Functional Outcome Following Spinal Cord Injury: Significance of Motor-Evoked Potentials and ASIA Scores

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1 81 Functional Outcome Following Spinal Cord Injury: Significance of Motor-Evoked Potentials and ASIA Scores Attain Curt, MD, Martin E. Keck, MD, Volker Dietz, MD ABSTRACT. Curt A, Keck ME, Dietz V. Functional outcome following spinal cord injury: significance of motor-evoked potentials and ASIA scores. Arch Phys Med Rehabil 1998;79:81-6. Objective: Prediction of outcome of ambulatory capacity and hand function in tetraplegic patients with spinal cord injury (SCI) using neurologic examination, according to the protocol of the American Spinal Injury Association (ASIA) and motorevoked potentials (MEP). Design: Correlation study on a prospective cohort. Setting: SCI center, university hospital. Patients: Thirty-six patients with acute and 34 with chronic SCI. Outcome Measures: (1) ASIA motor and sensory scores, (2) MEP recordings of upper and lower limb muscles, and (3) outcome of ambulatory capacity and hand function. Results: In acute and chronic SCI, both the initial ASIA scores and the MEP recordings were significantly related (p <.0001) to the outcome of ambulatory capacity and hand function. In tetraplegic patients, the MEP of the abductor digiti minimi muscle (Spearman correlation coefficient,.75; p <.0001) and the ASIA motor score for the upper limbs (Spearman correlation coefficient,.83; p <.0001) were most related to the outcome of hand function. Ambulatory capacity could be predicted by the ASIA motor score of the lower limbs (Spearman correlation coefficient,.78; p <.0001) and by MEP recordings of the leg muscles (Spearman correlation coefficient,.77; p <.0001). In patients with acute SCI, for the period 6 months posttrauma, the ASIA motor score increased significantly (ANOVA, p <.05), whereas the ASIA sensory scores and MEP recordings were unchanged (ANOVA, p > 0.1). Conclusion: Both ASIA scores and MEP recordings are similarly related to the outcome of ambulatory capacity and hand function in patients with SCI. MEP recordings are of additional value to the clinical examination in uncooperative or incomprehensive patients. The combination of clinical examination and MEP recordings allows differentiation between the recovery of motor function (hand function, ambulatory capacity) and that of impulse transmission of descending motor tracts by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation I N PATIENTS WITH spinal cord injury (SCI), clinical and electrophysiologic examinations are directed toward assessing the extent and level of SCI and also toward predicting From the Swiss Paraplegic Centre, University Hospital Balgrist, Zurich, Switzerland. Submitted for publication June 6, Accepted in revised form August 1, Supported by the Swiss National Science Foundation (grant ) and the International Research Institute for Paraplegia (P16/93). No commercial party having a direct or indirect interest in the subject matter of this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Armin Curt, MD, Swiss Paraplegic Centre, University Hospital Balgrist, Forchstrasse 340, Zurich CH-8008, Switzerland by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation /98/ /0 functional recovery.~ Furthermore, they can be applied following SCI to assess the extent of spinal cord recovery and the relationship to the development of neurologic deficits. The standardized clinical examination according to the protocol of the American Spinal Injury Association (ASIA) allows the clinician to evaluate the extent of SCI and to predict the prognosis of functional disabilityy However, in unconscious (eg, because of trauma), uncooperative (eg, because of psychiatric disorders or drugs), or incomprehending patients (eg, with language barriers), the clinical examination and the ASIA score are of limited value. Somatosensory-evoked potentials (SSEP), although mainly reflecting dorsal column function, are related to the extent of SCI and functional recovery of hand function and ambulatory capacity in patients with acute SCI. 4'5 However, in circumscribed lesions of the spinal cord, such as in anterior cord syndrome, they are less sensitive and fail to indicate the severity of SCI. With the introduction of painless transcranial magnetic stimulation, the corticospinal tract fibers can be examined. 6 By recording motor-evoked potentials (MEP) from different limb muscles in patients with SCI, the severity of spinal cord motor tract damage and the course of recovery can be assessed. The combination of clinical examination, such as for muscle strength and functional outcome (ambulatory capacity), and MEP recordings should allow one to estimate to what degree the functional recovery following SCI is the result of the recovery of descending motor tract for impulse transmission or of a reorganization of spinal cord function below the level of lesion. The goal of the prospective study described herein was to evaluate the degree to which MEP recordings can contribute toward an improved prediction of recovery for upper and lower limb motor function. In patients with tetraplegia resulting from acute or chronic cervical SCI, MEP of the upper and lower limbs were recorded to assess (1) the involvement of proximal and distal limb muscles, (2) the relationship between MEP recordings and the recovery of motor function, (3) the prognostic value of MEP recordings in comparison with the clinical examination, and (4) the follow-up of MEP parameters in patients with acute SCI during the first 6 months post-trauma and in patients with chronic SCI in relation to functional recovery. METHODS General Procedures and Patients Patients with acute cervical SCI who were hospitalized for primary rehabilitation and outpatients with chronic cervical SCI were selected for this study between 1993 and Patients were informed of the goals of the study before giving their written consent. Patients were permitted to leave the study at any time. All of the patients selected agreed to participate in the study, and none chose to drop out. Patients with diseases of the peripheral nervous system (eg, diabetes mellitus, peripheral nerve entrapments, plexus lesion) or cerebral lesions (traumatic and nontraumatic) were excluded from the study. Patients were divided into two groups: (1) those with acute SCI (n = 36; 31 men, 5 women; median age, 40.5yrs; range, 17 to 77yrs); and (2) those with chronic SCI (n = 34; 26 men

2 82 FUNCTIONAL OUTCOME AFTER SCI, Curt 8 women; median age, 32yrs; range, 18 to 73yrs). The second patient group was clinically stable with a time interval posttrauma of at least 6 months. These patients were selected to provide clinical and electrophysiologic parameters in chronic SCI patients. Fractures of the spine were verified radiologically (X-ray or computed tomography [CT]), by magnetic resonance imaging (MRI), or both. Patients were classified as having cervical SCI depending on the neurologic level of lesion in accordance with the ASIA protocol. Only patients with neurologic levels of lesion from C2 to T1 were selected to achieve a homogenous study population with circumscribed spinal cord lesion. Clinical and electrophysiologic examinations were performed in parallel at the Paraplegic Center. The first combined examinations in acute SCI patients were performed at a median 25 days (range, 1 to 110 days) posttrauma and in chronic SCI patients at 20.5 months (range, 6 to 310 months) posttrauma. ASIA Score Neurologic examinations of all patients were performed according to 1992 ASIA standards) In patients with acute SCI, two examinations were performed. The first was performed on admission to the Center and the second 6 months later. In patients with chronic SCI, only one examination was performed. From the ASIA protocol, the following measures were taken and analyzed separately: (1) ASIA motor score (total), (2) ASIA motor score of the upper limbs, (3) ASIA motor score of the lower limbs, (4) ASIA pin prick score, and (5) ASIA light touch score. Neurologic examinations were performed by specially trained physicians working full-time in the rehabilitation center under the supervision of a senior colleague. All of the physicians had a minimum of 1 year experience in treating SCI patients. Clinical Assessment of Ambulatory Capacity The ambulatory capacity of patients was assessed as being in one of four categories: (1) no ambulatory capacity, with the patient unable to walk or stand; (2) therapeutical ambulatory capacity, with standing and walking possible but only with the support of either two physiotherapists with two braces in parallel bars or with two sticks and the help of an accompanying person (such patients could perform these procedures only as a therapeutical approach); (3) functional ambulatory capacity, with daily walking possible over short distances without the aid of physiotherapists or braces (a category of ambulatory capacity used regularly in the activities of daily living and at work); and (4) full ambulatory capacity, with little or no disturbance in walking (a categorization corresponding to that used in earlier studiest's). The ambulatory category achieved in both patient groups was assessed at the chronic stage of SCI, that is, at least 6 months post-trauma. The categorization focused on both the walking ability and the activity regularly practiced at home by the patient. Clinical Assessment of Hand Function The extent and severity of impaired hand function in tetraplegia is of crucial importance to self-independence. Hand function was assessed by a combined analysis of hand muscle paresis and the functional capability of the hand with respect to grasping movements. The results were categorized into three types corresponding to earlier studies."4 Type 1 patients had passive hand function characterized by plegia of intrinsic hand muscles and an inability to extend the wrist actively, thus the patient could not voluntarily make grasping movements. Functionally, nothing can be kept in the hand because opening and closing of the hand is only possible by supination or pronation of the wrist. Table 1: Outcome of Hand Function in Patients According to Clinical Assessment of Acute and Chronic Patient Groups Type Acute SCl (%) Chronic SCI (%) Passive Active Intrinsic Type 2 patients had active hand function, with active extension of the wrist possible, allowing passive grasping movements of the hand by tenodesis effect. Type 3 patients had intrinsic hand function, with active grasping by the intrinsic hand muscles possible (eg, lateral or pulp pinch) but with a more or less reduced muscle strength and dexterity. This category presents little or no restriction on activities performed in daily living. MEP Recordings Transcranial magnetic stimulation a was performed with the subject in a supine position. A 13cm diameter coil, with the current flow clockwise, was positioned tangentially to the scalp and centered over Cz (international 10 to 20 electrode location) for recording MEP in anterior tibialis (TA) and quadriceps femoris (QF) muscles using surface electrodes. A contralateral lateralized position was used to achieve optimal excitation from the biceps brachii (BB) and abductor digiti minimi (ADM) muscles. The motor threshold was established by slowly increasing the stimulus intensity and, once achieved, further increased by 10%. The electromyographic (EMG) signals were amplified (gain of 5000; bandpass filter, 30 to 1000Hz), allowing the latency and amplitude of the MEP to be determined. To exclude pathologic MEP recordings from peripheral nerve lesions, nerve conduction of the ulnar nerve and F-wave analysis of ADM muscle and nerve conduction of the tibial nerve and H-reflex of soleus muscle were examined. The MEP recordings were performed in parallel with the clinical examinations. Normal values were determined from 10 healthy subjects and were in accordance with previous studies Statistics Statistical evaluations were performed using a Statistical Analysis System (SAS) software package. The Wilcoxon 2 sample test, student's t test, and cbi-squared test were employed to compare measurements from distinct samples. Spearman correlation analysis was performed for paired comparisons using ordinal data. Analysis of variance (ANOVA) was used to compare the MEP values of the acute and chronic tetraplegic patients. RESULTS Outcome of Hand Function and Ambulatory Capacity Both acute and chronic SCI patients had severe impairment of hand function (table 1). Approximately 40% to 50% were characterized as having only passive hand function; approximately 20% were characterized as having active hand function; and approximately 30% to 40% of SCI patients exhibited intrinsic hand function. Both patient groups demonstrated severe impairment of ambulatory capacity (table 2). More than 40% of the patients had Table 2: Outcome of Ambulatory Capacity in Patients According to Clinical Assessment of Acute and Chronic Patient Groups Type Acute SCI (%) Chronic SCI (%) Full Functional Therapeutic None

3 FUNCTIONAL OUTCOME AFTER SCI, Curt 83 Table 3: ASIA Scores (Mean and Standard Deviation) of Acute (Initial and Follow-up Examination) and Chronic Patient Groups With Cervical SCI Acute SCI (n = 36) Initial Examination Chronic SCI Increment After 6 Months (n - 34) ASiA Scores Mean SD Mean SD Percentage Mean SD Motor (total) * Upper limb * Lower limb * Light touch Pin prick * Scores with a significant increase, Wilcoxon 2 sample test, p < a complete paraplegia without any voluntary activity of the lower limbs. Approximately 10% of the patients showed only a therapeutical ambulatory capacity. An additional 10% demonstrated a functional ambulatory capacity which allowed restricted movement in day-to-day living. Full ambulatory capacity was achieved in approximately 30% of the acute and 15% of the chronic patient group. The impairment was similarily distributed in both patient groups (chi-squared test, p > 0.2). ASIA Scores During the 6 months posttrauma, the acute SCI patients showed a significant increase of the total ASIA motor scores in both upper and lower limbs (Wilcoxon 2 sample test, p <.05). The increase was higher in the lower limbs (66%) in comparison with the upper limbs (34%). However, there was no significant change in the ASIA sensory scores for pin prick or light touch (Wilcoxon 2 sample test, p = 0.2). The values of the ASIA motor and sensory scores in the acute patient group 6 months posttrauma and in the chronic patient group were not statistically different (student's t test, p > 0.4; table 3). Patients with incomplete SCI showed significantly better recovery of motor functions of the upper and lower limbs in comparison with those with complete SCI (Wilcoxon 2 sample test, p <.01). Complete SCI patients showed a mean increase of motor scores for the upper limbs of 4 points and for the lower limbs of 0.5 points. In contrast, incomplete SCI patients showed a mean increase of 9 points for the upper limbs and 19 points for the lower limbs. Statistical analysis revealed that, in patients with acute and chronic SCI, the ASIA scores were significantly related to the outcome of hand function and ambulatory capacity (Spearman correlation analysis, p <.0001). The ASIA motor score for the upper limbs showed the best correlation to the outcome of hand function (correlation coeffecient of.79 for the acute patients and.83 for the chronic patients, table 4). The ASIA motor score for the lower limbs was most sensitive in predicting the outcome of ambulatory capacity (correlation coeffecient of.79 for the acute patients and.78 for the chronic patients). The ASIA sensory scores were less sensitive than the motor scores, whereas pin prick scores were only slightly superior than light touch scores (table 5). MEP Recordings In both acute and chronic SCI patients, approximately 80% of the MEP in BB were normal, whereas only 10% had normal MEP recordings in ADM. In 80% of patients, the ADM latency was pathologic; and in 90%, the ADM amplitudes were pathologic. The MEP in ADM were significantly (p <.0001) correlated to the outcome of hand function (similar to the ASIA motor score), whereas the MEP in BB showed no correlation (table 4). Approximately 90% of patients with loss of MEP in ADM during the initial examination recovered no intrinsic hand muscle function. The MEP parameters in ADM of the patient groups were significantly different from normal values (AN- OVA, p <.05). In contrast, there was no difference between the values of the MEP in BB obtained in the acute or chronic patient groups and healthy subjects. The MEP recordings in proximal and distal lower limb muscles (QF, TA) were significantly correlated to the outcome of ambulatory capacity and were as sensitive as the ASIA motor scores (table 5). Only 10% of patients with incomplete tetraplegia showed normal MEP recordings of the lower limb muscles. MEP could not be recorded from the plegic muscles in any of the patients with complete tetraplegia. Therefore, the values obtained from the leg muscles of acute and chronic patient groups were significantly different from those in normal subjects (ANOVA, p <.05). All of the patients with normal MEP in TA during the initial examination recovered to full ambulatory capacity. Only 11% of those patients lacking MEP in TA during the initial examination recovered full ambulatory capacity, whereas 78% showed no or only therapeutical ambulatory capacity. In contrast to healthy subjects, in the SCI patient groups, the MEP recordings revealed a pathologic reduction of MEP amplitudes and a prolongation of MEP latencies or were even abolished (fig 1). The reduction in amplitude was most closely related to the degree of recovery of upper and lower limb function. Follow-up examinations of the MEP recordings (6 months posttrauma) did not show a significant change of latencies or amplitudes (ANOVA, p > 0.1). The latter parameters were comparable with those in the chronic SCI patient group (fig 2). DISCUSSION The purpose of this study was to evaluate to what degree MEP recordings can aid the clinician in predicting functional recovery in patients with cervical SCI. The study showed that MEP recordings are sensitive to indicate motor tract lesions in approximately 90% of SCI patients, predictive for the recovery of upper and lower limb motor function, of similar prognostic value to clinical examination in the prediction of functional recovery, and applicable in combination with the ASIA protocol to follow the recovery of clinical motor functions in relation to that of descending motor tracts for impulse transmission. Following SCI, ascending (sensory) and descending (motor tract) fiber tracts of the white matter and neuronal structures of the grey matter (anterior horn cells) can be severed. Electrophysiologic techniques (SSEP, MEP, EMG) allow separate examination of these neuronal structures and assessment of the Table 4: Spearman Correlation Analysis of Outcome of Hand Function and Both Clinical (ASIA Scores) and Electrophysiologic (MEP) Examinations of Both Acute and Chronic SCI Patients ASIA Scores Patients Full Motor Upper Motor Light Touch Pin Prick MEP in ADM Chronic SCI (correlation coefficient) Acute SCI (correlation coefficient) Significance (p value)

4 84 FUNCTIONAL OUTCOME AFTER SCI, Curt Table 5: Spearman Correlation Analysis of Outcome of Ambulatory Capacity and Both Clinical (ASIA) and Electrophysiologic (MEP) Examinations of Both Acute and Chronic SCI Patients ASIA Scores MEP Recordings Patients Full Motor Lower Motor Light Touch Pin Prick Quad Tib Chronic SCI (correlation coefficient) Acute SCI (correlation coefficient) Significance (p value) extent of lesion. 4-6'~2 In comparison with clinical examination, electrophysiologic parameters are less influenced by the cooperation of the patient and can be quantified. Furthermore, electrophysiologic examinations are advantageous in monitoring the recovery of spinal cord (conductivity of ascending and descending fiber tracts) from injury. Transcranial magnetic stimulation allows an examination of the conductivity of the motor tracts following cortical or spinal lesions in humans. In patients with traumatic or nontraumatic cortical lesions, the presence of MEP is indicative of good recovery. However, the recovery of special motor functions in these disorders cannot be predicted by MEP recordingsj 3-~6 In nontraumatic lesions of the spinal cord, MEP latencies are usually prolonged and have a reduced amplitude. 17-2o Earlier studies have shown that MEP recordings in these disorders are not closely related to the extent of neurologic deficits] t-23 However, in some cases, they can be more sensitive in revealing spinal cord involvement in comparison with clinical examination alone. In line with earlier reports, our study shows that ASIA scores are significantly related to the recovery of hand function and ambulatory capacity in patients with acute SCI. 2'4'5 Furthermore, in agreement with other studies, ~4z7 our investigation demonstrates that, in both acute and chronic cervical SCI, MEP latencies and amplitudes are pathologically affected in approximately 90% of patients. The MEP of proximal (QF) and distal (TA) muscles of the lower limbs in tetraplegic patients are similarly affected. In contrast, in the upper limbs, the MEP of the proximal (BB) muscle are mainly unaffected compared with that of distal (ADM) muscle in 90% of patients. 4O 45 g35 == 3O A ~ 2tB 1.5 ~ " I I I I no therap, functional full healthy ambulatory capacity no, t therap, functional ambulatory capacity I I I full healthy Fig 1. MEP recordings in SCI patients are significantly related to the outcome of lower and upper limb function. In the anterior tibial muscle in the acute SCI patient group, (A) the MEP latencies in comparison with those in healthy subjects are prolonged or even abolished (in the patients with no ambulatory capacity), and (B) the MEP amplitudes increased with higher degree of ambulatory capacity. In contrast to the findings in nontraumatic spinal cord lesions, ~9'2 the MEP were closely related to the neurologic deficit and motor function (p <.0001). In no patient was a clinically relevant motor deficit (muscle paresis < 4/5) of the limbs associated with normal MEP values in the respective muscles. No MEP could be recorded in patients with a complete plegia of a limb muscle in the initial or follow-up examination in accordance with earlier studies. ~2'21'28 Therefore, MEP recordings in SCI patients are more sensitive than SSEP recordings for revealing the involvement of motor tract fibers. In some patients, especially those with complete paraplegia as a result of anterior cord syndrome, SSEP may even appear to be normal or only slightly affected] 9 The MEP in SCI patients were highly predictive (ADM and lower leg muscles) of the recovery of muscle function such as hand function and ambulatory capacity. All of the patients with elicitable MEP recordings in the initial examination recovered functional muscle activity of 3/5 or more of the respective muscles. This is in contrast to patients with cortical lesions, in whom even in completely or severely paralyzed muscles, normal MEP can be recorded. 3 '31 The MEP recordings were at least as sensitive as the ASIA protocol in predicting the resulting functional deficit. Therefore, the use of MEP recordings is appropriate in uncooperative patients (approximately 15% of patients with acute SCI) to select the appropriate therapy (occupational and physiotherapeutic approaches) ~32 ~30 ~ gl.2.~ 1.=. =0.8 ~.0.6 ~0.4 T A B healthy I I I I acute (initial) acute (6 chronic months) patients t t I I healthy acute (initial) acute (6 chronic.., months) parleel[~l Fig 2. in follow-up recordings in the anterior tibial muscle, neither the values of (A) MEP latencies nor of (B) MEP amplitudes revealed a significant change. The parameters of the acute SCI patients showed comparable values as the chronic SCI patient group.

5 FUNCTIONAL OUTCOME AFTER SCl, Curt 85 In accordance with previous studies, 32'33 there was an increase in the ASIA motor scores in patients with acute SCI, whereas the ASIA sensory scores did not change significantly. The significant increase of the motor score in the incomplete tetraplegic patients was not restricted to recovery of motor function in the zone of partial preservation (upper limbs) but was also evident in the leg muscles. However, there was no significant change in MEP parameters (latencies and amplitudes) of upper and lower limbs in follow-up examinations performed as many as 6 months posttrauma in acute SCI patients. Furthermore, comparison of the MEP values in the acute and chronic SCI patients revealed no significant difference between the groups. Therefore, there is no indication for a recovery of descending motor tracts for impulse transmission recordable by MEP recordings. This is in contrast to studies performed in patients with stroke in whom an improvement of both latencies and amplitudes could be demonstrated The latter results agree with recordings of SSEP in acute SCI patients, which also did not change significantly in the followup period. 4'5 The discrepancy between the increase in motor scores, connected with a recovery of function, and the unaltered electrophysiologic recordings following SCI may be due to the fact that electrophysiologic recordings do not reveal some types of spinal cord recovery Such a recovery and reorganization of spinal cord function below the level of the lesion has been described previously. ~ In these patients, total unilateral transection of descending motor tracts combined with 85% to 90% transection of the contralateral tracts led to total paralysis of the lower limbs. However, recovery occurred such that even walking was possible after 2 months. In addition, the increased values of the ASIA motor score may be explained by an improved dexterity or strength acquired during the course of physiotherapeutic and occupational therapy. CONCLUSION The findings of our study of MEP recordings are in accordance with those in earlier studies of SSEP recordings which indicate that there is restricted recovery of spinal cord impulse transmission following SCI. The MEP technique can contribute toward diagnosing lesions of different neurologic structures within the spinal cord and in predicting the recovery of functional movements. Furthermore, MEP recordings allow one to differentiate between the recovery of spinal motor tract fibers and the outcome of functional deficits. Acknowledgments: The authors thank Dr. I. Gibson for editorial services, E. Harsch for technical assistance, and Th. Erni (biostatistician) for statistical support. References 1. Curt A, Dietz V. 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