (Phila Pa 1976) 2016;41(16): E981–6. [2] Kasimatis GB, Panagiotopoulos E, Megas P, Matzaroglou C, Gliatis J, Tyllianakis M, et al. The adult spinal cord injury without radiographic abnormalities syndrome: magnetic resonance imaging and clinical findings in adults with spinal cord injuries having normal radiographs and computed tomography atudies. J Trauma 2008;65:86–93. [3] Machino M, Ando K, Kobayashi K, Ota K, Morozumi M, Tanaka S, et al. MR T2 image classification in adult patients of cervical spinal cord injury without radiographic abnormality: A predictor of surgical outcome. Clin Neurol Neurosurg 2019;177:1–5.
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[4] Song J, Mizuno J, Inoue T, Nakagawa H. Clinical evaluation of traumatic central cord syndrome: emphasis on clinical significance of prevertebral hyperintensity, cord compression, and intramedullary high-signal intensity on magnetic resonance imaging. Surg Neurol 2006;65:117–23. [5] Kawano O, Ueta T, Shiba K, Iwamoto Y. Outcome of decompression surgery for cervical spinal cord injury without bone and disc injury in patients with spinal cord compression: a multicenter prospective study. Spinal Cord 2010;48:548–53. [6] Rowland JW, Hawryluk GW, Kwon B, Fehlings MG. Current status of acute spinal cord injury pathophysiology and emerging therapies: promise on the horizon. Neurosurg Focus 2008;25(5):E2. [7] Fehlings MG, Furlan JC, Massicotte EM, Arnold P, Aarabi B, Harrop J, et al. Interobserver and intraobserver reliability of maximum canal compromise and spinal cord compression for evaluation of acute traumatic cervical spinal cord injury. Spine (Phila Pa 1976) 2006;31:1719–25. [8] Mazaki T, Ito Y, Sugimoto Y, Koshimune K, Tanaka M, Ozaki T. Does laminoplasty really improve neurological status in patients with cervical spinal cord injury without bone and disc injury? A prospective study about neurological recovery and early complications. Arch Orthop Trauma Surg 2013;133:1401–5. [9] Stevens EA, Marsh R, Wilson JA, Sweasey TA, Branch Jr CL, Powers AK. A review of surgical intervention in the setting of traumatic central cord syndrome. Spine J 2010;10:874–80. [10] Machino M, Yukawa Y, Hida T, Ito K, Nakashima H, Kanbara S, et al. Modified double-door laminoplasty in managing multilevel cervical spondylotic myelopathy: surgical outcome in 520 patients and technique description. J Spinal Disord Tech 2013;26:135–40. [11] Machino M, Yukawa Y, Imagama S, Ito K, Katayama Y, Matsumoto T, et al. Surgical treatment assessment of cervical laminoplasty using quantitative performance evaluation in elderly patients: a prospective comparative study in 505 patients with cervical spondylotic myelopathy. Spine (Phila Pa 1976) 2016;41:757–63. [12] Imagama S, Matsuyama Y, Yukawa Y, Kawakami N, Kamiya M, Kanemura T, et al. C5 palsy after cervical laminoplasty: a multicentre study. J Bone Joint Surg [Br] 2010;92:393–400. [13] Machino M, Yukawa Y, Ito K, Nakashima H, Kanbara S, Morita D, et al. Can magnetic resonance imaging reflect the prognosis in patients of cervical spinal cord injury without radiographic abnormality? Spine (Phila Pa 1976) 2011;36: E1568–72. [14] 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 (Phila Pa 1976) 1981;6:354–64. [15] Machino M, Yukawa Y, Hida T, Ito K, Nakashima H, Kanbara S, et al. Can elderly patients recover adequately after laminoplasty?: a comparative study of 520 patients with cervical spondylotic myelopathy. Spine (Phila Pa 1976) 2012;37:667–71. [16] Machino M, Ando K, Kobayashi K, Ito K, Tsushima M, Matsumoto A, et al. The feature of clinical and radiographic outcomes in elderly patients with cervical spondylotic myelopathy: a prospective cohort study on 1025 patients. Spine (Phila Pa 1976) 2018;43(12):817–23. [17] Kothari P, Freeman B, Grevitt M, Kerslake R. Injury to the spinal cord without radiological abnormality (SCIWORA) in adults. J Bone Joints Surg [Br] 2000;82:1034–7. [18] Epstein NE, Hollingsworth R. Diagnosis and management of traumatic cervical central spinal cord injury: a review. Surg Neurol Int 2015;6:S140–53. [19] Tow AM, Kong KH. Central cord syndrome: functional outcome after rehabilitation. Spinal Cord 1998;36:156–60. [20] Hohl JB, Lee JY, Horton JA, Rihn JA. A novel classification system for traumatic central cord syndrome: The central cord injury scale (CCIS). Spine (Phila Pa 1976) 2010;35:E238–43. [21] Nouri A, Tetreault L, Singh A, Karadimas SK, Fehlings MG. Degenerative cervical myelopathy: epidemiology, genetics, and pathogenesis. Spine (Phila Pa 1976) 2015;40:E675–93. [22] Tetreault L, Goldstein CL, Arnold P, Harrop J, Hilibrand A, Nouri A, et al. Degenerative cervical myelopathy: a spectrum of related disorders affecting the aging spine. Neurosurgery 2015;77(Suppl. 4):S51–67. [23] Aarabi B, Alexander M, Mirvis SE, Shanmuganathan K, Chesler D, Maulucci C, et al. Predictors of outcome in acute traumatic central cord syndrome due to spinal stenosis. J Neurosurg Spine 2011;14:122–30. [24] Talbott JF, Whetstone WD, Readdy WJ, Ferguson AR, Bresnahan JC, Saigal R, et al. The brain and spinal injury center score: a novel, simple, and reproducible method for assessing the severity of acute cervical spinal cord injury with axial T2-weighted MRI findings. J Neurosurg Spine 2015;23 (4):495–504.
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Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical study
Differences in clinical outcomes between traumatic cervical myelopathy and degenerative cervical myelopathy: A comparative study of cervical spinal cord injury without major bone injury and cervical spondylotic myelopathy Masaaki Machino a, Kei Ando a, Kazuyoshi Kobayashi a, Masayoshi Morozumi a, Satoshi Tanaka a, Keigo Ito b, Fumihiko Kato b, Naoki Ishiguro a, Shiro Imagama a,⇑ a b
Department of Orthopedic Surgery, Nagoya University Graduate School of Medicine, Nagoya, Japan Department of Orthopedic Surgery, Chubu Rosai Hospital, Japan Organization of Occupational Health and Safety, Nagoya, Japan
a r t i c l e
i n f o
Article history: Received 11 June 2019 Accepted 6 August 2019
Keywords: Clinical outcomes Traumatic cervical myelopathy Degenerative cervical myelopathy Comparative study Cervical spinal cord injury without major bone injury Cervical spondylotic myelopathy
a b s t r a c t A comparative study to examine the surgical outcomes of traumatic cervical myelopathy (TCM) patients was designed. The study aim was to compare the surgical outcomes between TCM and degenerative cervical myelopathy (DCM) and to characterize the preoperative symptoms and postoperative residual symptoms in TCM patients. One hundred consecutive patients with TCM (81 men, 19 women; mean age, 57.7 years; range, 31–79 years) and 100 consecutive patients with DCM (88 men, 12 women; mean age, 58.4 years; range, 36–78 years) were included in this study. All patients were treated by laminoplasty. The pre- and postoperative neurological statuses were evaluated according to the Japanese Orthopaedic Association (JOA) scoring system for cervical myelopathy. The recovery rate (RR) of each function was compared between the two groups. The mean preoperative JOA scores of motor function of the upper extremity in the TCM and DCM groups were 1.9 and 2.3, respectively (P < 0.01). After surgery, the mean RRs of motor function of the upper extremity in the TDM and DCM groups were 36.4% and 55.7%, respectively (P < 0.01) and in the lower extremity were 32.3% and 46.5%, respectively (P < 0.05). The RR for sensory function of the lower extremity was significantly lower in TCM patients than in DCM patients (39.6 vs 68.2, respectively; P < 0.0001). Motor function impairments of the upper and lower extremities and sensory function impairments of the lower extremities after surgery were more persistent in the TCM group than in the DCM group. Ó 2019 Elsevier Ltd. All rights reserved.
1. Introduction Over the last decades, population aging has caused the incidence of spinal stenosis to rise, which has led to a consequent increase in cases of traumatic cervical myelopathy (TCM) caused by minor trauma [1]. TCM is a syndrome that involves spinal cord injury without evidence of spinal fracture or dislocation on plain radiography or computed tomography (CT) [2]. Surgical treatment of cervical myelopathy is aimed at decompressing the spinal cord to prevent further damage [3]. Although some neurological function can be recovered after surgery, a degree of irreversible neurological damage is unavoidable [4,5]. ⇑ Corresponding author at: Department of Orthopaedic Surgery, Nagoya University Graduate School of Medicine, 65, Tsurumai, Showa-ku, Nagoya, Aichi 466-8550, Japan. E-mail address: [email protected] (S. Imagama). https://doi.org/10.1016/j.jocn.2019.08.054 0967-5868/Ó 2019 Elsevier Ltd. All rights reserved.
Traumatic damage of the spinal cord might reflect poor outcomes with a lower recuperative potential [6]. The surgical outcome of laminoplasty might be worse in TCM patients than in degenerative cervical myelopathy (DCM) patients. Recovery of spinal cord function may be insufficient in TCM because of increased vulnerability of the spinal cord; therefore, surgical treatment of TCM patients has become a great concern [7–9]. To determine the best treatment for TCM, it is important to understand the differences in the characteristics of preoperative impairments and postoperative residual symptoms between TCM and DCM patients. However, no report has described the particular residual symptoms following surgery in TCM patients. We hypothesized that patients with TCM that occurs rapidly have more severe symptoms preoperatively and poorer outcomes postoperatively than those of patients with DCM that occurs slowly. Therefore, we designed a prospective comparative study
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MRI and myelography findings were consistent with myelopathy secondary to multisegmental cervical spondylotic stenosis. All patients exhibited myelopathy, which was confirmed by a physical examination, and cord compression was present between C2/C3 and C7/T1 disk levels (Fig. 1). Differences in the following parameters were evaluated among the two groups: age, sex, prevalence of diabetes, prevalence of hypertension, smoking history, and postoperative follow-up duration. This study was approved by the Institutional Review Board, and written informed consent was obtained from each patient prior to study participation or surgery. 2.2. Surgical technique for modified double-door laminoplasty
Fig. 1. Representative sagittal views in T2-weighted MRI before surgery of traumatic cervical myelopathy (TCM) and degenerative cervical myelopathy (DCM).
to examine the surgical outcomes of TCM patients from a single surgery. The purpose of this study was to compare the surgical outcomes between TCM and DCM and to characterize the preoperative symptoms and postoperative residual symptoms in TCM patients. 2. Material and methods 2.1. Study population 2.1.1. Patients with TCM One hundred consecutive TCM patients with cervical spinal cord injury (SCI) without major bone injury (81 men and 19 women; mean age, 57.7 years; range, 31–79 years) were enrolled. All patients underwent preoperative functional X-ray in the acute phase. The exclusion criteria were as follows: (1) presence of ossification of the posterior longitudinal ligament (OPLL); (2) history of rheumatoid arthritis, cerebral palsy, or tumors; (3) fracture or traumatic instability, such as dislocation/subluxation; (4) destructive spondyloarthritis due to hemodialysis; (5) previous cervical surgery; (6) spinal fusion with instrumentation; (7) thoracic spondylotic myelopathy; and (8) lumbar spinal canal stenosis. All patients presented symptoms of TCM and magnetic resonance imaging (MRI) findings consistent with symptoms secondary to cervical spinal canal stenosis. For each patient, TCM was confirmed by physical examination and MRI-confirmed cord compression between the C2/C3 and C7/T1 disk levels. Patients with profound neurological deficits and persistent spinal cord compression due to cervical spinal canal stenosis were indicated for surgery. The mean period from injury to operation was 18.4 ± 3.5 days. 2.1.2. DCM (Controls) One hundred consecutive DCM patients with cervical spondylotic myelopathy (CSM) (88 men and 12 women; mean age, 58.4 years; range, 36–78 years) were included in this study. The exclusion criteria were as follows: (1) presence of OPLL; (2) history of rheumatoid arthritis, cerebral palsy, or tumors; (3) spinal injuries; (4) destructive spondyloarthritis due to hemodialysis; (5) previous cervical surgery; (6) spinal fusion with instrumentation; (7) thoracic spondylotic myelopathy; and (8) lumbar spinal canal stenosis. All patients presented with symptoms of myelopathy.
All patients were treated by double-door laminoplasty, as described by Kurokawa, with some modifications [10,11]. The muscles attached to the C2 spinous process were preserved without detachment. Surgical exposure was limited as much as possible. The spinous processes between C3 and C7 were resected at their bases, and the laminae were cut at the center by using a high-speed drill. Bilateral gutters were created as hinges at the border between the laminae and facets in a manner that was slightly more medial than originally described, thus minimizing the invasion of facets [12]. After elevating the halves of the laminae (similar to opening a French door), bone graft struts (16–18 mm long) created from the C6 or C7 spinous process were tied to bridge the bilateral edges of the laminae. 2.3. Postoperative considerations All patients were allowed to sit up and walk on postoperative day 1 while wearing a Philadelphia collar. The collars were fitted for all patients, but they were allowed to remove them at their discretion. The cervical range of motion exercises were performed as soon as possible during the rehabilitation program. The ideal spinal alignment was explained to all patients after surgery. 2.4. Clinical outcome Operative time and blood loss were assessed. The pre- and postoperative severities of myelopathy were evaluated according to a scoring system proposed by the Japanese Orthopaedic Association (JOA) for cervical myelopathy [13]. The postoperative JOA score was assessed during the final follow-up. The JOA score quantifies neurological impairment by evaluating motor function in the upper and lower extremities (four points each), sensory function in the upper and lower extremities as well as in the trunk sensibility (two points each, total six), and urinary bladder function (three points). Thus, a perfect JOA score for cervical myelopathy is 17 points (Table 1). The recovery rate (RR) of the JOA score was calculated by using the formula suggested by Hirabayashi et al (Table 1) [14]. [RR = postoperative preoperative JOA scores)/(17 preoperative JOA score) 100%]. In addition, the achieved JOA score (postoperative JOA score preoperative JOA score) was also evaluated [15]. Each functional improvement was also expressed by a RR (sub-score RRs), and they were compared between the two groups [16]. 2.5. Statistical analysis Data were analyzed by using SPSS statistical software (version 18.0; SPSS, Inc., Chicago, IL, USA). All values are expressed as a mean ± standard deviation. The Mann–Whitney U test was used to analyze the differences between the two groups. Repeated measures analyses of variance in the same group were performed by using the Wilcoxon test. The chi-square test was used to analyze
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M. Machino et al. / Journal of Clinical Neuroscience 70 (2019) 127–131 Table 1 Evaluation of cervical myelopathy using the scoring system proposed by the Japanese Orthopedic Association (JOA score) and recovery rate of the JOA score. JOA score
Follow-up period (months) Surgery time (minutes) Blood loss (ml) Preoperative JOA score (points) Postoperative JOA score at final follow-up (points) Achieved JOA score (points) Recovery rate of the JOA score (%)
I. Motor function of the upper extremity 0. Impossible to eat with chopsticks or spoon 1. Possible to eat with spoon, but not with chopsticks 2. Possible to eat with chopsticks, but inadequate 3. Possible to eat with chopsticks, awkward 4. Normal II. Motor function of the lower extremity 0. Impossible to walk 1. Needs cane or aid on flat ground 2. Needs cane or aid only on stairs 3. Possible to walk without cane or aid but slowly 4. Normal
TCM
DCM
P value
24.9 ± 18.4 82.6 ± 23.4 62.7 ± 70.0 8.4 ± 3.6 11.5 ± 3.5
25.6 ± 12.5 82.4 ± 26.1 56.6 ± 51.2 8.8 ± 2.0 13.2 ± 2.5
0.7706 0.5949 0.2428 0.2613 <0.001***
3.1 ± 2.3 40.0 ± 26.0
4.3 ± 2.3 53.5 ± 26.2
<0.001*** <0.001***
Values given are mean ± SD unless otherwise specified. JOA score indicates Japanese Orthopaedic Association score for cervical myelopathy; SD, standard deviation; TCM, traumatic cervical myelopathy; DCM, degenerative cervical myelopathy. *Statistically significant values. *p < 0.05, **p < 0.01, ***p < 0.001.
III. Sensory function A. Upper extremity 0. Apparent sensory loss 1. Minimal sensory loss 2. Normal B. Lower extremity (same as A) C. Trunk (same as A) IV. Bladder function 0. Complete retention 1. Severe disturbance (sense of retention, dribbling, incomplete continence) 2. Mild disturbance (urinary frequency, urinary hesitancy) 3. Normal Recovery rate of the JOA score (Hirabayashi method). Recovery rate (%) = [Postoperative score Preoperative score]/[Full score (17) Preoperative score] 100. Achieved JOA score. Achieved score (points) = Postoperative score Preoperative score.
differences between groups. P < 0.05 was considered to be indicative of statistical significance.
3. Results There were no significant differences in the patient demographic data (age, sex). No significant intergroup differences were observed in the prevalence of diabetes, hypertension, and smoking history between both groups (Table 2). The TCM patients underwent expansive laminoplasty, which was performed on C3–C7 in 90 patients and on C3–C6 in 10 patients. In the DCM patients, laminoplasty was performed at the following disk levels: C3–C7 (n = 86) and C3–C6 (n = 14). There were no statistically significant differences in the follow-up period, operation time, or blood loss between the two groups (Table 3). The mean JOA scores in the TCM and DCM groups were 8.4 ± 3.6 and 8.8 ± 2.0 points before surgery and 11.6 ± 3.5 and 13.2 ± 2.5 points at the final postoperative follow-up, respectively. The postoperative JOA scores at the final follow-up were significantly lower in the TCM group than in the DCM group (P < 0.001). The TCM
Table 2 Patient demographics and comorbidities between two groups.
Number of patients Age (years) Gender (Males/Female) Diabetes Hypertension Smoking history
Table 3 Clinical outcomes between two groups.
TCM
DCM
P value
100 57.7 ± 11.0 81/19 15 (15%) 24 (24%) 23 (23%)
100 58.4 ± 9.3 88/12 18 (18%) 28 (28%) 20 (20%)
0.4677 0.2411 0.7037 0.5247 0.7310
Values given are mean ± SD unless otherwise specified. SD indicates standard deviation; TCM, traumatic cervical myelopathy; DCM, degenerative cervical myelopathy.
group showed significantly lower RRs of JOA scores than those of the DCM group (40.1% ± 26.1% vs. 53.5% ± 26.2%, respectively; P < 0.001). The mean achieved JOA scores in the TCM and DCM groups were 3.2 ± 2.4 and 4.4 ± 2.3 points, respectively, with significant difference between the two groups (P < 0.001, Table 3). Before surgery, the mean preoperative JOA scores of motor function in the upper extremity in the TCM and DCM groups were 1.9 ± 1.2 and 2.3 ± 0.9 points, respectively (P = 0.0016). Adversely, the JOA scores of sensory function of the trunk were significantly lower in the DCM group than in the TCM group (1.0 ± 0.9 vs. 1.4 ± 0.8, respectively, P = 0.0016, Table 4). After surgery, the motor function scores for the upper extremity were 2.7 ± 1.1 points (TCM) and 3.3 ± 0.7 points (DCM) at final follow-up (P < 0.0001). The scores of motor and sensory function for the lower extremities were lower in the TCM group than in the DCM group after surgery (P = 0.0039, P = 0.0012, respectively, Table 4). The mean RRs of motor function of the upper extremity in the TDM and DCM groups were 36.4% and 55.7%, respectively (P = 0.005). The RR of lower extremity motor function was significantly lower in the TCM group than in the DCM group (32.3% vs. 46.5%, respectively; P = 0.0108). The TCM patients showed significantly lower RR for sensory function of the lower extremity than that of the DCM patients (39.6% vs. 68.2%, respectively; P < 0.0001, Table 5). 4. Discussion Damage to the spinal cord caused by traumatic injury may influence the surgical outcome. However, the preoperative symptoms and postoperative residual symptoms have not been fully evaluated in TCM patients. This study aimed to compare the surgical outcomes between TCM and DCM and to characterize the preoperative symptoms and postoperative residual symptoms in TCM patients. The TCM patients showed significantly lower JOA scores for motor function of the upper extremity than those of the DCM patients before surgery. After surgery, upper extremity motor function impairments and lower extremity motor and sensory function impairments persisted more than other symptoms in the TCM patients than in the DCM patients. Such findings should be included in the preoperative discussions on the risks and benefits of surgery. The pathophysiology of SCI is best described as biphasic, consisting of a primary and secondary phase of injury [6]. The primary phase involves the initial mechanical injury that directly imparts force to the spinal cord and disrupts axons, blood vessels, and cell membranes. This is followed by the delayed onset of a secondary injury phase involving vascular dysfunction, edema, ischemia, excitotoxicity, electrolyte shifts, free radical production, inflammation, and delayed apoptotic cell death. Whereas neurological defi-
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Table 4 Preoperative and postoperative Japanese Orthopaedic Association scores for each function in the two groups. TCM
DCM
P value
Preoperative JOA score Motor function of the Upper extremity (points) Motor function of the Lower extremity (points) Sensory function of the Upper extremity (points) Sensory function of the Lower extremity (points) Sensory function of the Trunk (points) Bladder function (points)
1.9 ± 1.2 1.9 ± 1.3 0.09 ± 0.3 0.82 ± 0.9 1.4 ± 0.8 2.4 ± 0.9
2.3 ± 0.9 2.1 ± 0.8 0.18 ± 0.4 0.83 ± 0.8 1.0 ± 0.9 2.4 ± 0.6
0.0016** 0.1070 0.0899 0.9346 0.0016** 0.9240
Postoperative JOA score Motor function of the Upper extremity (points) Motor function of the Lower extremity (points) Sensory function of the Upper extremity (points) Sensory function of the Lower extremity (points) Sensory function of the Trunk (points) Bladder function (points)
2.7 ± 1.1 2.6 ± 1.1 0.8 ± 0.7 1.3 ± 0.8 1.7 ± 0.6 2.5 ± 0.8
3.3 ± 0.7 3.0 ± 0.9 1.0 ± 0.8 1.6 ± 0.7 1.6 ± 0.6 2.7 ± 0.5
<0.0001*** 0.0039** 0.1465 0.0012** 0.9675 0.0528
Values given are mean ± SD unless otherwise specified. JOA score indicates Japanese Orthopaedic Association score for cervical myelopathy; SD, standard deviation; TCM, traumatic cervical myelopathy; DCM, degenerative cervical myelopathy. *Statistically significant values. *p < 0.05, **p < 0.01, ***p < 0.001.
Table 5 Recovery rate of the Japanese Orthopaedic Association (JOA) score for each function in the two groups.
Motor function of the Upper extremity (%) Motor function of the Lower extremity (%) Sensory function of the Upper extremity (%) Sensory function of the Lower extremity (%) Sensory function of the Trunk (%) Bladder function (%)
TCM
DCM
P value
36.4 ± 51.1 32.3 ± 34.2 37.0 ± 38.0 39.6 ± 40.4 59.5 ± 47.2 44.2 ± 45.4
55.7 ± 43.9 46.5 ± 41.8 42.9 ± 41.7 68.2 ± 41.9 67.7 ± 38.5 60.2 ± 48.9
0.0050** 0.0108* 0.2654 <0.0001*** 0.2564 0.0753
Values given are mean ± SD unless otherwise specified. SD, standard deviation. *Statistically significant values. *p < 0.05, **p < 0.01, ***p < 0.001.
cits are present immediately following the initial injury, the secondary injury phase results in a protracted period of tissue destruction. TCM is associated with hyperextension injury of the cervical spine and is commonly observed in patients with minor trauma without bony injury and in patients with a pre-existing pathology, such as canal stenosis [13]. The most common of the incomplete SCI syndromes, central cord syndrome, usually results from neck hyperextension in older people with spinal stenosis [17]. In a hyperextension injury, the cord is compressed between the enfolded ligamentum flavum and the vertebral osteophyte [18]. Before surgery, the TCM patients in the present study had a significantly lower JOA score for motor function of the upper extremity than that of the DCM patients. Generally, in patients with TCM, motor function impairments of the upper extremity are caused by central cord syndrome [19]. Because central cord syndrome is usually caused by damage to the cervical spinal cord, it is characterized by weakness in the arms with lesser weakness of the legs and less loss of sensation in regions in which the nerves branch from the sacral segments [20]. There is loss of sensation of pain, temperature, light touch, and pressure below the level of injury. The spinal tracts that serve the arms are more affected because of their central location in the spinal cord, whereas the corticospinal fibers that serve the legs are spared because of their more external location. The pathophysiology of DCM involves static factors, which lead to acquired or developmental stenosis of the cervical canal and dynamic factors that involve repetitive damage to the cervical cord [21]. These mechanical factors in turn result in direct damage to neurons and glia as well as a secondary cascade of events, includ-
ing ischemia, excitotoxicity, and apoptosis [22]. DCM is a common degenerative disease of the spine that is the direct result of spinal cord compression. With age, the spine undergoes natural degenerative changes that can affect its basic anatomy and lead to stenosis of the spinal canal. In the current study, motor function impairments of the upper extremity and motor and sensory function impairments of the lower extremity after surgery were more persistent than other symptoms in the TCM patients than in the DCM patients. TCM causes irreversible paralysis and sensory damage, and it remains controversial as to whether conservative or surgical treatment strategies are best for adult patients with TCM [23,24]. When considering surgery, associated risks should be fully disclosed and explained, and the patient’s general condition should be thoroughly ascertained. To date, no definitive management protocol has been established for TCM. In our institution, we perform radiography and CT to identify cervical spine fractures or dislocations, and when instability is not evident on extension-flexion radiographs, patients are allowed to sit up and walk while wearing a Philadelphia collar. Rehabilitation is then started immediately after injury. Moreover, the role of surgery in TCM patients remains controversial. In our institution, patients with spinal cord compression in delayed MRI are offered cervical laminoplasty to achieve a more favorable outcome and prevent symptom deterioration. On the basis of the results of this study, we speculate that the spinal cord relatively resists chronic pressure to progress slowly by degenerative change. In contrast, the spinal cord might be vulnerable to a sudden on-set contusion because of an injury caused by an external force. A better understanding of both the biological and mechanical mechanisms that cause TCM will significantly
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improve physicians’ ability to treat patients diagnosed with this disease and decrease the prevalence of patients suffering from spinal cord impairment. There were some limitations in our study. The follow-up duration was relatively brief, and patient-based objective outcomes, such as quality of life determined by using the Short-Form Health Survey 36, subjective satisfaction, and axial back pain measured by using the visual analog scale, were not assessed. Objective measures should be added in future studies. In this study, we used only the JOA scores for to assess neurological function. However, many previous investigators have used the JOA scoring system and its RR to evaluate outcomes [12–14]. We did not compare the surgical outcomes in the patients who underwent double-door laminoplasty and those who underwent either anterior or posterior surgery. Despite these limitations, these findings provide baseline data that may help clinicians accurately assess preoperative impairments and postoperative outcomes in patients with TCM. 5. Conclusion This study investigated the surgical outcomes between TCM and DCM and characterized the preoperative symptoms and postoperative residual symptoms of TCM patients. Symptoms of motor function impairments of the upper and lower extremities and sensory function impairments of the lower extremities after surgery were more persistent in TCM patients than in DCM patients. Funding No funds were received in support of this work. No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. The Institutional Review Board in our institution approved this study, and written informed consent was obtained from each patient before study participation or surgery. The authors declare no conflict of interest. Declaration of Competing Interest The authors have no financial conflicts of interest. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.jocn.2019.08.054. References [1] Ouchida J, Yukawa Y, Ito K, Katayama Y, Matsumoto T, Machino M, et al. Delayed magnetic resonance imaging in patients with cervical spinal cord injury without radiographic abnormality. Spine (Phila Pa 1976) 2016;41(16): E981–6. [2] Kasimatis GB, Panagiotopoulos E, Megas P, Matzaroglou C, Gliatis J, Tyllianakis M, et al. The adult spinal cord injury without radiographic abnormalities syndrome: magnetic resonance imaging and clinical findings in adults with spinal cord injuries having normal radiographs and computed tomography atudies. J Trauma 2008;65:86–93. [3] Machino M, Ando K, Kobayashi K, Ota K, Morozumi M, Tanaka S, et al. MR T2 image classification in adult patients of cervical spinal cord injury without radiographic abnormality: A predictor of surgical outcome. Clin Neurol Neurosurg 2019;177:1–5.
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