Somatosensory Evoked Potentials during Harrington ...

[Reprinted

from

THE JOURNAL Of BONE AND JOINT

Vol. 6O-A, No.4, Copyrighted

SURGERY

pp. 52l>-532. June 1978]

1978 by The Journal

of Bone and Joint Surgery,

Inc.

Printed in U.S.A.

Somatosensory Evoked Potentials during Harrington Instrumentation for Scoliosis' BY GORDON

L. ENGLER,

FRED DANZIGER,

M,D,!,

NEIL I. SPIELHOLZ,

M.D.t,

HENRY

MERKIN,

PH,D,t, B.A.t,

WILLIAM

N. BERNHARD,

AND TED WOLFF,

M,D·t,

E.E.t,

NEW YORK, N.Y. From the Departments of Orthopedic Surgery. Rehabilitation Medicine. and Anesthesiology. New York University Medical Center. New York City ABSTRACT: The somatosensory evoked potential can be obtained in the anesthetized patient during corrective surgery on the spine. The techniques of anesthesia and somatosensory evoked potential recordings described herein were utilized in fifty-five patients during surgical correction of scoliosis with Harrington instrumentation and spine fusion. No detectable complications were encountered and no neurological morbidity ensued in our series. This method may prove to be of significant value when potential injury to the spinal cord may be encountered during correction of spinal deformities.

Dawson probably was the first to describe changes in electrical potentials (somatosensory evoked potentials) that were recorded on the scalp following stimulation of peripheral nerves in the extremities. He determined that these changes in potentials were in fact cerebral action potentials arising in the central or post-central cerebral cortex. Based on his findings, tests for spinal cord function have been done in a variety of experimental and clinical situations. The prognostic significance of those potentials in cases of spinal cord injury was documented by Donaghy and Numoto in 1969. They concluded that the clinical recovery of motor function in animals was correlated with early recovery of the somatosensory evoked potentials. In their experiments, a weight was dropped on the dorsal surface of the spinal cord after laminectomy. Examination of the cord then revealed that a symmetrical lesion was not produced in all cases, and this may explain some discrepancies between recovery of the potentials and recovery of motor function in some of their animals. They provided good evidence to show, in a second series of animals, that the early recovery of the evoked potential is very well correlated with the recovery of motor function, and that the laterality of the recovery of motor function also is closely correlated with the laterality of the evoked potentials. They concluded that the recovery of the evoked potentials within four hours after injury indicated a good prognosis in their experimental animals, Failure to elicit such a response meant a poor prognosis. " Supported in part by NINCDS grant NS 10]64-04.

t 566 First Avenue. New York. N.Y. 10016. Please address reprint requests to Dr. Engler. 528

The technique has been studied further in laboratory animals :1 and it was shown that the size of the evoked response diminished when a weight was applied (not dropped) on the dorsal surface of the exposed spinal cord. If the weight remained for fifteen minutes, the evoked potential disappeared. When the weight was removed within two minutes, the evoked response usually returned within two minutes. It was presumed, therefore, that a vascular mechanism was mediating the change. Clinical use of the somatosensory evoked potentials gained strong impetus with the work of Perot in 1972, and his technique and findings served as the basis for much of the clinical application of the method. He was one of the first to suggest that somatosensory evoked potentials may be of significant use as a predictive tool for impending injury to the spinal cord during operations on or near the cord. Further work to demonstrate the use of the evoked potential was carried out by D'Angelo and associates in 1973. They showed that the evoked cortical response probably is due to impulses conducted in the ipsilateral posterior column and spinocervical tract (in the cat); the latter considered to be the feline equivalent of the spinothalamic tract in humans 1. Conduction therefore might be inhibited by mechanical distortion or disruption of the fibers, ischemia, hypoxia, or other neurochemical depression. They stated that with the technique only the integrity of the posterior columns can be ascertained, but not the factors that initiate the pathological spiral of changes following impact injuries to the spinal cord. Recently, Nash and associates 11-13 demonstrated the direct correlation between hypotension and a deterioration of the potentials. Their data supported the concept that a definite relationship exists between lowering the blood pressure along with compression of the cord and the diminution of spinal cord function. Monitoring of the findings in the spinal cord in two instances of unstable thoracic-spine compression fracture was described recentl y 14, and the improvement of the evoked responses correlated well with neurological recovery. We decided that the method might be valuable in the monitoring of function in the spinal cord in patients undergoing spine fusion for scoliosis with Harrington instrumentation, especially in those patients with severe scoliosis and neuromuscular disease, in whom the risk of THE JOURNAL

OF BONE AND JOlNT SURGERY

SOMATOSENSORY

EVOKED

POTENTIALS

DURING

complication of intraoperative injury to the cord is great because of the need for extensive correction of the curve.

Methods We studied fifty-five such patients with progressive scoliosis. Six patients had a complicating neuromuscular disorder such as myotonia dystrophica, Duchenne muscular dystrophy, neurofibromatosis, poliomyelitis, or spinal muscular atrophy. The remainder had idiopathic scoliosis and were neurologically normal. The potentials were recorded with a TECA TE-4 electromyograph equipped with an NS-6 nerve stimulator, AA-6 amplifier, and A VM averager (TECA Corp., White Plains, New York). Patients were studied preoperatively to be sure that somatosensory evoked potentials could be obtained by stimulating one or both lower extremities. The side giving the best response was used during surgery, while circling the positions of the recording scalp electrodes with ink preoperatively allowed us to reproduce the electrodes' positions during the operation. The superficial peroneal nerve and the posterior tibial nerve were stimulated simultaneously through the skin with two pairs of metal surface electrodes coated lightly with an electrolyte gel. To stimulate the superficial peroneal nerve, two strips, four centimeters long, were placed transversely across the anterior aspect of the ankle. One of these electrodes was taped just proximal to the lateral malleolus and the other, just distal to it. The posterior tibial nerve was stimulated with a plastic block fitted with two small circular metal discs (TECA Corp.) taped behind the medial malleolus so that the proximal disc was situated at about the proximal end of the tarsal tunnel. Both proximal electrodes were connected to the cathode of the stimulator and the distal electrodes, to the anode. The preoperative study was done with the patient awake. One stimulus lasting 0.05 to 0.1 millisecond was delivered per second and the intensity was then adjusted (usually between 100 and 150 volts) so that shocks were felt clearly but were not painful. In that way, electromyographic activity of facial muscles due to grimacing was avoided. The patient was instructed to look at the ceiling to avoid alpha electroencephalographic interference, and to relax the face, jaw, and neck muscles as much as possible. To reduce the time required for each run during the operation, the stimulation rate was increased to two to five per second and the intensity was increased to a maximum of 300 volts. The stimulator was turned off after each run. Bare platinum electroencephalogram-needle recording electrodes (Grass Corp., Quincy, Massachusetts) were used. The reference electrode was placed just posterior to the anterior hairline in line with the nasion and the active electrode, in the Pz position of the Ten-Twenty International Electroencephalogram System. This site corresponds to 70 per cent of the distance measured from the nasion to the inion in the mid-sagittal plane. A flat metal plate coated with an electrolyte gel was taped to the shoulder opposite the side being stimulated, for the ground VOL. 60-A, NO.4,

JUNE J 978

INSTRUMENTATION

FOR SCOLIOSIS

529

electrode. The recording electrodes were connected in such a way to the input of the preamplifier that an upward deflection indicated that the active electrode was positive to the reference. The amplifer gain was twenty microvolts per division, and the sampling time was 100 or 200 milliseconds. Two hundred consecutive responses were summated for each somatosensory evoked potential. For the preoperative evaluation, two to three potentials were recorded from each lower extremity, and another run was performed without stimulation to act as a control. During surgery, the potentials were monitored periodically to obtain values before the spine was subjected to distraction. After distraction, they were studied at two to five-minute intervals for about one hour. Anesthesia Until 1975, intravenous thiopental (three to five milligrams per kilogram of body weight), succinylcholine (one milligram per kilogram of body weight), and oxygen were used to induce anesthesia. Tracheal intubation was done using cuffed flexometallic or polyvinylchloride tubes. Anesthesia was maintained with 60 per cent nitrous oxide, oxygen, and 0.5 to 1.5 per cent halothane. A small dose of a long-acting muscle relaxant (d-tubocurarine or pancuronium) sometimes was administered at the start of surgery to produce immobility but the dose seldom was repeated. An alternative technique was to combine intravenous narcotics (approximately two milligrams per kilogram of body weight of meperidine or 0.005 milligram per kilogram of body weight of fentanyl) with 60 per cent nitrous oxide and oxygen and to administer a nondepolarizing muscle relaxant every forty-five to sixty minutes. All patients received mechanical ventilation with a tidal volume sufficient to keep the arterial Pc02 between thirty-five and forty torr (minute volume of ninety milliliters per kilogram of ideal body weight). To test the patient's ability to move the lower extremities, the following techniques of wake-up from anesthesia were used. 1. Nitrous oxide and halothane were discontinued and the patient received ventilation with 100 per cent oxygen. Thiopental (three milligrams per kilogram of body weight) was then used to reinduce anesthesia after a satisfactory response was obtained to the vocal command, "move your feet". 2. With the nitrous oxide, narcotic, and muscle relaxant sequence, first nitrous oxide was discontinued. If the patient failed to respond to the vocal command, the narcotic was partially reversed with intravenous naloxone (0.1 to 0.4 milligram). If the patient then appeared sufficiently awake but still seemed paralyzed, atropine (0.6 to one milligram) and neostigmine (0.5 to 1.5 milligrams) were administered to partially reverse the neuromuscular blockade. Partial reversal of the muscle relaxant then allowed voluntary motion on command and yet prevented sustained, violent movements. After satisfactory voluntary movement of the feet was demonstrated,

530

G. L. ENGLER

thiopental (three milligrams per kilogram of body weight) was used to reinduce anesthesia, followed by nitrous oxide and more narcotic. Recording of the somatosensory evoked potentials during anesthesia eliminated the need for arousal of the patient during the surgical procedure and allowed greater latitude in the selection of drugs for anesthesia. We now induce anesthesia with thiopental intravenously (three to five milligrams per kilogram of body weight) and oxygen. Endotracheal intubation, facilitated with succinylcholine (one milligram per kilogram of body weight) is done using tracheal tubes fitted with large-diameter large-residualvolume cuffs, and anesthesia is maintained with 60 per cent nitrous oxide and oxygen supplemented with meperidine (approximately two milligrams per kilogram of body weight) or fentanyl (0.005 milligram per kilogram of body weight). Pancuronium (initially 0.08 milligram per kilogram of body weight) or d-tubocurarine (initially 0.3 to 0.5 milligram per kilogram of body weight) is used to ensure immobility. Halothane and enfiurane are avoided because in our experience they interfere with the recording of evoked cortical potentials 2. The use of nitrous oxide, oxygen, narcotics, and non-depolarizing neuromuscular blocking agents allows the recording of somatosensory evoked potentials and avoids the hazards of wake-up from anesthesia during the operative procedure while the patient is in the prone position. But if evoked cortical potentials cannot be recorded, arousal as previously described can be accomplished, and the patient's ability to move the feet voluntarily can be tested. Results Our initial attempts to record intraoperative somatosensory evoked potentials were either unsuccessful or inconclusive. Considerable improvement in the method was obtained by: (1) eliminating halothane as an anesthetic

AND ASSOCIATES

agent; (2) substituting bare platinum electroencephalogram needles for Teflon-coated ones; and (3) performing preoperative studies with marking of the recording sites. Following the maneuver of spinal distraction but before the spine fusion was accomplished, twenty-three (42 per cent) of the fifty-five patients tested showed an increase in the amplitude of P I (Figs. 1 and 2). This increase ranged from 0.2 to 1. 5 microvolts to a twofold increase in the amplitude of the pre-distraction recording. Twenty-one (38 per cent) of the fifty-five patients showed a decrease of 0.2 to 1.3 microvolts in the amplitude of P, after the distraction was completed. The PI returned to the predistraction value within ten minutes in all cases. The other eleven patients (20 per cent) showed no change in PI amplitude after the distraction was begun. No clinical evidence of neurological deficit attributable to the surgery was detected. In thirty-eight (69 per cent) of the fifty-five patients a decrease was seen in the latency of P I after the institution of spinal distraction. This decrease ranged from a maximum of five milliseconds to a minimum of two milliseconds and persisted throughout the remainder of the surgical procedure. An increase in the latency of PI occurredin six patients (11 per cent) to a maximum of three milliseconds. a change in the latency occurred in the other eleven patients (20 per cent). Poorly defined potentials were obtained preoperatively in two patients (Fig. 3). Neither of these patients was able to tolerate stimulation of more than seventy- five volts when awake. During surgery, when stimulus intensity was increased, the potentials were elicited easily in both of them. In one adult patient with idiopathic scoliosis, the potentials could not be obtained either before or during surgery, but were obtained two weeks afterward. Discussion Unlike the technique of recording the action potentials directly from an exposed nerve, the somatosensory evoked potentials as recorded with scalp electrodes require

II)JV N2

(m

b)

I

I

100

200

see FIG.

Typical somatosensory evoked potentials. The first upward deflection (p[) usually appears between 33.0 and 36.0 milliseconds after the stimulus, while P2 usually appears at between 54.0 and 58.0 milliseconds. The amplitude varies with the stimulation voltage and level of anesthesia. In this tracing, P, was approximately 1.0 microvolt and occurred at 34.5 milliseconds, while P, was approximately 0.8 microvolt and occurred at 56.5 milliseconds.

(rn sec ) FIG.

200 2

Intraoperative potentials obtained before the Harrington rod was inserted (a) and after distraction (b). Note the increase in amplitude and decrease in latency after distraction.

THE JOURNAL

OF BONE AND JOlNT SURGERY

SOMA TOSENSOR Y EVOKED

POTENTIALS

DURING

special averaging or summating techniques because of marked attenuation of the potentials between their origin and the recording electrode. High preamplifier gains are necessary even though they introduce so-called noise into the record. Major sources of noise that interfere with successful recordings are electroencephalographic, electromyographic, and thermal (that generated by the instrument itself) . Averaging techniques allow one to extract a signal that is buried in noise, and are successful only when the noise is both truly random and not infinitely larger than the signal. Very large potentials, such as those coming from muscle, are difficult to average out. For this reason, it is vital during the preoperative study for the patient to remain as relaxed as possible, especially as regards the muscles of the face, jaw, and neck. Swallowing or blinking during a run may suddenly introduce a large, spurious potential. Each run therefore must be observed carefully to determine if the signal of interest shows a gradual increase on the averaged trace (Figs. I, 2, and 3). If a relatively large potential appears suddenly, coincident with a burst on the control channel, it must be ignored. On occasion, the averaged trace has to be erased and the run re-started. Since the somatosensory evoked potential is an averaged response, it is not surprising to find that it shows slight variations in configuration and latency from trial to trial in anyone subject. Intersubject variations may be even more conspicuous (Fig. 4). Some anesthetic agents have an effect on the potentials 2. In our experience, halothane seriously interfered with the recording of evoked potentials, and even with the agents we use now (nitrous oxide, narcotics, and relaxants) the amplitude may be markedly decreased compared with the awake response. Fortunately, stimuli of higher intensity can be used in the anesthetized patient to bring out recordable responses (Fig. 3). The potentials we have described, elicited in all but one patient preoperatively and intraoperatively, seem to have promise for use as a monitoring indication of whether the spinal cord has retained its functional continuity. We do not have any explanation of the one exceptional case

a)

IlflV

b)

200

( m see) FIG

3

n, Preoperative potentials from a patient who could not tolerate more than seventy-five volts of stimulation. The potentials appear to be present, but are of very low amplitude. b, Intraoperative potentials from the same patient using 300 volts of stimulation (made possible by anesthesia).

VOL. 60-A, NO.4,

JUNE 1978

531

INSTRUMENT ATION FOR SCOLIOSIS

mentioned previously except possible technical error; that patient had a normal test two weeks after operation. It should be emphasized that in none of our fifty-five patients did postoperative signs develop of neurological deficit ascribable to the spinal distraction and fusion, so that the test circumstances did not offer any instance in which an actual injury could have been monitored. Additionally, it may well be asked whether the continued presence of the potentials can guarantee that the spinal cord escaped injury during the operation. This false-negative result could occur if a lesion was engendered that: (1) spared only the fiber tracts that convey the potentials, or (2) might ultimately affect those tracts, but did not do so within the time that the patient was monitored in the operating room. More information therefore is needed concerning the physiology of the evoked potentials, especially as regards their anatomical conduction path, and the mechanisms of the

f

a)

l

200

( m see)

I')-LV 200

( m see) FIG.

4

Preoperative potentials from two different patients (a and b) showing the variability in general configuration. One pattern usually is reproducible in the same patient. Most subjects have an initial positive deflection as in a but occasionally an initial negative deflection is found, as in b.

changes in the potentials during manipulation of the spine. We especially need to know how ischemia and other potential operative hazards may infiuence these evoked potentials. Because the pathological lesion of the paraplegia that may occur as a complication during spine fusion has not been identified yet, the technique described may offer a method of study applicable to that lesion. Vascular embarrassment of the spinal cord is one possible cause of a neurological deficit following spine fusion 10. The arteria radiculomedullaris magna (artery of Adarnkiewicz) has been implicated. If it is true that this feeder of the anterior spinal artery supplies only the anterior part of the cord, the somatosensory evoked potentials would not be affected by disruption of that artery because the potentials are carried primarily in the posterior columns (the fasciculus gracilis) when the lower extremity is used as the site for stimulation. Some investigators 8, however, reported that selective occlusion of this artery is

532

G. L. ENGLER AND ASSOCIATES

not necessarily disastrous to the continuity of spinal cord function. If the anterior spinal artery itself is (reversibly) occluded distal to the entrance of the artery of Adamkiewicz, almost all of the transverse diameter of the cord will be infarcted 7; in this situation it might be apparent, by sudden loss of the potentials, that the occlusion should be relieved if possible. In the studies of experimental trauma of the spinal cord produced by dropping a weight on the exposed dura, it was shown that the potential disappears within a minute of the moment of impact 4. However, that type of trauma is not comparable to ischemia and it may not be safe to draw an analogy between experiments of that kind and clinical problems 9. An immediate loss of the potentials because of ischemia is unlikely 9, because in dogs the evoked potentials were recorded over the posterior columns for about twenty minutes after the cord had been rendered totally ischemic. If these findings are applicable to humans, the monitoring would have to be continued for a long time after the distraction was completed for the test to be of practical value. In our study, no patient lost the ability to show somatosensory evoked potentials during surgery and no neurological complications appeared postoperatively. Some patients (38 per cent), however, did show a transient drop in amplitude of potentials. This change may have in-

dicated a mild, reversible alteration of blood flow to the posterior columns. On the other hand, some patients (42 per cent) demonstrated an improvement in the amplitude of potentials shortly after distraction was begun (Fig. 2), and they also showed a decreased latency. If these improvements were real (that is, not artefacts of the technique), they suggest that straightening of the spine may result in more than just skeletal correction. Larger -caliber fibers or a greater number of fibers may transmit the stimulation after correction of the deformity. At present, the only alternative way to monitor the spinal cord is the so-called wake-up test. Vauzelle and associates reported on its use in 124 patients, and in that series no untoward complications were encountered. We have used it successfully also. But there are a number of possible hazards involved in arousing an intubated patient from anesthesia, with the patient lying prone on a convex frame. 1. Raising the head may cause accidental extubation which could be disastrous with the patient prone. Reintubation of a patient in this posture is quite difficult. 2. A sudden, deep inhalation during arousal possibly could lead to aspiration of air into the open vessels in the wound and to pulmonary aeroembolism. 3. A violent movement could dislodge the Harrington rod or fracture the lamina, or dislodge intravenous tubes.

References

1

l

1. CARPENTER, M. B.: Human Neuroanatomy. Ed. 7, pp. 248-249. Baltimore, Williams and Wilkins, 1976. 2. CLARK, D. L., and ROSNER. B. S.: Neurophysiologic Effects of General Anesthetics: 1. The Electroencephalogram and Sensory Evoked Responses in Man. Anesthesiology, 38: 564-582, 1973. 3. CROFT, T. J.; BRODKEY,J. S.; and NULSEN, F. E.: Reversible Spinal Cord Trauma: A Model for Electrical Monitoring of Spinal Cord Function. J. Neurosurg., 36: 402-406, 1972. 4. D'ANGELO, C. M.; VANGILDER, J. C.; and TAUB, ARTHUR: Evoked Cortical Potentials in Experimental Spinal Cord Trauma. J. Neurosurg., 38: 332-336, 1973. 5. DAWSON, G. D .. Cerebral Responses to Electrical Stimulation of Peripheral Nerve in Man. J. Neurol ., Neurosurg. and Psychiat., 10: 137-140, 1947. 6. DONAGHY, R. M., and NUMOTO, M.: Prognostic Significance of Sensory Evoked Potential in Spinal Cord Injury. Presented at the Seventeenth Spmal Cord Injury Conference, Veterans Administration Hospital. Bronx, New York. September 1969. 7. FRIED, L. C., and APARICIO, OSCAR: Experimental Ischemia of the Spinal Cord. Histologic Studies after Anterior Spinal Artery Occlusion. Neurology, 23: 289-293, 1973. 8. FRIED, L. C.; DI CHIRO, GIOVANNI; and DOPPMAN, J. L.: Ligation of Major Thoraco-Lumbar Spinal Cord Arteries in Monkeys. J. Neurosurg., 31: 608-614. 1969. 9. GELFAN, SAMUEL, and TARLOV, 1. M.: Differential Vulnerability of Spinal Cord Structures to Anoxia. J. Neurophysiol., 18: 170· 188, 1955. 10. KElM, H. A., and Hn.AL, S. K.: Spinal Angiography in Scoliosis Patients. J. Bone and Joint Surg., 53-A: 904-912, July 1971. 11. NASH, C. L., JR.; BRODKEY, J. S.; and CROFT, T. J.: A Model for Electrical Monitoring of Spinal Cord Function in Scoliosis Patients Undergoing Correction. In Proceedings of the Scoliosis Research Society. J. Bone and Joint Surg., 54-A: 197-198, Jan. 1972. 12. NASH, C. L., JR.; SCHATZINGER,L.; and LORlG, R.: Intraoperative Monitoring of Spinal Cord Function during Scoliosis Spine Surgery. J. Bone and Joint Surg., 56-A: 1765, Dec. 1974. 13. NASH, C. L., JR.; LORIG, R. A.; SCHATZlNGER. L. A.; and BROWN, R. H.: Spinal Cord Moniwring During Operative Treatment of the Spine. Clin. Orthop., 126: 100-105, 1977. 14. NASH, C. L.; SCHATZINGER, L. A.; BROWN, R. H.; and BRODKEY.J.: The Unstable Thoracic Compression Fracture; Its Problems and the Use of Spinal Cord Monitoring in the Evaluation of Treatment. Spine, 2: 261-265, 1977. 15. PEROT. P. L.. JR.: The Clinical Use of Somatosensory Evoked Potentials in Spinal Cord Injury. Clin. Neurosurg .• 20: 367-381, 1972. 16. V AUZELLE. c.; STAGNARA.P.; and JOUVINROUX, P.: Functional Monitoring of Spinal Cord Activity During Spinal Surgery. Clin. Orthop .• 93: 173·178. 1973.

THE JOURNAL

OF BONE AND JOINT SURGERY