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Journal of Back and Musculoskeletal Rehabilitation 28 (2015) 261–266 DOI 10.3233/BMR-140513 IOS Press
Predictive factors relating to prognosis of anterior decompressive surgery for proximal-type cervical spondylotic amyotrophy Ling-De Kong1, Lin-Feng Wang1, Jing-Tao Zhang, Ying-Ze Zhang, Wen-Yuan Ding and Yong Shen∗ Department of Spine Surgery, The Third Hospital of Hebei Medical University, Shijiazhuang, Hebei, China
Abstract. BACKGROUND AND OBJECTIVE: Cervical spondylotic amyotrophy (CSA) is a relatively rare disorder. This study was conducted to elucidate the prognosis of proximal-type CSA after anterior decompressive surgery by evaluating clinical factors and imaging findings. METHODS: Anterior decompressive surgery was performed in 40 patients with proximal-type CSA between March 2000 and December 2011. Patients were classified into 2 categories based on axial T2-weighted magnetic resonance imaging (MRI) findings: “nerve root compression (NRC)”, with nerve root compressed at the intervertebral foramen, and “spinal cord compression (SCC)” with spinal cord compressed at the medial or paramedial site of spinal canal. Manual muscle testing (MMT) was used to evaluate the surgical effect. Scapular, deltoid, and biceps brachii muscles of the affected side were tested and the sum scores were calculated. Clinical factors and imaging findings, such as age, duration of disease, preoperative MMT grade, number of affected levels and signal intensity changes of spinal cord, were collected to analyze prognostic factors. RESULTS: After anterior decompressive surgery, 30 patients (75%) showed an improvement. NRC was observed in 6 patients and SCC in the rest 34 patients based on MRI findings. All patients (100%) with NRC had an improvement, while only 24 patients (70.6%) with SCC improved. In patients with SCC, there was a significant difference in duration of disease between patients who had an improvement and those who had not (P < 0.01). CONCLUSIONS: Anterior decompressive surgery is effective in the treatment of most patients with CSA. NRC on MRI may indicate a good surgical outcome. In patients with SCC, a long duration of disease is a risk factor for poor prognosis. Keywords: Cervical spondylotic amyotrophy, anterior surgery, predictive factor, magnetic resonance imaging
1. Introduction Cervical myelopathy and radiculopathy due to cervical spondylosis are well-known cervical disorders. But occasionally, patients with cervical spondylosis present with weakness and wasting of upper limb mus∗ Corresponding author: Yong Shen, Department of Spine Surgery, The Third Hospital of Hebei Medical University, 139 Ziqiang Road, Shijiazhuang 050051, Hebei, China. Tel.: + 86 0311 88602316; Fax: +86 0311 88602016; E-mail: [email protected]. 1 The first two authors contributed equally to this article.
cles without significant sensory deficits or gait disturbance, this condition is referred to as cervical spondylotic amyotrophy (CSA) [1,2]. A patient with this condition was first described by Brain [3], and many reports of this syndrome followed [1,4–6]. According to the most predominantly affected muscle groups, CSA is classified as either proximal-type (scapular, deltoid, and biceps) or distal-type (triceps, forearm, and hand). Difficulty in shoulder abduction, positive armdrop sign, or positive wrist-drop sign is always found in those patients. CSA usually presents as a unilateral disorder. In rare case, it is reported to have bilateral up-
c 2015 – IOS Press and the authors. All rights reserved ISSN 1053-8127/15/$35.00
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per limbs involved [7]. The pathophysiology of CSA has not been clarified, but two different mechanisms have been proposed to explain the pathogenesis. Selective damage to either ventral nerve root or anterior horn may cause CSA [4,5,8]. Treatments of CSA include conservative and operative management [9–11]. Inui et al. [12] recommended that conservative treatment should be initially tried, and if conservative treatment failed, surgical intervention was indicated. However, even with surgical treatment, some patients may not benefit from surgery to the extent that they regain the muscle strength of upper extremity. There are a few studies investigate prognostic factors of surgical treatment for CSA [13–15], but the patient populations are heterogeneous, because the ventral nerve root lesion and the anterior horn lesion are not clearly distinguished. As we know, the essential pathophysiologies of the two types of lesion are obviously different. Thus, we made an effort to identify the lesion type of CSA on the basis of magnetic resonance imaging (MRI) findings, and then elucidated the prognostic factors of postoperative patients by evaluating clinical factors and imaging findings.
2. Methods 2.1. Patient population After institutional ethics board approval, a retrospective study was performed in our institution for patients with proximal-type CSA who underwent surgery between March 2000 and December 2011. The inclusion criteria were as follows: presence of severe muscle atrophy of the shoulder girdle muscles; presence of MRI-documented spinal cord compression and/or nerve root compression; mild or no sensory deficit in the upper extremity; absence of gait disturbance or abnormal tendon reflexes; having no subjective improvement of symptom or objective improvement of muscle strength after continuous cervical traction for 2 to 3 weeks. Patients with ossification of posterior longitudinal ligament of the cervical spine, cervical disc herniation, or subjective symptoms or neurologic findings associated with neuropathy were excluded. To exclude patients with amyotrophic lateral sclerosis, we performed careful neurological evaluations. If it was difficult to differentiate between amyotrophic lateral sclerosis and proximal-type CSA, additional electrophysiologic examination was performed. The final decision was made by a spine surgeon and a neurologist in consensus.
2.2. Surgical procedure All surgery was performed by a single surgeon (Y. Shen). Cervical anterior decompression and fusion was adopted for every case, even if patients suffered a lesion involving 3 intervertebral levels. The surgical procedures could be anterior cervical disectomy and fusion (ACDF) or anterior cervical corpectomy and fusion (ACCF). Extensive decompression was performed including removal of the affected discs or vertebrae, osteophytes, and posterior longitudinal ligament to expose the dura throughout the length of the discectomy or corpectomy. Additional uncinate processes were partially resected when patients had a foraminal stenosis due to uncovertebral osteophytes. Finally, a cervical cage or a titanium mesh cage filled with autologous bone grains was inserted into the intervertebral space to guarantee firm fusion. 2.3. Assessment of surgical outcome Manual muscle testing (MMT) was used to quantify the muscle strength. Scapular, deltoid, and biceps brachii muscles of the affected side were tested, and the sum scores of the muscles, which rang from 0 to 15, were calculated. The grade of recovery gained by surgical treatment at the final follow-up was in comparison with that at admission. Improvements in the sum scores were classified from excellent to poor (excellent, 3 or more scores of recovery by MMT; good, 1 to 2 scores of recovery by MMT; fair, no improvement by MMT; poor, worsening by MMT). Grades of excellent and good neurologic recovery were considered as “improvement”, and grades of fair and poor as “no improvement”. 2.4. Relevant factors Relevant clinical factors, such as age, sex, duration of disease, were collected from the patients’ records. MRI yielded factors such as number of affected levels and signal intensity changes of spinal cord. Furthermore, MRI findings were classified into 2 categories: “nerve root compression (NRC)” and “spinal cord compression (SCC)”. Patients with NRC were characterized by having nerve root compressed alone at the intervertebral foramen on T2-weighted axial view (Fig. 1a), having no cord compression nor signal intensity changes on T1- or T2-weighted sagittal view. However, patients with SCC had spinal cord compressed at the medial or paramedial site of spinal
L.-D. Kong et al. / Prognosis of anterior decompressive surgery for proximal type CSA
a
b
263
c
Fig. 1. a Axial T2-weighted MRI showed nerve root compression (NRC) on the left C5 nerve root at the C4-5 intervertebral foramen. b Axial T2-weighted MRI showed spinal cord compression (SCC) at the paramedial site of spinal canal behind the C4-5 intervertebral level. c Axial T2-weighted MRI showed both nerve root and spinal cord were compressed at the C4-5 intervertebral level.
canal (Fig. 1b), combined with or without signal intensity changes on MRI. Patients with both NRC and SCC were also considered as SCC (Fig. 1c). MRI findings were independently evaluated by 2 spine surgeons, and the final results were formed by consensus discussion between the 2 surgeons. Surgical outcomes were evaluated in all patients. To determine which prognostic factors relate to surgical outcomes, we compared each of the clinical factors and imaging findings between patients who had an improvement and those who had not. 2.5. Statistical analysis Data were analyzed using the Statistical Package for the Social Sciences (version 13.0 for Windows; SPSS, Chicago, IL, USA). Chi-square test and MannWhitney U test were used to analyze qualitative data and quantitative date, respectively. P < 0.05 was considered to indicate a statistically significant difference.
3. Results Forty proximal-type CSA patients were enrolled in the study, consisted of 31 men and 9 women, with the age at the initial visit of (57.8 ± 11.2) years. The duration of disease was (11.5 ± 8.9) months and overall follow-up period was (71.2 ± 34) months. The numbers of patients with intervertebral levels affected were 21 with one level, 14 with two levels, and 5 with three levels. Preoperative sum scores of scapular- deltoidbiceps brachii muscles were (9.1 ± 2.9) scores, and postoperative sum scores were (10.7 ± 3.0) scores (Table 1). No patients had bilateral upper limbs involved. There were no incidences of infections, cervical fluid leakage, esophageal or tracheal ruptures, neurological deterioration, or recurrent laryngeal nerve
Table 1 Data of patients with proximal-type CSA Parameter Total cases (no.) Sex (men: women) Age at first visit (years) Duration of disease (months) Follow-up period (months) Affected intervertebral levels (no.) 1-level (no.) 2-levels (no.) 3-levels (no.) Sum scores of muscle strength (scores) Preoperative Postoperative
Value 40 31:9 57.8 ± 11.2 11.5 ± 8.9 71.2 ± 34.0 21 14 5 9.1 ± 2.9 10.7 ± 3.0
CSA cervical spondylotic amyotrophy.
palsy. Four patients complained of significant axial pain, which subsided gradually in 1–2 months without any treatment. All patients achieved solid fusion at 1 year postoperatively. Regarding improvement of MMT after surgery, 16 patients were graded as excellent, 14 patients good, 10 patients fair, and no patients poor. Therefore, 75% of patients had an improvement. Based on MRI findings, NRC was observed in 6 patients and SCC in the rest 34 patients. All patients with NRC had an improvement (excellent, 4; good, 2), but only 70.6% of patients with SCC had an improvement (excellent, 12; good 12; fair 10, Table 2). All patients with NRC are listed on Table 3. All but 2 patients had insignificant nerve root pain before surgery. Three patients had mild sensory deficits, involving mainly the C5 or C6 dermatomes. MRI showed NRC behind the C4-5 level in 4 patients and the C5-6 level in 1 patient. One patient had both the C4-5 level and the C5-6 level involved. In patients with SCC on MRI, 13 of 34 (38.2%) had signal intensity changes, and all changes were behind C4-5 or C5-6 intervertebral levels, or both. Prognostic factors were compared between 24 patients who had
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L.-D. Kong et al. / Prognosis of anterior decompressive surgery for proximal type CSA Table 2 Outcomes of surgery according to site of compression in MRI Cases with NRC (n = 6) Cases with SCC (n = 34) Total cases (n = 40)
Excellent (no.) 4 12 16
Good (no.) 2 12 14
Fair (no.) 0 10 10
Improvement rate 100.0% 70.6% 75.0%
MRI magnetic resonance imaging, NRC nerve root compression, SCC spinal cord compression. Table 3 Summary of clinical symptoms, imaging features, and outcome in 6 patients with NRC Case no. 1 2 3 4 5 6
Age at surgery 39 55 64 51 48 62
Insignificant nerve root pain No Yes Yes No Yes Yes
Mild sensory deficits No No Yes No Yes Yes
Affected intervertebral levels in MRI C4-5 C4-5,C5-6 C4-5 C5-6 C4-5 C4-5
Sum scores of preoperative MMT 12 10 7 10 12 7
Sum scores of postoperative MMT 15 13 9 14 14 10
Surgical outcome Excellent Excellent Good Excellent Good Excellent
NRC nerve root compression, MRI magnetic resonance imaging, MMT manual muscle testing. Table 4 Predictive factors relating to prognosis in 34 cases with SCC No. of cases Age at first visit (years) Duration of disease (months) Sum scores of preoperative muscle strength (scores) No. of affected intervertebral levels (single: multiple) Signal intensity change Low signal on T1 MRI (yes: no) High signal on T2 MRI (yes: no)
Improvement 24 57.9 ± 10.3 6.2 ± 2.3 9.2 ± 3.1 11:13
No improvement 10 60.5 ± 11.6 23.5 ± 10.1 8.7 ± 2.7 5:5
P value – 0.52 < 0.01 0.57 0.55
3:21 9:15
1:9 4:6
0.74 0.88
SCC spinal cord compression, MMT manual muscle testing, MRI magnetic resonance imaging.
an improvement and 10 patients who had not. There was a significant difference in duration of disease between the two groups (6.2 ± 2.3 months vs. 23.5 ± 10.1 months, P < 0.01). Other factors, such as age, preoperative MMT, number of affected intervertebral levels, signal intensity changes on MRI, showed no significant difference (Table 4).
4. Discussion The pathophysiology of CSA has not been clarified, but two different mechanisms have been proposed. Keegan [4] demonstrated from autopsy finding that selective damage to the ventral nerve root was the cause of CSA. However, Fujwara [16] attributed CSA to a vascular insufficiency mechanism to the anterior horn cell. Shinomiya et al. [6] proposed on the basis of electrophysiologic findings that both ventral nerve root lesion and anterior horn lesion might cause this syndrome. From the axial view of MRI, both NRC and SCC were observed in CSA patients. It seems that
there are two groups of patients, in one group, the disease is attributable to selective ventral root lesion, which presents with NRC on MRI; in the other group, the disease is caused by an injury to the anterior horn, which presents with SCC on MRI. An understanding of the pathophysiology of this syndrome is essential to ascertain prognostic factors. In this study, only 6 patients showed NRC on MRI. Though the number of those patients is small, their surgical outcomes were satisfactory. All of them showed excellent or good neurologic status at final follow-up. This might due to the fact that the ventral nerve root has greater ability to recover compared with the anterior horn. On the basis of the two mechanisms discussed above, it is logical to speculate that NRC on MRI usually indicates a good surgical outcome. As shown in Table 3, CSA patients with NRC tend to present with mild sensory deficits and nerve root pain. Besides, C4-5 is the most frequently involved intervertebral level in the 6 patients, which means that C5 nerve root is associated with the amyotrophy. It has to be noticed that C5 nerve root palsy is also well
L.-D. Kong et al. / Prognosis of anterior decompressive surgery for proximal type CSA
recognized as a complication after cervical laminoplasty, and patients with postoperative C5 palsy generally have a good recovery too [17]. However, there seems to be no association between the 2 types of paralysis in essential etiology. Of the 34 patients with SCC, only 24 patients showed an improvement in neurologic status at final follow-up. Regardless of the absence of symptoms in the lower extremities, these CSA patients were considered to be closely related to cervical myelopathy. Thus, factors that have been proven to be correlated with prognosis of cervical myelopathy were collected and analyzed. The result showed that patients with a long duration of disease tended to have a poor surgical outcome. Based on this result, we recommend that timely surgical intervention should be performed for proximal-type CSA patients if conservative treatment failed, as delayed surgical intervention may lead to losing the best opportunity for patients to get a satisfactory outcome. The role of high signal intensity on T2-weighted MRI or low signal intensity on T1-weighted MRI in CSA patients has been studied [16,18]. We observed that all signal intensity changes were behind C4-5 or C5-6 intervertebral levels, which implicates that impairment of C4, C5 segment of the cervical cord might contribute to the pathology of proximal-type CSA. The pathology of this signal abnormality has been assumed to vary from acute edema to chronic myelomalacia, and is associated with a poor prognosis of cervical myelopathy [19]. However, in this study, these signal abnormalities could not reveal the prognosis of surgical treatment for CSA, and this result is consistent with previous studies [14,15]. A possible reason for this phenomenon is that the spinal cord lesion can not reflect the pathological changes of anterior horn. For example, even if the spinal cord is severely damaged, the anterior horn part may suffer only a slight lesion. The methods of operative treatment for CSA are still controversial. Both anterior approach and posterior approach have been reported to be effective [9,20,21]. Fujiwara et al. [22] described performing laminoplasty with or without selective foraminotomy for 32 patients, and reported excellent or good results in the most CSA patients. Shinomiya et al. [6] reported 10 patients of anterior decompression and fusion for proximal-type CSA, and found that all patients had an improvement. Zhang et al. [21] analyzed the records of 21 proximaltype patients who underwent anterior decompressive surgery, and observed that 81% of patients gained 1 or more grades of muscle power improvement. Usually,
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posterior approach is indicated for patients with a lesion involving multiple intervertebral levels. However, laminoplasty has the disadvantage of leaving the anterior compressive lesion as it is. Besides, patients with a straight or kyphotic curvature of the cervical spine would not be ideal candidates for posterior decompression. On the other hand, anterior decompression and fusion is believed to provide an optimal chance of neurological recovery through the complete elimination of the ventral compression. Unlike distal-type CSA, the proximal type is characterized by less numbers of affected intervertebral levels [15,22]. In our study, lesions involving 1 intervertebral level are most, followed by 2-level and 3-level lesions. Anterior decompressive surgery was performed in all these patients. At the end of the study, our surgical strategy seems favorable, because 75% of these patients gained an excellent or good result. Amyotrophic lateral sclerosis sometimes can closely resemble CSA. Thus, it is essential to perform careful neurological evaluations to avoid confusion with amyotrophic lateral sclerosis, especially when surgical strategy is planned. Usually, CSA involves only a few muscles, but in patients with amyotrophic lateral sclerosis, muscles innervated by the upper cervical cord can be affected. If it is difficult to distinguish between the two diseases according to clinical manifestations, electrophysiologic examination should be performed. There are several limitations to this retrospective study. First, we only investigated the recovery of muscle strength, the surgical outcomes were not assessed by modified Japanese Orthopaedic Association scale score, Neck Disability Index, or other scales, which should be needed to make this study more valuable. Second, only a few possible factors were evaluated, further evaluation of imaging studies or electrophysiologic studies might reveal additional predictive factors. Third, in order to improve homogeneity, NRC patients were excluded in the analysis of predictive factors, but patients with SCC were not further stratified due to the relatively small number of cases. Thus, further studies with more possible factors and larger sample size are necessary to confirm these findings. In conclusion, we have demonstrated the outcome of anterior decompressive surgery for proximal-type CSA, together with the predictive factors relating to the prognosis. Selective damage to either ventral nerve root or anterior horn may cause CSA. NRC on MRI indicates a good surgical outcome. In patients with SCC, a long duration of disease is a risk factor for poor prognosis. For these patients, we recommend that timely surgical intervention should be performed if conservative treatment is ineffective.
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Conflict of interest [12]
The authors do not have any possible conflicts of interest. [13]
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Dorsen M, Ehni G. Cervical spondylotic radiculopathy producing motor manifestations mimicking primary muscular atrophy. Neurosurgery, 1979; 5 (4):427-431. Yanagi T, Kato H, Sobue I. Clinical characteristics of cervical spondylotic amyotrophy. Rinsho Shinkeigaku, 1976; 16 (7):520-528. Brain WR, Northfield D, Wilkinson M. The neurological manifestations of cervical spondylosis. Brain, 1952; 75 (2):187-225. Keegan JJ. The cause of dissociated motor loss in the upper extremity with cervical spondylosis. J Neurosurg, 1965; 23 (5):528-536. Matsunaga S, Sakou T, Imamura T, et al. Dissociated motor loss in the upper extremities. Clinical features and pathophysiology. Spine (Phila Pa 1976), 1993; 18 (14):1964-1967. Shinomiya K, Komori H, Matsuoka T, et al. Neuroradiologic and electrophysiologic assessment of cervical spondylotic amyotrophy. Spine (Phila Pa 1976), 1994; 19 (1):21-25. Gebere-Michael SG, Johnston JC, Metaferia GZ, et al. Bilaterally symmetric cervical spondylotic amyotrophy: A novel presentation and review of the literature. J Neurol Sci, 2010; 290 (1-2):142-145. Imajo Y, Kato Y, Kanchiku T, et al. Pathology and prognosis of proximal-type cervical spondylotic amyotrophy: New assessment using compound muscle action potentials of deltoid and biceps brachii muscles. Spine (Phila Pa 1976), 2011; 36 (7):E476-481. Mori K, Yamamoto T, Nakao Y, et al. Cervical spondylotic amyotrophy treated by anterior decompression. Three case reports. Neurol Med Chir (Tokyo), 2006; 46 (7):366-370. Shibuya R, Yonenobu K, Yamamoto K, et al. Acute arm paresis with cervical spondylosis: Three case reports. Surg Neurol, 2005; 63 (3):220-228; discussion 228. Tofuku K, Koga H, Yone K, et al. Conservative treatment with hyperbaric oxygen therapy for cervical spondylotic amyotro-
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Journal of Back and Musculoskeletal Rehabilitation 28 (2015) 261–266 DOI 10.3233/BMR-140513 IOS Press
Predictive factors relating to prognosis of anterior decompressive surgery for proximal-type cervical spondylotic amyotrophy Ling-De Kong1, Lin-Feng Wang1, Jing-Tao Zhang, Ying-Ze Zhang, Wen-Yuan Ding and Yong Shen∗ Department of Spine Surgery, The Third Hospital of Hebei Medical University, Shijiazhuang, Hebei, China
Abstract. BACKGROUND AND OBJECTIVE: Cervical spondylotic amyotrophy (CSA) is a relatively rare disorder. This study was conducted to elucidate the prognosis of proximal-type CSA after anterior decompressive surgery by evaluating clinical factors and imaging findings. METHODS: Anterior decompressive surgery was performed in 40 patients with proximal-type CSA between March 2000 and December 2011. Patients were classified into 2 categories based on axial T2-weighted magnetic resonance imaging (MRI) findings: “nerve root compression (NRC)”, with nerve root compressed at the intervertebral foramen, and “spinal cord compression (SCC)” with spinal cord compressed at the medial or paramedial site of spinal canal. Manual muscle testing (MMT) was used to evaluate the surgical effect. Scapular, deltoid, and biceps brachii muscles of the affected side were tested and the sum scores were calculated. Clinical factors and imaging findings, such as age, duration of disease, preoperative MMT grade, number of affected levels and signal intensity changes of spinal cord, were collected to analyze prognostic factors. RESULTS: After anterior decompressive surgery, 30 patients (75%) showed an improvement. NRC was observed in 6 patients and SCC in the rest 34 patients based on MRI findings. All patients (100%) with NRC had an improvement, while only 24 patients (70.6%) with SCC improved. In patients with SCC, there was a significant difference in duration of disease between patients who had an improvement and those who had not (P < 0.01). CONCLUSIONS: Anterior decompressive surgery is effective in the treatment of most patients with CSA. NRC on MRI may indicate a good surgical outcome. In patients with SCC, a long duration of disease is a risk factor for poor prognosis. Keywords: Cervical spondylotic amyotrophy, anterior surgery, predictive factor, magnetic resonance imaging
1. Introduction Cervical myelopathy and radiculopathy due to cervical spondylosis are well-known cervical disorders. But occasionally, patients with cervical spondylosis present with weakness and wasting of upper limb mus∗ Corresponding author: Yong Shen, Department of Spine Surgery, The Third Hospital of Hebei Medical University, 139 Ziqiang Road, Shijiazhuang 050051, Hebei, China. Tel.: + 86 0311 88602316; Fax: +86 0311 88602016; E-mail: [email protected]. 1 The first two authors contributed equally to this article.
cles without significant sensory deficits or gait disturbance, this condition is referred to as cervical spondylotic amyotrophy (CSA) [1,2]. A patient with this condition was first described by Brain [3], and many reports of this syndrome followed [1,4–6]. According to the most predominantly affected muscle groups, CSA is classified as either proximal-type (scapular, deltoid, and biceps) or distal-type (triceps, forearm, and hand). Difficulty in shoulder abduction, positive armdrop sign, or positive wrist-drop sign is always found in those patients. CSA usually presents as a unilateral disorder. In rare case, it is reported to have bilateral up-
c 2015 – IOS Press and the authors. All rights reserved ISSN 1053-8127/15/$35.00
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L.-D. Kong et al. / Prognosis of anterior decompressive surgery for proximal type CSA
per limbs involved [7]. The pathophysiology of CSA has not been clarified, but two different mechanisms have been proposed to explain the pathogenesis. Selective damage to either ventral nerve root or anterior horn may cause CSA [4,5,8]. Treatments of CSA include conservative and operative management [9–11]. Inui et al. [12] recommended that conservative treatment should be initially tried, and if conservative treatment failed, surgical intervention was indicated. However, even with surgical treatment, some patients may not benefit from surgery to the extent that they regain the muscle strength of upper extremity. There are a few studies investigate prognostic factors of surgical treatment for CSA [13–15], but the patient populations are heterogeneous, because the ventral nerve root lesion and the anterior horn lesion are not clearly distinguished. As we know, the essential pathophysiologies of the two types of lesion are obviously different. Thus, we made an effort to identify the lesion type of CSA on the basis of magnetic resonance imaging (MRI) findings, and then elucidated the prognostic factors of postoperative patients by evaluating clinical factors and imaging findings.
2. Methods 2.1. Patient population After institutional ethics board approval, a retrospective study was performed in our institution for patients with proximal-type CSA who underwent surgery between March 2000 and December 2011. The inclusion criteria were as follows: presence of severe muscle atrophy of the shoulder girdle muscles; presence of MRI-documented spinal cord compression and/or nerve root compression; mild or no sensory deficit in the upper extremity; absence of gait disturbance or abnormal tendon reflexes; having no subjective improvement of symptom or objective improvement of muscle strength after continuous cervical traction for 2 to 3 weeks. Patients with ossification of posterior longitudinal ligament of the cervical spine, cervical disc herniation, or subjective symptoms or neurologic findings associated with neuropathy were excluded. To exclude patients with amyotrophic lateral sclerosis, we performed careful neurological evaluations. If it was difficult to differentiate between amyotrophic lateral sclerosis and proximal-type CSA, additional electrophysiologic examination was performed. The final decision was made by a spine surgeon and a neurologist in consensus.
2.2. Surgical procedure All surgery was performed by a single surgeon (Y. Shen). Cervical anterior decompression and fusion was adopted for every case, even if patients suffered a lesion involving 3 intervertebral levels. The surgical procedures could be anterior cervical disectomy and fusion (ACDF) or anterior cervical corpectomy and fusion (ACCF). Extensive decompression was performed including removal of the affected discs or vertebrae, osteophytes, and posterior longitudinal ligament to expose the dura throughout the length of the discectomy or corpectomy. Additional uncinate processes were partially resected when patients had a foraminal stenosis due to uncovertebral osteophytes. Finally, a cervical cage or a titanium mesh cage filled with autologous bone grains was inserted into the intervertebral space to guarantee firm fusion. 2.3. Assessment of surgical outcome Manual muscle testing (MMT) was used to quantify the muscle strength. Scapular, deltoid, and biceps brachii muscles of the affected side were tested, and the sum scores of the muscles, which rang from 0 to 15, were calculated. The grade of recovery gained by surgical treatment at the final follow-up was in comparison with that at admission. Improvements in the sum scores were classified from excellent to poor (excellent, 3 or more scores of recovery by MMT; good, 1 to 2 scores of recovery by MMT; fair, no improvement by MMT; poor, worsening by MMT). Grades of excellent and good neurologic recovery were considered as “improvement”, and grades of fair and poor as “no improvement”. 2.4. Relevant factors Relevant clinical factors, such as age, sex, duration of disease, were collected from the patients’ records. MRI yielded factors such as number of affected levels and signal intensity changes of spinal cord. Furthermore, MRI findings were classified into 2 categories: “nerve root compression (NRC)” and “spinal cord compression (SCC)”. Patients with NRC were characterized by having nerve root compressed alone at the intervertebral foramen on T2-weighted axial view (Fig. 1a), having no cord compression nor signal intensity changes on T1- or T2-weighted sagittal view. However, patients with SCC had spinal cord compressed at the medial or paramedial site of spinal
L.-D. Kong et al. / Prognosis of anterior decompressive surgery for proximal type CSA
a
b
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c
Fig. 1. a Axial T2-weighted MRI showed nerve root compression (NRC) on the left C5 nerve root at the C4-5 intervertebral foramen. b Axial T2-weighted MRI showed spinal cord compression (SCC) at the paramedial site of spinal canal behind the C4-5 intervertebral level. c Axial T2-weighted MRI showed both nerve root and spinal cord were compressed at the C4-5 intervertebral level.
canal (Fig. 1b), combined with or without signal intensity changes on MRI. Patients with both NRC and SCC were also considered as SCC (Fig. 1c). MRI findings were independently evaluated by 2 spine surgeons, and the final results were formed by consensus discussion between the 2 surgeons. Surgical outcomes were evaluated in all patients. To determine which prognostic factors relate to surgical outcomes, we compared each of the clinical factors and imaging findings between patients who had an improvement and those who had not. 2.5. Statistical analysis Data were analyzed using the Statistical Package for the Social Sciences (version 13.0 for Windows; SPSS, Chicago, IL, USA). Chi-square test and MannWhitney U test were used to analyze qualitative data and quantitative date, respectively. P < 0.05 was considered to indicate a statistically significant difference.
3. Results Forty proximal-type CSA patients were enrolled in the study, consisted of 31 men and 9 women, with the age at the initial visit of (57.8 ± 11.2) years. The duration of disease was (11.5 ± 8.9) months and overall follow-up period was (71.2 ± 34) months. The numbers of patients with intervertebral levels affected were 21 with one level, 14 with two levels, and 5 with three levels. Preoperative sum scores of scapular- deltoidbiceps brachii muscles were (9.1 ± 2.9) scores, and postoperative sum scores were (10.7 ± 3.0) scores (Table 1). No patients had bilateral upper limbs involved. There were no incidences of infections, cervical fluid leakage, esophageal or tracheal ruptures, neurological deterioration, or recurrent laryngeal nerve
Table 1 Data of patients with proximal-type CSA Parameter Total cases (no.) Sex (men: women) Age at first visit (years) Duration of disease (months) Follow-up period (months) Affected intervertebral levels (no.) 1-level (no.) 2-levels (no.) 3-levels (no.) Sum scores of muscle strength (scores) Preoperative Postoperative
Value 40 31:9 57.8 ± 11.2 11.5 ± 8.9 71.2 ± 34.0 21 14 5 9.1 ± 2.9 10.7 ± 3.0
CSA cervical spondylotic amyotrophy.
palsy. Four patients complained of significant axial pain, which subsided gradually in 1–2 months without any treatment. All patients achieved solid fusion at 1 year postoperatively. Regarding improvement of MMT after surgery, 16 patients were graded as excellent, 14 patients good, 10 patients fair, and no patients poor. Therefore, 75% of patients had an improvement. Based on MRI findings, NRC was observed in 6 patients and SCC in the rest 34 patients. All patients with NRC had an improvement (excellent, 4; good, 2), but only 70.6% of patients with SCC had an improvement (excellent, 12; good 12; fair 10, Table 2). All patients with NRC are listed on Table 3. All but 2 patients had insignificant nerve root pain before surgery. Three patients had mild sensory deficits, involving mainly the C5 or C6 dermatomes. MRI showed NRC behind the C4-5 level in 4 patients and the C5-6 level in 1 patient. One patient had both the C4-5 level and the C5-6 level involved. In patients with SCC on MRI, 13 of 34 (38.2%) had signal intensity changes, and all changes were behind C4-5 or C5-6 intervertebral levels, or both. Prognostic factors were compared between 24 patients who had
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L.-D. Kong et al. / Prognosis of anterior decompressive surgery for proximal type CSA Table 2 Outcomes of surgery according to site of compression in MRI Cases with NRC (n = 6) Cases with SCC (n = 34) Total cases (n = 40)
Excellent (no.) 4 12 16
Good (no.) 2 12 14
Fair (no.) 0 10 10
Improvement rate 100.0% 70.6% 75.0%
MRI magnetic resonance imaging, NRC nerve root compression, SCC spinal cord compression. Table 3 Summary of clinical symptoms, imaging features, and outcome in 6 patients with NRC Case no. 1 2 3 4 5 6
Age at surgery 39 55 64 51 48 62
Insignificant nerve root pain No Yes Yes No Yes Yes
Mild sensory deficits No No Yes No Yes Yes
Affected intervertebral levels in MRI C4-5 C4-5,C5-6 C4-5 C5-6 C4-5 C4-5
Sum scores of preoperative MMT 12 10 7 10 12 7
Sum scores of postoperative MMT 15 13 9 14 14 10
Surgical outcome Excellent Excellent Good Excellent Good Excellent
NRC nerve root compression, MRI magnetic resonance imaging, MMT manual muscle testing. Table 4 Predictive factors relating to prognosis in 34 cases with SCC No. of cases Age at first visit (years) Duration of disease (months) Sum scores of preoperative muscle strength (scores) No. of affected intervertebral levels (single: multiple) Signal intensity change Low signal on T1 MRI (yes: no) High signal on T2 MRI (yes: no)
Improvement 24 57.9 ± 10.3 6.2 ± 2.3 9.2 ± 3.1 11:13
No improvement 10 60.5 ± 11.6 23.5 ± 10.1 8.7 ± 2.7 5:5
P value – 0.52 < 0.01 0.57 0.55
3:21 9:15
1:9 4:6
0.74 0.88
SCC spinal cord compression, MMT manual muscle testing, MRI magnetic resonance imaging.
an improvement and 10 patients who had not. There was a significant difference in duration of disease between the two groups (6.2 ± 2.3 months vs. 23.5 ± 10.1 months, P < 0.01). Other factors, such as age, preoperative MMT, number of affected intervertebral levels, signal intensity changes on MRI, showed no significant difference (Table 4).
4. Discussion The pathophysiology of CSA has not been clarified, but two different mechanisms have been proposed. Keegan [4] demonstrated from autopsy finding that selective damage to the ventral nerve root was the cause of CSA. However, Fujwara [16] attributed CSA to a vascular insufficiency mechanism to the anterior horn cell. Shinomiya et al. [6] proposed on the basis of electrophysiologic findings that both ventral nerve root lesion and anterior horn lesion might cause this syndrome. From the axial view of MRI, both NRC and SCC were observed in CSA patients. It seems that
there are two groups of patients, in one group, the disease is attributable to selective ventral root lesion, which presents with NRC on MRI; in the other group, the disease is caused by an injury to the anterior horn, which presents with SCC on MRI. An understanding of the pathophysiology of this syndrome is essential to ascertain prognostic factors. In this study, only 6 patients showed NRC on MRI. Though the number of those patients is small, their surgical outcomes were satisfactory. All of them showed excellent or good neurologic status at final follow-up. This might due to the fact that the ventral nerve root has greater ability to recover compared with the anterior horn. On the basis of the two mechanisms discussed above, it is logical to speculate that NRC on MRI usually indicates a good surgical outcome. As shown in Table 3, CSA patients with NRC tend to present with mild sensory deficits and nerve root pain. Besides, C4-5 is the most frequently involved intervertebral level in the 6 patients, which means that C5 nerve root is associated with the amyotrophy. It has to be noticed that C5 nerve root palsy is also well
L.-D. Kong et al. / Prognosis of anterior decompressive surgery for proximal type CSA
recognized as a complication after cervical laminoplasty, and patients with postoperative C5 palsy generally have a good recovery too [17]. However, there seems to be no association between the 2 types of paralysis in essential etiology. Of the 34 patients with SCC, only 24 patients showed an improvement in neurologic status at final follow-up. Regardless of the absence of symptoms in the lower extremities, these CSA patients were considered to be closely related to cervical myelopathy. Thus, factors that have been proven to be correlated with prognosis of cervical myelopathy were collected and analyzed. The result showed that patients with a long duration of disease tended to have a poor surgical outcome. Based on this result, we recommend that timely surgical intervention should be performed for proximal-type CSA patients if conservative treatment failed, as delayed surgical intervention may lead to losing the best opportunity for patients to get a satisfactory outcome. The role of high signal intensity on T2-weighted MRI or low signal intensity on T1-weighted MRI in CSA patients has been studied [16,18]. We observed that all signal intensity changes were behind C4-5 or C5-6 intervertebral levels, which implicates that impairment of C4, C5 segment of the cervical cord might contribute to the pathology of proximal-type CSA. The pathology of this signal abnormality has been assumed to vary from acute edema to chronic myelomalacia, and is associated with a poor prognosis of cervical myelopathy [19]. However, in this study, these signal abnormalities could not reveal the prognosis of surgical treatment for CSA, and this result is consistent with previous studies [14,15]. A possible reason for this phenomenon is that the spinal cord lesion can not reflect the pathological changes of anterior horn. For example, even if the spinal cord is severely damaged, the anterior horn part may suffer only a slight lesion. The methods of operative treatment for CSA are still controversial. Both anterior approach and posterior approach have been reported to be effective [9,20,21]. Fujiwara et al. [22] described performing laminoplasty with or without selective foraminotomy for 32 patients, and reported excellent or good results in the most CSA patients. Shinomiya et al. [6] reported 10 patients of anterior decompression and fusion for proximal-type CSA, and found that all patients had an improvement. Zhang et al. [21] analyzed the records of 21 proximaltype patients who underwent anterior decompressive surgery, and observed that 81% of patients gained 1 or more grades of muscle power improvement. Usually,
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posterior approach is indicated for patients with a lesion involving multiple intervertebral levels. However, laminoplasty has the disadvantage of leaving the anterior compressive lesion as it is. Besides, patients with a straight or kyphotic curvature of the cervical spine would not be ideal candidates for posterior decompression. On the other hand, anterior decompression and fusion is believed to provide an optimal chance of neurological recovery through the complete elimination of the ventral compression. Unlike distal-type CSA, the proximal type is characterized by less numbers of affected intervertebral levels [15,22]. In our study, lesions involving 1 intervertebral level are most, followed by 2-level and 3-level lesions. Anterior decompressive surgery was performed in all these patients. At the end of the study, our surgical strategy seems favorable, because 75% of these patients gained an excellent or good result. Amyotrophic lateral sclerosis sometimes can closely resemble CSA. Thus, it is essential to perform careful neurological evaluations to avoid confusion with amyotrophic lateral sclerosis, especially when surgical strategy is planned. Usually, CSA involves only a few muscles, but in patients with amyotrophic lateral sclerosis, muscles innervated by the upper cervical cord can be affected. If it is difficult to distinguish between the two diseases according to clinical manifestations, electrophysiologic examination should be performed. There are several limitations to this retrospective study. First, we only investigated the recovery of muscle strength, the surgical outcomes were not assessed by modified Japanese Orthopaedic Association scale score, Neck Disability Index, or other scales, which should be needed to make this study more valuable. Second, only a few possible factors were evaluated, further evaluation of imaging studies or electrophysiologic studies might reveal additional predictive factors. Third, in order to improve homogeneity, NRC patients were excluded in the analysis of predictive factors, but patients with SCC were not further stratified due to the relatively small number of cases. Thus, further studies with more possible factors and larger sample size are necessary to confirm these findings. In conclusion, we have demonstrated the outcome of anterior decompressive surgery for proximal-type CSA, together with the predictive factors relating to the prognosis. Selective damage to either ventral nerve root or anterior horn may cause CSA. NRC on MRI indicates a good surgical outcome. In patients with SCC, a long duration of disease is a risk factor for poor prognosis. For these patients, we recommend that timely surgical intervention should be performed if conservative treatment is ineffective.
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Conflict of interest [12]
The authors do not have any possible conflicts of interest. [13]
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