Background

Degenerative cervical disease manifested as myelopathy and/or radiculopathy is a common pathological condition affecting the adult population [1]. As the spinal cord and nerve roots are located close to one other, the compressive lesions of these structures can develop concurrently. Spinal cord pathology such as cord compression and intramedullary damage is well elucidated by MRI, which plays a crucial role in degenerative cervical myelopathy (DCM) management. Cervical foraminal stenosis causing nerve root compression is also depicted by MRI. However, there are still limitations to how much they can help distinguish compressed cervical nerve root in relation to its clinical symptoms [2]. MRI findings of cervical foraminal stenosis mainly focused on structural abnormalities resulting in cervical nerve root compression: cervical disc pathology, facet joint hypertrophy and yellow ligament hypertrophy [2, 3]. Recently, nerve ultrasound (US) is becoming the established measure to directly observe cervical nerve roots and the pathological conditions [4]. Furthermore, preoperative C5 nerve root swelling has been reported in some DCM patients [5]. However, it is uncertain whether spinal cord decompression affects cervical nerve roots or not. The aim of this study was to demonstrate morphological changes in the cervical nerve roots before and after spinal cord decompression surgery in association with the amplitude of compound muscle action potentials, which represent motor function.

Materials & methods

From April 2019 to Dec 2020, a total of thirty-two consecutive degenerative cervical myelopathy patients underwent surgical treatment. The varieties of surgical procedures, such as anterior decompression with fusion, posterior laminoplasty or laminectomy with or without foraminotomy, were performed to decompress the spinal cord and nerve root. In this study, to investigate how spinal cord decompression affects the nerve root, thirteen patients with cervical degenerative myelopathy were included based on the surgical procedure aimed to decompress only the spinal cord such as laminoplasty or laminectomy. Myelopathy resulted from cervical spondylosis in nine patients, cervical disc herniation in one, and ossification of posterior longitudinal ligament (OPLL) in three. There were nine male and four female patients. The mean age of the subjects was 69 years old (58–79). The preoperative MRI demonstrated spinal cord compression and intramedullary change compatible with DCM diagnosis (Table 1). The Japanese Orthopaedic Association (JOA) score was used for the functional evaluation. The JOA score is a 17-point scale that indicates the severity of cervical myelopathy based on sensorimotor and bladder function [6]. Strength of the deltoid and bicep muscles was assessed by manual muscle testing using medical research council grade (0–5) [7].

Table 1 Patient demographics.
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All patients underwent the cervical nerve root ultrasound examination and compound muscle action potentials recorded at deltoid and biceps muscles before and two weeks after operation. The cervical nerve root ultrasound examination was performed using SONIMAGE HS1 (KONICA MINOLTA, Tokyo, Japan) with an 18-MHz linear-array transducer (L18-4). The participants were tested in the supine position. The absent C7 anterior tubercle and the large anterior tubercle of C6 are the key landmarks to confirm the cervical level. Other structures including thyroid, carotid artery and vein and scalene muscles also help us to locate cervical nerve roots. The diameter (D) and the transverse diameter (TD) of bilateral C5 and C6 nerve roots were measured at the point where the nerve emerges between the anterior and posterior tubercle of the transverse process. The cross-sectional area (CSA) was calculated using the following formula: D × TD × π/4. The measurements were made more than twice and the mean CSA value was used for analysis. The ultrasound examination was conducted by a single physician (N.T) with more than five years experience in nerve ultrasound. The intraobserver and test-retest reliabilities were evaluated before we started this study. The Intraclass correlation coefficient (ICC) estimates and their 95% confident intervals were calculated using SPSS statistical package version 23 (SPSS Inc., Chicago, IL) based on a mean-rating (k = 2), absolute-agreement, 2-way mixed-effects model [8]. The ICC was 0.95 (95% CI; 0.85–0.98). Values <0.5 are indicative of poor reliability, values between 0.5 and 0.75 indicate moderate reliability, values between 0.75 and 0.9 indicate good reliability, and values greater than 0.90 indicate excellent reliability. The results of the ICC were evaluated as “good” to “excellent.”

The degree of foraminal stenosis on MRI was evaluated using the formula reported by Kim [9]: the narrowest width of neural foramen/extraforaminal nerve root on the axial T2-weighted images at the intervertebral disc level. The correlation between foraminal stenosis on MRI and CSA of nerve roots was examined.

The compound muscle action potentials (CMAPs) were recorded using the standard EMG machine (NeuroPak, Nihon Koden, Tokyo, Japan). The recording and reference electrodes were placed on the middle of the deltoid and biceps muscles and the acromion and lateral epicondyle, respectively. The Erb-point electrical stimulation, a square wave of 0.1 ms in duration, was given at 1/s. We measured the amplitudes of CMAPs from the baseline to the negative peak.

All participants provided informed consent. This study was approved by our hospital institutional review board. This study was supported by the Grant of Japan Orthopaedics and Traumatology Research Foundation No. 395.

Wilcoxon signed rank test and Spearman’s correlation test were respectively used for the paired samples and the correlation. P < 0.05 was considered to be significant. All statistical analyses were performed with EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphical user interface for R (The R Foundation for Statistical Computing, Vienna, Austria) [10].

Results

Table 2 showed JOA scores, Manual Muscle Testing of deltoid and biceps, the CSA of the C5 and C6 nerve roots and the CMAPs of deltoid and biceps. The JOA scores before and two weeks after surgery were 8.4 (3–13.5) (95% CI: 6.3–10.5) and 11 (6.5–15) (95% CI: 9.4–12.6), respectively. All patients displayed a postoperative functional improvement without a new onset of C5 palsy.

Table 2 JOA score, MMT, CSA and CMAPs before and after surgery.
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The mean degrees of the C4–5 and C5–6 foraminal stenosis on MRI were 67.6 (25.0–123.1) (95% CI: 58.5–76.7) % and 56.5 (21.7–82.4) (95% CI: 50.1–62.9) %, respectively. Each pair of foraminal stenosis and CSA of the nerve roots, that is, C4/5 foramen and C5 nerve root, C5/6 foramen and C6 nerve root, showed no significant correlation (P = 0.53 and 0.08).

The CSA of C5 nerve root displayed no significant change between before and after surgery (P = 0.2), however, that of the C6 nerve root reduced significantly (P = 0.038) after surgery.

The amplitude of the deltoid and biceps CMAPs showed no significant change before and after surgery (P = 0.05 and 0.05).

Case presentation

A sixty-seven-year-old male patient (patient no. 5) with gait disturbance was referred to our hospital. He was diagnosed with DCM by sensorimotor dysfunction with hyperreflexia and cord compression at C4–5 and C5–6 with intramedullary signal changes shown by MRI (Fig. 1a). Both nerve root ultrasound examination and CMAP recordings were conducted before and 2 weeks after surgery (Fig. 1b–d). He underwent C4–C6 laminoplasty with good neurological recovery without C5 palsy. He could walk with a cane two weeks after surgery. The numbness in his hand had also improved. The CSA of the C6 nerve root reduced postoperatively without amplitude reduction of the deltoid and biceps muscle (Fig. 1c, d).

Fig. 1: Patient no. 5: MRI, nerve root US and CMAPs.
figure 1

a The left panel shows the mid-sagittal cervical spine MRI. It demonstrates the cord compression with the intramedullary change at C4–5 and C5–6. The right upper and lower panel showed C4–5 and C5–6 axial section, respectively. b The left and right panel show the CSA of right C5 nerve root (arrow) before and 2 weeks after surgery, respectively. Asterisks (*) indicate the anterior tubercle of the C5 transverse process. Double asterisks (**) indicate the posterior tubercle of the C5 transverse process. CSA reduction was not exhibited postoperatively. c The left and right panel shows the CSA of right C6 nerve root (arrow) before and 2 weeks after surgery, respectively. Asterisks (*) indicate the anterior tubercle of the C5 transverse process. Double asterisks (**) indicate the posterior tubercle of the C5 transverse process. CSA reduction was exhibited postoperatively. d The upper left and right panel show the preoperative and postoperative deltoid CMAPs, respectively. The lower left and right panel show the preoperative and postoperative biceps CMAPs, respectively.

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Discussion

Morphological change of the cervical nerve root had been observed after spinal cord decompression surgery. Both spinal cord and nerve root are involved in degenerative cervical spine, and radiculopathy in nonmyelopathic degenerative cervical cord compression was reported as a predictor for developing DCM [11]. Thus, nerve root assessment may be useful for evaluating cervical myelopathy in addition to cervical radiculopathy.

Because the time period between the pre- and post-operative examination was within two weeks in this study, the rapid reversible mechanisms such as inflammation and edema [12] conceivably contributed to the nerve root CSA change. Spinal cord decompression improves not only the spinal cord compression itself but also the circulatory condition at and around the compressed spinal cord; the ischemic state or vascular congestion would resolve after spinal cord decompression [13, 14]. Median nerve CSA reduction with pain and numbness improvement after steroid injection for carpal tunnel syndrome was reported [15,16,17]. And local nerve ischemia, inflammation and vascular congestion were considered underlying reversible conditions alleviated by the steroid injections [15].

MRI had a limited resolution to delineate the intra-spinal canal cervical nerve roots. In fact, the narrowing of the C4–5 and C5–6 neural foramen on axial MRI displayed no correlation with the CSA of the C5 and C6 spinal nerves. On the other hand, ultrasound examination can directly observe the nerve root at the sulcus of the transverse process. The swollen CSA of cervical nerve roots in cervical radiculopathy [4, 18] and myelopathy [5] were reported in previous cross-sectional studies. In contrast, this study focused on the longitudinal changes. Fifteen out of twenty six C5 nerve roots (57.7%) and fourteen C6 nerve roots (53.8%) showed preoperative CSA enlargement as compared to the reported normal values: C5, 6.7 ± 2.0 mm2, and C6, 11.3 ± 2.9 mm2 [19]. Sixteen C5 nerve roots (61.5%) and nine C6 nerve roots (34.6%) also showed CSA enlargement postoperatively. Although C6 nerve roots showed a significant reduction of CSA, we observed a varying degree of CSA change in each of the patients before and after surgery. The heterogeneity of cervical degenerative disease presumably explains the results. On the other hand, the deltoid and biceps CMAP amplitude assuming C5 and C6 nerve root motor function showed no significant change with no postoperative C5 palsy between before and after surgery. C6, 7 and 8 nerve roots distributed the dermatome of the hand, whereas C5 nerve root did not [20]. Thus, the significant C6 nerve root CSA change might be associated with hand sensory function improvement.

Cervical radiculopathy and cervical myelopathy are generally considered to be two separate disease entities. However, the distinct lesion site remains to be clarified in some cases; for example, patients presenting with a unilateral upper extremity weakness concomitant with spinal cord compression such as cervical spondylotic amyotrophy. The lesion site of the postoperative C5 palsy, nerve root and/or spinal cord lesion, is also not settled [21, 22]. This study showed the nerve root morphological changes after spinal cord decompression surgery, that provided us with clues to help clarify the functional connection between spinal cord and nerve root.

Since this study is a small case series and we observed a varying degree of CSA changes in each patient before and after surgery, further investigation is essential to confirm longitudinal changes of nerve roots. In addition, the correlation between sensory recovery and CSA changes had not been evaluated in this study. Spinal cord deformation and the extent of the intramedullary damage also need to be analysed. Moreover, we had no postoperative C5 palsy in this study.

In summary, the CSA of C6 nerve roots significantly reduced after spinal cord decompression, whereas CMAPs of deltoid and biceps showed no significant change between before and after surgery. Independent CSA changes on ultrasound might be useful when conducting a functional evaluation of the postoperative nerve root.