GILDENBERG PL: Treatment of spasmodic torticollis by dorsal column stimulation. Proc 7th Symp World Soc. Stereotactic and Functional Neurosurgery, Sao ...
Int Rehab Med 1980, 2, 82-85 © EULAR PUBLISHERS Basle
SPINAL CORD STIMULATION
Neurophysiological evaluation of chronic spinal cord stimulation in patients with upper motor neuron disorders M. R. Dimitnjevic, M. M. Dimnnyevic, A. M. Sherwood, and J. Faganel The Institute for Rehabilitation and Research, Texas Medical Centre, Houston, and the Institute of Clinical Neurophysiology, University of Ljubljana School of Medicine, Ljubljana
Summary Spinal cord stimulation was found to be an effective method for improving motor performance in patients with upper motor neuron disorders. Electromyographic analysis of segmental and suprasegmental activity was performed in 11 patients who had used spinal cord stimulation for more than 12 months. Neurophysiological analysis of electromyographic findings revealed improvement of volitional motor control and a reduction of spasticity in the examined muscles of the lower limbs in all patients. Keywords Neurophysiology — Spinal cord stimulation — Upper motor neuron disorders
Introduction Cook, Dooley, Illis, and their co-workers reported independently on the effectiveness of spinal cord stimulation (SCS) for modification of motor control in patients with upper motor neuron disorders (1-3). Later, they published similar results obtained from a larger number of patients (4-6). Numerous other groups were able to repeat these observations (7-13), but Young and Goodman (14) and Rosen and Barsoum (15) reported failure to repeat the results of the others. It would seem this discrepancy was in the use of the quantitative techniques for measurement of benefit of SCS (16-17) for evaluation of physiological mechanisms of neural control. On the other hand, those authors who used measurements of physiological parameters of bladder function or electrophysiological events correlated to spasticity or sensory 82
functions were able to report positive changes of these parameters occurring in relation to SCS (3, 6, 11). In a preliminary study of underlying neurophysiological changes related to SCS, somatosensory cortical-evoked potentials and spinal cord potentials of the lumbar cord did not reveal significant changes (18). Measurement of the amount of suppression of phasic reflexes during vibration, before and after SCS, was a useful method for detecting effects of SCS, yet it did not show obvious suppression due to a large variability of the amount of suppression within the 3 patients tested. On the other hand, electromyographic recording of activity in the leg and trunk muscles during testing of volitional movements, stretch, and cutaneomuscular reflexes showed more persistent changes related to spinal cord stimulation (18). Therefore, in this neurophysiological study, we applied electromyographic (EMG) analysis of volitional and reflex movements before and after SCS.
Patients Eleven patients (4 female and 7 male) were included in this study. Their age varied from 23 to 57 years. Six patients had multiple sclerosis, with moderate motor impairment, and were able to walk with support. Five patients had chronic spinal cord injury at the levels of C3 to T4; they were not functional walkers.
Method Polyelectromyographic evaluation was performed in all patients before SCS and up to 18 months after
DIMITRIJEVIC ET AL: NEUROPHYSIOLOGICAL EVALUATION OF SCS
they had been using SCS continuously. Before this study, bioengineering evaluation of the equipment and electrode placement was performed. During polyelectromyographic recording SCS was discontinued. The applied method, polyelectromyography (PEMG) is a simultaneous recording of muscle activity using surface electrodes over the patient's lower limbs and lower trunk muscles. Twelve pairs of Beckman recessed silver-silver chloride electrodes were placed over the muscle belly approximately 5 cm apart and connected to an ink jet recorder (Elema Schonander). In our study we recorded EMG activity from the following muscles: abdominal, paraspinal, quadriceps, adductors, hamstrings, tibialis anterior and triceps surae. A gain of 100 microvolts per division and a bandwidth of 7 to 700 Hz were used. The patients were placed in a comfortable, supine position on an examination table, and a standard protocol of maneuvers for activation of segmental reflexes and descending influences from the brain and brain stem was applied. We recorded voluntary relaxation, volitional movements in the lower limbs, and patterns of spasm activation using Jendrassik or related maneuvers. By mechanical stimulation of the skin over both lower limbs, we observed local responses and patterns of irradiation of elicited activity to the opposite limb. Finally, we recorded reflex responses to passive movements, muscle vibration, sudden sustained stretch, repetitive tendon taps, and noxious plantar stimuli. We analyzed the amount and distribution of the elicited EMG activity, and the consistency of responses after three repetitions of each maneuver.
Results After SCS all patients under this study reported improved motor control, diminished spasticity, and increased endurance. Simultaneous recording of muscle activity in abdominal, paraspinal, and lower Iimb muscles revealed significantly different patterns of activity before spinal cord stimulation and after the system was implanted. Relaxation All patients were able to relax voluntarily before and after SCS. Voluntary induced activity Before SCS, patients with spinal cord injury were able to induce some voluntary activity in tested muscles; it was usually widespread, unselective, and bilateral. After SCS, the amount of voluntary induced activity did not increase, but attempts to voluntarily activate the examined muscles had a less widespread effect on distant muscle groups. In patients with multiple sclerosis who did not show
widespread activation on voluntary contraction, an improvement of reciprocal activation of antagonistic muscles was noted. Passively induced activity In spinal cord injured patients this maneuver induced long bilateral tonic bursts of activity, which got shorter and showed less irradiation after SCS (Fig. 1). In multiple sclerosis patients this test was within normal limits before and after SCS.
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Fig. 1. Polyelectromyographic recording of the response to passive knee flexion and extension before and after spinal cord stimulation. EMG bursts are shown as horizontal bars in which vertical value represents the relative amount of the elicited amplitude of EMG activity in the raw recording. The movements were performed at a standard slow rate of clinical maneuver for passive muscle stretch.
Clonus All patients with spinal cord injury and the majority of multiple sclerosis patients had sustained clonus before SCS. In 5 patients with multiple sclerosis, SCS decreased the duration of clonus and in one patient it was no longer elicitable. Vibration reflex In all examined spinal cord injured patients, vibration elicited long tonic bursts of activity with some irradiation and slow or absent habituation. After SCS, vibration elicited shorter responses which showed an increased tendency to habituation and less irradiation of activation of motor unit activity in non-vibrated muscle groups. In patients with multiple sclerosis vibration reflexes were close to normal before and after SCS. 83
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Segmental reflexes After spinal cord stimulation, segmental reflexes did not change except for the diminished irradiation in both spinal cord injured patients and those with multiple sclerosis. In a summary of the results, the most prominent feature in the PEMG recordings of various maneuvers were shorter tonic responses to passive stretch of the muscles, with less irradiation to other ipsilateral and contralateral muscles. There was also less irradiation of voluntary and reflexly induced motor activity in the tested muscles. We observed significantly decreased duration of dorms, which was usually sustained before the SCS. Vibratory induced tonic responses of the muscles were of shorter duration and habituated quicker than before SCS. There were no significant changes in the amount of voluntarily induced activity in patients where it had been poorly pronounced previous to treatment with SCS; however, attempts to voluntarily activate examined muscles had more locally organized activity after SCS than before.
suppressed excitability levels for segmental reflexes as well as for the effects of brain influence on segmental reflexes. Therefore, we were unable to demonstrate with this method any specific neural control mechanisms, but a generalized non-specific decrease of responsiveness of the nervous system to proprioceptive and exteroceptive stimuli. At the same time, we have reported a modest improvement of desired movement which can also be a result of diminished spasticity. It may be that suprasegmental mechanisms maintaining the abnormal segmental activity are modified during SCS. Finally, the results of PEMG recordings of reflex and voluntary activity, which showed improvement of voluntary control and reduction of spasticity in all 11 patients studied, can suggest that the effects of SCS lie in modification of the interaction of brain and segmental reflexes. This can possibly occur through improvement in the volitional and supraspinal control over segmental reflexes.
Discussion
Grant Support from: Bob and Vivian Smith Foundation, Houston, Texas The Rehabilitation and Research and Training Center No. 4 (Rehabilitation Services Administration Grant 16-P-56813/6).
Acknowledgement
In this study we have attempted to electromyographically record volitional control, segmental reflexes, and released phenomena in patients with motor impairments before and after SCS. PEMG analysis performed in 11 patients before and after SCS showed constant, repeatable, and definite changes after continuous SCS. Thus, PEMG studies are providing evidence of changes in motor control in all examined patients. The physiological mechanisms of the effect of SCS on modification of abnormal motor patterns is not fully understood. Although SCS primarily depolarized posterior columns, it has a definite motor effect. Some patients reported larger areas of normal sensation after SCS. However, the evaluation of sensory function by neurophysiological methods did not show significant changes in our preliminary studies (18). Some authors who have noticed beneficial clinical changes have also applied some neurophysiological methods for the evaluation of changes occurring in relation to SCS (3, 6, 11). They used cervical somatosensory evoked potentials, brain stem auditory evoked potentials, visual evoked potentials, contingent negative variation, and Hreflex studies. They were able to demonstrate that SCS modified the amplitude of some deflections of cervical somatosensory evoked potentials and latency of brain stem auditory evoked potentials, but did not change visual evoked potentials and contingent negative variation. Studies of H-reflex revealed temporary facilitation and restoration of inhibition of H-reflex by cutaneous stimulation which occurred during SCS. The general feature of our PEMG findings was 84
Zusammenfassung Die Rackenmarksstimulation erwies rich als eine wirksame Methode fiir die Verbesserung des motorischen Verhaltens von Patienten mit Lasionen des oberen motorischen Neurons. Bei 11 Patienten, welche die Riickenmarksstimulation wahrend mehr als 12 Monaten angewendet hatten, wurde eine elektromyografische Untersuchung der segmentalen und suprasegmentalen Aktivitat durchgefiihrt. Die neurophysiologische Analyse der EMG-Befunde ergab eine Verbesserung der willkiirlichen Muskelkontrolle und eine Verminderung der Spastizitat in den untersuchten Muskeln der unteren Extemitaten bei alien Patienten.
Résumé La stimulation medullaire s'est aver& constituer une methode efficace pour l'amelioration des fonctions motrices chez les malades porteurs de troubles des motoneurones superieurs. L'analyse electromyographique de l'activite segmentaire et supra-segmentaire a ete effecutee chez 11 malades ayant utilise la stimulation medullaire depuis plus de 12 mois. L'analyse neurophysiologique de ces resultats revele dans tous les cas une amelioration de la cornmande motrice volontaire et une diminution de la spasticite des muscles de la jambe etudies.
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12. DAVIS R, Fu ri ER MA, BOLTON D, KOMRAD M: Clinical efficacy and safety of chronic spinal stimulation used in multiple sclerosis and other demyelinating diseases. Advances in External Control of Human Extremities. Proc 6th International Symposium on External Control of Human Extremities Aug 28-Sept 1, 1978, Dubrovnik. Yugoslav Committee for Electronics and Automation, Belgrade, 1978, pp. 557-567. 13. WALTZ JM, KAILASH CP: Spinal cord stimulation in disorders of the motor system. Advances in External Control of Human Extremities. Proc 6th International Symposium on External Control of Human Extremities Aug 28-Sept 1, 1978, Dubrovnik. Yugoslav Committee for Electronics and Automation, Belgrade, 1978, pp. 545-556. 14. YOUNG RF, GOODMAN SJ: Dorsal spinal cord stimulation in the treatment of multiple sclerosis. Neurosurg 1979; 5 (2): 225-230. 15. ROSEN JA, BARSOUM AH: Failure of chronic dorsal column stimulation in multiple sclerosis. Ann Neurol 1979; 6: 66-67. 16. KURTZKE JF: On the evaluation of disability in multiple sclerosis. Neurol 1961; 11: 686. 17. TOURTELOTrE WW, HAERER AF, SIMPSON JF, KUZMA JW, SIKORSKI J: Quantitative clinical neurological testing. I. A study of a battery of tests designed to evaluate in part the neurological function of patients with multiple sclerosis and its use in a therapeutic trial. Ann NY Acad Sci 1965; 122: 480-505. 18. DIMITRIJEVIC MR, DIMITRIJEVIC MM, SHERWOOD AM, GREGORIC MR: Long term physiological effects of spinal cord stimulation. Advances in External Control of Human Extremities. Proceedings 6th International Symposium on External Control of Human Extremities, August 28September 1, 1978, Dubrovnik, Yugoslavia. Committee for Electronics and Automation, Belgrade, 1978, pp. 673-680.
Reprints from: M. R. Dimitrijevic, M.D. Department of Neurophysiology The Institute for Rehabilitation and Research Texas Medical Center Houston, Texas 77030 USA
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