Abstract
Background
To investigate the relationship between neurological deficit and subsequent recovery as assessed by ASIA score and findings of electrodiagnostic study in acute spinal cord injury (SCI) patients.
Methods
Thirty-five patients with acute SCI presenting within 48 h of injury were clinically evaluated for the level, extent, and severity of SCI according to the ASIA standards in a tertiary-level care center. Electrodiagnostic studies of bilateral two motor (tibial and peroneal), one sensory (sural) nerves, and five muscles [iliopsoas, vastus medialis, tibialis anterior, gastrocnemius, and extensor hallucis longus (EHL)] were conducted and repeated at 3 months and 6 months.
Results
The neurological recovery was highly significant (p < 0.001) at 6 months. The difference in mean amplitude was statistically significant (p < 0.05) for all the nerves; mean conduction velocity significant for peroneal and sural nerves, and with no significant difference in mean latency. The differences in mean recruitment of motor unit potential (MUP) and mean peak-to-peak amplitude were highly significant (p < 0.001). Statistically significant kappa agreement between neurological recovery according to ASIA score and nerve conduction velocity was found for right tibial nerve (K = 0.324); electromyography finding of recruitment of MUP with right and left tibialis anterior (k = 0.400) and left EHL (k = 0.407); peak-to-peak amplitude with right tibialis anterior (k = 0.211), right gastrocnemius (k = 0.390), and right EHL (k = 0.211).
Conclusions
There is a strong relationship between electrodiagnostic findings and ASIA scoring to predict neurological deficit and subsequent recovery after acute traumatic SCI. Serial neurologic evaluation by ASIA score and electrodiagnostic studies may help in designing customized rehabilitation programs for the patients according to the expected neurological recovery; and evaluating future research in the field of SCI with more scientific authenticity.
Keywords: Spinal cord injury, magnetic resonance imaging, Electromyography, Nerve conduction, ASIA score
Introduction
Spinal cord injury (SCI) following trauma is a common scenario presenting to any health care facility. The clinical presentation is highly variable ranging from no neurological deficit to incomplete or complete paralysis with or without bowel bladder incontinence depending on the severity and level of SCI [1, 2]. Clinical examination of these patients is commonly done with the help of American Spine Injury Association (ASIA) scale by the treating clinicians for assessment of degree of injury and prognosis [3, 4].
Clinical assessment predicts the level, severity, and various neurological components, which is supported by radiological investigations including radiographs, computed tomography (CT), and magnetic resonance imaging (MRI). There are diagnostic tools which integrate electrophysiological findings [electromyography (EMG) and nerve conduction velocity (NCV)] of patient and supplement clinical and neuro-radiological investigations. EMG is a technique for evaluating and recording the electrical activity produced by skeletal muscles in different signals/electromyograph forms. Electrical activity can be assessed by analysis of frequency, spectrum, amplitude, or root mean square of electrical action potentials. The results of these correspond better with the clinical manifestation than do the results of MRI [5]. Nerve conduction study (NCS) is a test for studying the conduction of signals through a nerve and shows the condition of the best surviving nerve fibers [6]. These both tools are not only helpful in differentiating various neurological affections at different parts of spinal cord system but also define more objective parameters, so compliance is also better in un-cooperative patients.
As the numbers of patients with SCI are increasing day by day, increased need is felt to investigate diagnostic tools that can predict the neurological prognosis. The information gained from these tools can help in counseling the anxious relatives, forecasting length of stay, expenditure in the hospital, and customizing rehabilitation. We conducted a prospective study aimed to investigate the relationship between neurological deficit and subsequent recovery as assessed by ASIA score and findings of electrodiagnostic study in acute spinal cord injury (SCI) patients.
Materials and Methods
This prospective study was carried out on 35 patients with acute SCI presented within 48 h of injury to author’s tertiary health care center during a period from June 2014 to November 2016. The study was approved by institutional review board and ethical committee. Prior written informed consent was taken from each patient explaining the procedure, risks, and benefits. Patients with non-traumatic cause for SCI, patients with head injury/medically unstable condition, patients with previous implanted metallic devices, patients with claustrophobia, pacemakers and cochlear implants, patients presenting with previous neurological deficits, and gunshot wounds were excluded from the study.
Detailed informative history of the patient was taken in a chronological order. General physical examination and neurological examination of the patient were performed. Clinical assessment (sensory score, motor score, and zone of partial preservation) was done at the time of admission, 3rd day, 7th day, 3 months, and 6 months as per the international guidelines [3]. Traumatic SCI was classified into five categories on the ASIA Impairment Scale [4]. Plain roentgenogram examination (lateral, antero-posterior film) was done. Routine laboratory investigation for preanaesthetic check-up was done in patients requiring surgery. MRI was done in all cases within 48 h of injury to assess the health of spinal cord and electrodiagnostic tests were after patient was stable (usually within 2 weeks). Patient who needed surgery for unstable vertebral column injuries was operated as per requirement and electrodiagnostic studies was done preoperatively.
Clinical evaluation and plain radiography were done at each follow-up. EMG and NCV were done at 3 month and 6 month follow-up. Neurological recovery was documented as per ASIA impairment scale (AIS), and following outcome was measured and assessed. Neurologic outcome/recovery was assessed after doing neurological examination on each follow-up. Any increase in motor power, regain of bladder sensation, and bladder and bowel recovery was noticed, and the patient was graded as per ASIA score [3, 4].
Electrophysiological study was done in the Department of Physiology using an Aleron 401 model electromyography machine for determination of nerve conduction velocity and electromyogram. The following electrophysiological tests were performed after explaining the procedure to patient in his/her own language, to allay apprehension. Bilateral tibial and peroneal nerves were tested for motor NCS and bilateral sural nerves were tested for sensory NCS. For EMG study, iliopsoas, vastus medialis, tibialis anterior, gastrocnemius, and extensor hallucis longus (EHL) of bilateral lower limbs were tested. Insertional and spontaneous activity was observed in all the above tested muscles, and recruitment of motor units and peak-to-peak amplitude of Motor Unit Potentials (MUPs) were also recorded.
Statistical Analysis
Nominal variables (means and standard deviation) were analyzed using Student’s t test and repeated measure analysis of variances (ANOVA). Chi-square test, Friedman ANOVA, and Cochran’s Q test were implied for categorical and ordinal data, while Spearman coefficient of correlation was employed for find out correlation between variables using Standard Statistical Software (SPSS version 20.0) and a p value of < 0.05 was considered statistically significant.
Results
The mean age of patients was 31.34 ± 10.63 years (range 16–65 years). Total 29 were males and six were females. Severe pain, swelling, and deformity preceded by trauma were the universal presenting symptoms in this series of patients. Next, most common presenting symptoms were weakness in lower limbs (94.3%) and retention of urine (77.1%). In reference to neurological assessment, initial assessment and any kind of recovery at subsequent follow-ups like increase in motor power, regaining sensations, voluntary anal contraction, regain of bladder sensation, and bladder and bowel recovery were evaluated and graded as per ASIA score [3, 4].
Table 1 depicts distribution of subjects according to their neurological status estimated by ASIA score. The neurological recovery was highly significant (p < 0.001) by Friedman ANOVA test.
Table 1.
Distribution of subjects according to their neurological status estimated by ASIA score (n = 35)
| ASIA score | Initial | 3 months | 6 months | Significance (p)a |
|---|---|---|---|---|
| A | 7 (20.0%) | 0 (0.0%) | 0 (0.0%) | – |
| B | 0 (0.0%) | 0 (0.0%) | 0 (0.0%) | – |
| C | 20 (57.1%) | 17 (48.6%) | 6 (17.1%) | 0.023 |
| D | 6 (17.1%) | 8 (22.9%) | 11 (31.4%) | 0.468 |
| E | 2 (5.7%) | 10 (28.6%) | 18 (51.4%) | 0.002 |
| Median | C | D | E | < 0.001 |
aFriedman ANOVA test
Table 2 depicts descriptive statistics of results of motor NCS of tibia and peroneal nerves initially and at subsequent follow-ups along with normative data. There was no statistically significant difference in mean latency at various follow-up visits for both the nerves. The difference in mean amplitude at various follow-up visits was statistically significant (p < 0.05) for both the nerves. The difference in mean conduction velocity of tibial nerve at various follow-up visits was statistically non-significant, but was statistically significant (p < 0.05) for peroneal nerve.
Table 2.
Descriptive statistics of result of Motor nerve conduction study of tibial and peroneal nerve initially and at follow-ups along with normative data (n = 35)
| Motor nerve | Initial | 3 months | 6 months | Significance (p)a |
|---|---|---|---|---|
| Latency (ms) | ||||
| Tibial nerve (mean ± SD) | ||||
| Right | 8.73 ± 4.34 | 9.02 ± 4.24 | 9.26 ± 3.99 | 0.484 |
| Left | 8.86 ± 4.84 | 9.39 ± 4.40 | 9.43 ± 4.04 | 0.480 |
| Peroneal nerve (mean ± SD) | ||||
| Right | 4.55 ± 4.91 | 4.86 ± 4.86 | 5.36 ± 4.66 | 0.504 |
| Left | 4.50 ± 4.67 | 5.01 ± 4.74 | 5.72 ± 4.99 | 0.171 |
| Normative data (mean ± SD) | 4.5 ± 0.8 (tibial nerve) | |||
| 4.8 ± 0.8 (peroneal nerve) | ||||
| Amplitude (mV) | ||||
| Tibial nerve (mean ± SD) | ||||
| Right | 5.50 ± 6.20 | 6.50 ± 6.65 | 7.01 ± 6.53 | < 0.001 |
| Left | 5.59 ± 6.11 | 6.78 ± 6.54 | 7.55 ± 6.32 | 0.003 |
| Peroneal nerve (mean ± SD) | ||||
| Right | 1.84 ± 2.97 | 2.40 ± 3.23 | 3.09 ± 3.47 | < 0.001 |
| Left | 1.74 ± 2.87 | 2.34 ± 3.08 | 2.90 ± 3.17 | < 0.001 |
| Normative data (mean ± SD) | 12.9 ± 4.8 (tibial nerve) | |||
| 5.9 ± 2.6 (peroneal nerve) | ||||
| Conduction velocity (m/s) | ||||
| Tibial nerve (mean ± SD) | ||||
| Right | 28.53 ± 14.41 | 29.83 ± 14.08 | 31.14 ± 13.40 | 0.079 |
| Left | 26.65 ± 14.78 | 28.38 ± 13.54 | 29.47 ± 14.17 | 0.222 |
| Peroneal nerve (mean ± SD) | ||||
| Right | 21.43 ± 22.02 | 23.80 ± 22.46 | 25.84 ± 21.80 | 0.003 |
| Left | 20.09 ± 20.57 | 22.48 ± 20.85 | 24.51 ± 20.86 | 0.004 |
| Normative data (mean ± SD) | 47 ± 6 (tibial nerve) | |||
| 47 ± 4 (peroneal nerve) | ||||
ms milliseconds, mV millivolts, m/s meters per second
aRepeated-measures ANOVA
Table 3 depicts descriptive statistics of results of sensory NCS of sural nerve initially and at subsequent follow-ups along with normative data. There was no statistically significant difference in mean latency at various follow-up visits. The difference in mean amplitude and mean conduction velocity at various follow-up visits was statistically significant (p < 0.05).
Table 3.
Descriptive statistics of result of sensory nerve conduction study of sural nerve initially and at follow-ups along with normative data (n = 35)
| Sural nerve | Mean ± SD | |||
|---|---|---|---|---|
| Initial | 3 months | 6 months | Significance (p)a | |
| Latency (ms) | ||||
| Right | 4.30 ± 4.11 | 4.53 ± 3.66 | 5.30 ± 3.74 | 0.270 |
| Left | 4.58 ± 4.27 | 4.78 ± 3.74 | 5.61 ± 3.89 | 0.274 |
| Normative data | 2.9 ± 0.03 | |||
| Amplitude (mV) | ||||
| Right | 1.61 ± 4.08 | 2.00 ± 3.58 | 3.06 ± 4.63 | < 0.001 |
| Left | 1.54 ± 4.13 | 2.23 ± 2.34 | 3.00 ± 4.52 | < 0.001 |
| Normative data | 16.6 ± 7.5 | |||
| Conduction velocity (m/s) | ||||
| Right | 18.34 ± 16.98 | 22.11 ± 17.55 | 24.23 ± 16.81 | < 0.001 |
| Left | 16.92 ± 15.61 | 20.38 ± 15.61 | 22.47 ± 15.17 | < 0.001 |
| Normative data | 50.9 ± 5.4 | |||
ms milliseconds, mV millivolts, m/s meters per second
aRepeated-measures ANOVA
Table 4 depicts the comparison of NCS findings in study subjects with normative data. Regarding latency, difference in findings among study subjects and normative data was found statistically significant in bilateral tibial nerve and sural nerve initially as well as on follow-up visits. Similarly regarding amplitude and conduction velocity, difference in findings among study subjects and normative data were found statistically significant in bilateral tibial nerve, peroneal nerve, and sural nerve initially as well as on follow-up visits.
Table 4.
Two tailed t test comparing results of NCS in study subjects with normative data (n = 35)
| Mean difference (p value) | |||
|---|---|---|---|
| Initial | 3 months | 6 months | |
| Latency (ms) | |||
| Tibial nerve | |||
| Right | 4.23 (< 0.001) | 4.52 (< 0.001) | 4.76 (< 0.001) |
| Left | 4.36 (< 0.001) | 4.89 (< 0.001) | 4.93 (< 0.001) |
| Peroneal nerve | |||
| Right | − 0.25 (0.767) | 0.06 (0.943) | 0.56 (0.486) |
| Left | − 0.3 (0.709) | 0.21 (0.797) | 0.92 (0.285) |
| Sural nerve | |||
| Right | 1.4 (0.048) | 1.63 (0.010) | 2.4 (< 0.001) |
| Left | 1.68 (0.023) | 1.88 (0.004) | 2.71 (< 0.001) |
| Amplitude (mV) | |||
| Tibial nerve | |||
| Right | − 7.4 (< 0.001) | − 6.4 (< 0.001) | − 5.89 (< 0.001) |
| Left | − 7.31 (< 0.001) | − 6.12 (< 0.001) | − 5.35 (< 0.001) |
| Peroneal nerve | |||
| Right | − 4.06 (< 0.001) | − 3.5 (< 0.001) | − 2.81 (< 0.001) |
| Left | − 4.16 (< 0.001) | − 3.56 (< 0.001) | − 3.0 (< 0.001) |
| Sural nerve | |||
| Right | − 14.99 (< 0.001) | − 14.60 (< 0.001) | − 13.54 (< 0.001) |
| Left | − 15.06 (< 0.001) | − 14.37 (< 0.001) | − 13.60 (< 0.001) |
| Conduction velocity (m/s) | |||
| Tibial nerve | |||
| Right | − 18.47 (< 0.001) | − 17.17 (< 0.001) | − 15.86 (< 0.001) |
| Left | − 20.35 (< 0.001) | − 18.62 (< 0.001) | − 17.53 (< 0.001) |
| Peroneal nerve | |||
| Right | − 25.57 (< 0.001) | − 23.20 (< 0.001) | − 21.16 (< 0.001) |
| Left | − 26.91 (< 0.001) | − 24.52 (< 0.001) | − 22.49 (< 0.001) |
| Sural nerve | |||
| Right | − 32.56 (< 0.001) | − 28.79 (< 0.001) | − 26.67 (< 0.001) |
| Left | − 33.98 (< 0.001) | − 30.52 (< 0.001) | − 28.43 (< 0.001) |
ms milliseconds, mV millivolts, m/s meters per second
Tables 5 and 6 depict the EMG findings of various muscles of lower limbs initially and at follow-ups. This difference in mean recruitment of MUP and mean peak-to-peak amplitude at various follow-up visits of various muscles of bilateral lower limbs were highly significant (p < 0.001).
Table 5.
Electromyography (EMG) findings [recruitment of MUP (%)] of various lower limb muscles initially and at follow-ups (n = 35)
| Lower limb muscles | Mean ± SD | |||
|---|---|---|---|---|
| Initial | 3 months | 6 months | Significance (p)a | |
| Iliopsoas | ||||
| Right | 11.74 ± 20.97 | 28.66 ± 30.79 | 41.29 ± 27.63 | < 0.001 |
| Left | 13.43 ± 24.72 | 29.00 ± 30.02 | 41.54 ± 28.54 | < 0.001 |
| Vastus medialis | ||||
| Right | 13.80 ± 23.19 | 22.83 ± 25.13 | 41.09 ± 27.61 | < 0.001 |
| Left | 11.77 ± 20.77 | 23.54 ± 28.20 | 40.20 ± 30.66 | < 0.001 |
| Tibialis anterior | ||||
| Right | 8.06 ± 15.67 | 22.97 ± 27.11 | 38.91 ± 28.75 | < 0.001 |
| Left | 9.80 ± 18.31 | 20.14 ± 24.87 | 39.20 ± 30.35 | < 0.001 |
| Gastrocnemius | ||||
| Right | 10.57 ± 21.07 | 19.51 ± 24.24 | 34.34 ± 29.95 | < 0.001 |
| Left | 11.11 ± 21.36 | 19.86 ± 25.24 | 36.63 ± 31.62 | < 0.001 |
| Extensor hallucis longus | ||||
| Right | 10.77 ± 21.16 | 20.00 ± 27.44 | 34.91 ± 30.49 | < 0.001 |
| Left | 9.17 ± 18.29 | 17.91 ± 24.91 | 36.54 ± 30.32 | < 0.001 |
aRepeated-measures ANOVA
Table 6.
Electromyography (EMG) findings [peak-to-peak amplitude (uv)] of various lower limb muscles initially and at follow-ups (n = 35)
| Lower limb muscles | Mean ± SD | |||
|---|---|---|---|---|
| Initial | 3 months | 6 months | Significance (p)a | |
| Iliopsoas | ||||
| Right | 537.11 ± 807.19 | 947.54 ± 873.74 | 1543.03 ± 867.12 | < 0.001 |
| Left | 574.71 ± 833.69 | 932.86 ± 877.23 | 1766.00 ± 1585.28 | < 0.001 |
| Vastus medialis | ||||
| Right | 613.46 ± 793.54 | 895.06 ± 850.60 | 1400.23 ± 809.70 | < 0.001 |
| Left | 575.80 ± 730.83 | 927.00 ± 851.02 | 1566.20 ± 743.75 | < 0.001 |
| Tibialis anterior | ||||
| Right | 510.83 ± 665.82 | 969.22 ± 896.96 | 1480.23 ± 891.36 | < 0.001 |
| Left | 518.80 ± 667.95 | 885.63 ± 903.36 | 1388.23 ± 798.81 | < 0.001 |
| Gastrocnemius | ||||
| Right | 578.71 ± 768.59 | 818.43 ± 805.90 | 1285.26 ± 904.02 | < 0.001 |
| Left | 565.60 ± 707.99 | 922.17 ± 923.74 | 1402.66 ± 904.14 | < 0.001 |
| Extensor hallucis longus | ||||
| Right | 487.63 ± 699.08 | 745.03 ± 766.52 | 1401.63 ± 836.71 | < 0.001 |
| Left | 498.94 ± 684.91 | 805.09 ± 780.12 | 1461.94 ± 891.78 | < 0.001 |
aRepeated-measures ANOVA
As shown in Table 7, statistically significant kappa agreement between neurological recovery according to ASIA score and nerve conduction velocity findings in lower limb nerves was found with right tibial nerve (k = 0.324) only.
Table 7.
Agreement in neurological recovery according to ASIA score and nerve conduction velocity findings in lower limb
| Neurological recovery by nerve conduction velocity findings in lower limb | Neurological recovery by ASIA score | Kappa agreement | |
|---|---|---|---|
| No | Yes | ||
| Tibial nerve | |||
| Right | |||
| No | 5 | 8 | Κ = 0.324 |
| Yes | 2 | 20 | p = 0.036 |
| Left | |||
| No | 4 | 6 | Κ = 0.308 |
| Yes | 3 | 22 | p = 0.061 |
| Peroneal nerve | |||
| Right | |||
| No | 4 | 10 | Κ = 0.156 |
| Yes | 3 | 18 | p = 0.301 |
| Left | |||
| No | 4 | 11 | Κ = 0.125 |
| Yes | 3 | 17 | p = 0.393 |
| Sural nerve | |||
| Right | |||
| No | 2 | 5 | Κ = 0.107 |
| Yes | 5 | 23 | p = 0.526 |
| Left | |||
| No | 2 | 6 | Κ = 0.068 |
| Yes | 5 | 22 | p = 0.687 |
As shown in Table 8, statistically significant kappa agreement between neurological recovery according to ASIA score and electromyography finding (recruitment of MUP) in lower limb nerves was found with right and left tibialis anterior (k = 0.400) and left EHL (k = 0.407) only. Similarly, statistically significant kappa agreement between neurological recovery according to ASIA score and electromyography finding (peak-to-peak amplitude) in lower limb nerves was found with right tibialis anterior (k = 0.211), right gastrocnemius (k = 0.390), and right EHL (k = 0.211) only.
Table 8.
Agreement in neurological recovery according to ASIA score and electromyography findings in lower limb
| Neurological recovery by electromyography findings in lower limb | Neurological recovery by ASIA score | Kappa agreement | |
|---|---|---|---|
| No | Yes | ||
| Recruitment of MUP | |||
| Iliopsoas | |||
| Right | |||
| No | 0 | 2 | Κ = − 0.098 |
| Yes | 7 | 26 | p = 0.466 |
| Left | |||
| No | 0 | 1 | Κ = − 0.053 |
| Yes | 7 | 27 | p = 0.612 |
| Vastus medialis | |||
| Right | |||
| No | 1 | 1 | Κ = 0.146 |
| Yes | 6 | 27 | p = 0.275 |
| Left | |||
| No | 1 | 1 | Κ = 0.146 |
| Yes | 6 | 27 | p = 0.275 |
| Tibialis anterior | |||
| Right | |||
| No | 3 | 2 | Κ = 0.400 |
| Yes | 4 | 26 | p = 0.016 |
| Left | |||
| No | 3 | 2 | Κ = 0.400 |
| Yes | 4 | 26 | p = 0.016 |
| Gastrocnemius | |||
| Right | |||
| No | 3 | 4 | Κ = 0.286 |
| Yes | 4 | 24 | p = 0.091 |
| Left | |||
| No | 3 | 4 | Κ = 0.286 |
| Yes | 4 | 24 | p = 0.091 |
| EHL | |||
| Right | |||
| No | 3 | 4 | Κ = 0.286 |
| Yes | 4 | 24 | p = 0.091 |
| Left | |||
| No | 4 | 4 | Κ = 0.407 |
| Yes | 3 | 24 | p = 0.016 |
| Peak-to-peak amplitude | |||
| Iliopsoas | |||
| Right | |||
| No | 0 | 1 | Κ = − 0.053 |
| Yes | 7 | 27 | p = 0.612 |
| Left | |||
| No | 0 | 0 | Κ = − 0.000 |
| Yes | 7 | 28 | p = 1.000 |
| Vastus medialis | |||
| Right | |||
| No | 0 | 0 | Κ = − 0.000 |
| Yes | 7 | 28 | p = 1.000 |
| Left | |||
| No | 0 | 0 | Κ = − 0.000 |
| Yes | 7 | 28 | p = 1.000 |
| Tibialis anterior | |||
| Right | |||
| No | 1 | 0 | Κ = 0.211 |
| Yes | 6 | 28 | p = 0.042 |
| Left | |||
| No | 0 | 1 | Κ = − 0.053 |
| Yes | 7 | 27 | p = 0.612 |
| Gastrocnemius | |||
| Right | |||
| No | 2 | 0 | Κ = 0.390 |
| Yes | 5 | 28 | p = 0.004 |
| Left | |||
| No | 0 | 0 | Κ = − 0.000 |
| Yes | 7 | 28 | p = 1.000 |
| EHL | |||
| Right | |||
| No | 1 | 0 | Κ = 0.211 |
| Yes | 6 | 28 | p = 0.042 |
| Left | |||
| No | 0 | 0 | Κ = − 0.000 |
| Yes | 7 | 28 | p = 1.000 |
Discussion
Electrophysiological studies have been supplemented to the other modes of investigations in the management and assessment of acute SCI cases since last 5 decades in selective centers. These are also implemented for differential diagnosis of central (spinal cord) injuries as well as for peripheral nervous system affections. Additionally, these are also additive value in high risk cases including unconscious and un-cooperative patients, as results are unaffected by subjective variations [7]. We studied nerve conduction study (NCS) of two motor (tibial and peroneal) and one sensory nerve of both lower limb (sural).
Neurological Status
The median neurological grade at the initial presentation was C which improved to D in initial 3 months and further improved to E in the next 3 months. The neurological recovery was highly significant (p < 0.001) by the Freidman ANOVA test. Initially, maximum subjects (57.1%) were classified into grade C. 20% subjects presented with complete injury (ASIA score A) initially, whereas only 5.7% were having no deficit (ASIA score E). At the end of 6 months, maximum subjects had no deficit (51.4%). All of the patients in our study showed improvement. Several studies in the literature have documented a positive correlation of initial ASIA scores with the ultimate outcome of ambulatory capacity in patients with traumatic SCI [8, 9].
Nerve Conduction Study
Mean latency and mean conduction velocity of tibial nerve (right and left) increase with subsequent follow-up, but this change was non-significant. Increment in mean amplitude of right and left tibial nerve was statistically significant (p < 0.001 and p 0.03 for right and left, respectively). Mean latency of bilateral peroneal nerves and sural nerves increase non-significantly in subsequent follow-up. Increment in mean conduction velocity and mean amplitude of peroneal nerves was statistically significant (p = 0.003, p = 0.004 of NCV for right and left, respectively; p < 0.001 of amplitude for right and left both). Significant (p < 0.001 for right and left both) improvement in both parameters was observed for sural nerve.
Kirshblum et al. found no significant differences between the groups (study subjects versus normative data) with regard to sural latency, peroneal latency, or tibial latency. In contrast, statistically significant differences were found between the groups for sural amplitude, peroneal CMAP, peroneal NCV, tibial CMAP, and tibial NCV (p < 0.0001) [10]. Iseli et al. found the SSEP recording in parallel to the clinical examinations. In both groups, the mean amplitude of the tibial SSEP [group A (trauma) n = 39, amplitude 0.42 (SD 0.56 μV); group B (ischemia) n = 24, amplitude 0.77 (SD 0.46) μV)] was significantly reduced compared with control group [amplitude 2.6 (SD 1.54) μV; Scheffe’s test, p < 0.05] ANOVA testing of the tibial SSEP latency values of the control group [latency 40.99 (SD 3.8) ms] and the two patients groups [traumatic: 50.83 (SD 10.27) ms; ischemic: 48.80 (SD 7.3) ms] indicated a significant difference between the healthy subjects and the patients (p < 0.05) [11]. A very few studies in the literature had reported normal NCV after SCI [12, 13]. The tibial SSEP can be used to predict recovery of lower limb function and is related to outcome of ambulatory capacity. It has been reported that a loss of tibial SSEP in patients with acute SCI indicates a poor recovery and patients with an initially elicitable tibial SSEP show some recovery [14, 15]. We also observed the same and substantiated these points in the present study. We reported statistically significant (p < 0.001) differences of latencies in both tibial nerves among study subjects and normative data initially as well as on follow-up visits, while for sural nerve differences was found statistically significant only at 6 months of follow-up (p < 0.001). Whereas differences among subjects and normative value regarding amplitude and conduction velocity was found to be statistically significant in all the studied nerves of lower limbs initially as well as on subsequent visits.
Electromyography Findings
Mean recruitment of MUPs and peak-to-peak amplitude of bilateral iliopsoas, vastus medialis, tibialis anterior, gastrocnemius, and EHL of both lower limbs increased significantly at subsequent follow-up at 3 or 6 months, (p < 0.001). Curt et al. found that most of patients (70%) with acute SCI who subsequently recovered an ambulatory capacity, post-trauma MEP from the anterior tibial muscle were recorded [16]. Most patients (about 80%) who achieved a full ambulatory capacity had normal MEP latencies of anterior tibial and quadriceps femoris muscles. Only a few (< 20%) patients who suffered an initial loss of lower limb MEP finally achieved a full or functional ambulatory capacity. In the literature, a few studies had reported diminished lower limb compound motor action potentials after SCI [16–18]. Chang et al. reported that approximately 80% of patients with incomplete motor lesion MEP could be recorded from anterior tibial muscle. These patients show a slow spinal conduction velocity (a mean of 32 m/s compared to a normal value of about 60 m/s) and the MEP amplitudes were reduced [19].
Analysis of Neurological Outcomes (ASIA Score), Nerves, and Muscles with Electrodiagnostic Findings
Data analysis of Electrodiagnostic findings when analyzed according to ASIA grades showed a significant improvement over time in patients ASIA grades A, C, and D both in NCS and EMG. Patients with ASIA E grade showed only very minor variation in the parameters assessed both on NCS and EMG; and these changes were non-significant. There was no patient in the study group with ASIA B grade initially. The Literature reports even different muscles and nerves show different pattern of electrodiagnostic findings even within the same SCI individuals [10, 18–20]. Some of these electrodiagnostic changes may be caused by traction and compression of nerves during treatment and rehabilitation, distinct patterns of change development for different peripheral nerves after SCI, nerve edema, different muscle membrane instability, and variable denervation patterns between individuals and within different muscle [10, 20–22].
Correlation of Neurological Outcomes (ASIA Score) with Electrodiagnostic Findings
In the present study, statistically significant correlation of ASIA score with motor nerve conduction (MNC) velocity was found to be maximum with right peroneal nerve (0.601, 0.732, and 0.606 at 0, 3, and 6 months respectively), left peroneal nerve (0.578, 0.658, and 0.513 at 0, 3, and 6 months respectively), right tibial nerve (0.512, 0.616, and 0.569 at 0, 3, and 6 months, respectively), and left tibial nerve (0.422, 0.628, and 0.660 at 0, 3, and 6 months, respectively), by spearman’s correlation test. Similarly, statistically significant correlation of ASIA score with sensory nerve conduction (SNC) velocity was found to be with right sural nerve (0.612, 0.663, and 0.502 at 0, 3, and 6 months, respectively) and left sural nerve (0.635, 0.68, and 0.491 at 0, 3, and 6 months, respectively).
The statistically significant correlation of ASIA score with recruitment of MUP as well as peak-to-peak amplitude was found to be with all studied muscles of both lower limbs (correlation coefficient ranging from 0.677–0.422, 0.805–0.583, and 0.740–0.460 at 0, 3, and 6 months, respectively) by Spearman’s correlation test. Iseli et al. reported that the initial ASIA motor and sensory scores were strongly indicative of recovery in both groups (ischemic and traumatic SCI patients). Similar to the clinical examination, the tibial SSEP recordings were also strongly indicative for the degree of ambulatory recovery (traumatic r = 0.72, (p < 0.00001); ischemic r = 0.43, (p < 0.04). Of all the clinical and electrophysiological indices, the best prediction of outcome of ambulatory capacity was achieved by the combination of motor score and tibial SSEP recording in both the groups [11]. Rutz et al. did not reveal any significant correlation (spearman’s correlation analysis p < 0.1) between the initial electrophysiological recording and the recovery of neurological deficit (ASIA score) and the outcome of ambulatory capacity assessed at the end of rehabilitation programme [23].
In the study by Li et al., the correlation between root mean square (RMS) of the EMG signal and the ISNCSCI motor score was confirmed by Kendall correlation analysis. Kendall correlation value between overall muscles/levels, motor scores, and the RMS of the EMG data is 0.85, with the 95% CI falling into the range of 0.76–0.95. Significant correlations were also observed for the soleus (0.51), tibialis anterior (TA) (0.53), triceps (0.52), and extensor carpi radialis (ECR) (0.80) muscles. Patients with motor score of 5 had nearly significantly higher RMS EMG values than patients with motor score of 0 (p = 0.059 and 0.052, respectively). At the soleus and TA, the RMS of EMG value was significantly higher (p < 0.01) 4 patients with ASIA motor score of 5 than for those with ISNCSCI motor score of 0 [24]. Results of the present study are in agreement with the finding of Li et al. that if there is initial elicitable electrophysiological activity is present; these have significantly higher initial motor score and recovery of muscle function in subsequent follow-up [15]. Curt and Dietz reported that MEP values of lower limb were similarly sensitive and comparable to ASIA motor score of limbs in predicting recovery of ambulatory capacity [25]. This seems to valid and similar to our study that the electrophysiological studies provide supplementary information to the clinical examination. We also agree and find the present study as similar to Li et al. that recommend the development of EMG-based objective SCI characterization protocol with higher sensitivity and resolutions. These correlations will be relevant in evaluating the future research intervention in neuronal regeneration or repair [24].
Agreement in Neurological Recovery According to ASIA Score and NCV Findings
In the present study, statistically significant kappa agreement between neurological recovery according to ASIA score and NCV findings in lower limb nerve was found with right tibial nerve (k = 0.324) only as described in Table 6.
Agreement in Neurological Recovery According to ASIA Score and EMG Findings
In the present study, statistically significant kappa agreement between neurological recovery according to ASIA score and EMG finding (recruitment of MUP) was found with right and left tibialis anterior (k = 0.400) and left EHL (K = 0.407) only. Similarly, statistically significant Kappa agreement between neurological recovery according to ASIA score and EMG findings (peak-to-peak amplitude) was found with right tibialis anterior (k = 0.211), right gastrocnemius (k = 0.390), and right EHL (k = 0.211) only.
Extensive literature review did not reveal any study in the English literature reporting agreement of neurological recovery according ASIA score and NCV findings and ASIA score and EMG findings.
The present study has a few limitations. Recruitment of small number of patients in our study is the limitation of our study, but as being the first study of its kind with serial evaluation provides added strength. Further extensive studies in the future are required to develop research protocols utilizing the clinical, Electrodiagnostic, and neuroimaging modalities.
Conclusion
There is a strong relationship between electrodiagnostic findings and ASIA scoring to predict neurological deficit and subsequent recovery after acute traumatic SCI. Serial neurologic evaluation by ASIA score and electrodiagnostic studies may help in designing customized rehabilitation programs for the patients according to the expected neurological recovery; and evaluating future research in the field of SCI with more scientific authenticity.
Source of Grant
None.
Compliance with Ethical Standards
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standard statement
This article does not contain any studies with human or animal subjects performed by the any of the authors.
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Footnotes
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