CASE REPORTS

Peripheral

Ischemia as a Complicating Factor During Somatosensory Evoked Potential Monitoring of Aortic Surgery

and Motor

Laverne D. Gugino, PhD, MD, Karl H. Kraus, DVM, Ritta Heino, MD, Linda S. Aglio, MD, W. Jay Levy, MD, Lawrence Cohn, MD, and Rosemarie Maddi, MD

T

HE incidence of paraplegia following aortic surgery is reported to vary between 2% and 25%.lm4 This reported incidence has made intraoperative spinal cord monitoring an area of interest.5-9 Two monitoring modalities, somatosensory evoked potentials (SEP) and motor evoked potentials (MEP), can detect ischemia of nervous system structures. Of these, the SEP, although controversial, is used most for both experimental and clinical monitoring of aortic aneurysm surgery.5-i0 The SEP monitors physiologic integrity of the peripheral nerve, from the site of stimulation to the cerebral cortex, via the dorsal columns of the spinal cord. The most sensitive area of the spinal cord to ischemia is the anterior horn area, as shown by the distribution of postoperative spinal cord injury.” Although some investigators have suggested that a steal of blood from the posterior to anterior spinal cord may occur during aortic cross-clamping, changes in SEPs will, at best, indirectly monitor ischemia of the motor areas1*J3 Hence, SEP monitoring has yielded low specificity and sensitivity to postoperative neurologic deficits in the absence of shunt or partial bypass use during these operations.r4J5 As suggested by McNulty et a1,r3 use of these operative adjuncts, however, does in part improve the predictive value of SEP monitoring for postoperative neurologic deficits. Recent investigations have used MEPs induced by electrical stimulation to monitor spinal cord function during aortic occlusion.16-ia Monitoring MEPs may be more sensitive than SEPs to spinal cord ischemia. Clinical examples using magnetic transcranially induced MEPs in humans during aortic aneurysm surgery have yet to be reported. An often neglected factor in spinal cord monitoring is that an insult to any part of the nervous system pathway that is monitored will result in a change in the evoked potentials.19 Ischemia to the peripheral nervous system is an important factor that must be addressed during future clinical investigations involving evoked potential monitoring of aortic aneurysm surgery. Two cases are presented, one in which SEPs alone and one in which both SEPs and MEPs were monitored during aortic surgery. Both cases demonstrate the importance of peripheral ischemia as a possible explanation for changes in SEPs and/or MEPs during aortic surgery. CASE REPORTS Case 1 A 67-year-old woman was scheduled for a thoracic aortic aneurysm repair. Preoperative angiography revealed an aortic Journal of Cardiothoracic and Vascular Anesthesia,

aneurysm, 6 cm in diameter, extending from just beyond the left subclavian artery to the diaphragm. Without premeditation, anesthesia was induced with fentanyl, 4 mg, midazolam, 2 mg, and pancuronium, 10 mg. Anesthetic maintenance included a fentanyl infusion (5 ugikgihr), isoflurane (end-tidal concentration of 0.5%), oxygen, and pancuronium. Nitroglycerin, nitroprusside, esmolol, and phenylephrine infusions were used for hemodynamic control during the operation. Hemodynamic monitoring included right radial and femoral arterial cannulation for blood pressure monitoring and a pulmonary artery catheter for following pulmonary artery pressures. Monitoring of SEPs was used for intraoperative spinal cord monitoring. Stimulating electrodes were placed over the right and left posterior tibia1 nerves at the ankle for detection of spinal cord and lower limb ischemia. Stimulation of the right median nerve at the wrist served as a control for nonsurgical influences on cortical SEPs. The median nerve was stimulated with 200 usec square wave pulses of 50 mA at a rate of 4.71 Hz. The tibia1 nerve stimuli intensity was 70 mA with pulse durations of 200 usecs at a rate of 4.71 Hz. The stimulating cathode was placed 3 cm proximal to the anode. The SEP scalp recording montage included Cz’-Fz for the posterior tibial-induced responses, and C3’-Fz for median nerve SEPs (lo-20 International Electrode System). A semiautomated four-channel evoked potential acquisition program (Sentry Program, Cadwell Laboratories, Kennewick, WA) was used for on-line collection and analysis of the SEPs from the lower limbs and right arm. All SEPs were initially filtered with analog filter band widths of 10 to 300 Hz. After anesthetic induction, baseline SEPs were gathered, which consisted of a grand average of 10 SEPs generated by 100 stimulus repetitions for each recording channel. The grand average allowed sufficient data for determination of optimum digital filter band widths using the “phase synchrony” method. 1o~2oThese digital filter band widths included 12.5 Hz to 226.5 Hz for the median SEP, 10.9 to 139.1 Hz for the left posterior trbial nerve SEP, and 10.0 to 157.8 Hz for the right posterior tibial-induced SEP. A mean and standard deviation were also determined for latency and amplitude of the N19 peak for the median and P40 troughs for the posterior tibia1 nerve SEPs. The evoked potential acquisition program was then allowed to cycle through the three recording channels. During each cycle, a peak detection system automatically analyzed the detected waveform component of interest for latency

From the Departments ofAnesthesia and Cardiac Surgery, Brigham and Women S Hospital, Boston, MA, and the Department of Neurosurgery, Cleveland Clinic Florida, Ft. Lauderdale, FL. Reprints are not available. Comright 0 1992 by W.B. Saunders Company 1053-0770/92/0606-0015$03.00/0 Key words: aortic surgery, motor evoked potentials, somatosensory evoked potentials

Vol6, No 6 (December), 1992: pp 715-719

715

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GUGINO ET AL

closed, the SEPs improved as the peripheral pulses returned. At this point. palpable pulses, however, remained absent below the popliteal fossa. The SEPs continued to improve as serial physical and Doppler examinations led to the conclusion that the patient had embolized to her lower extremities. The patient then underwent bilateral embolectomies during which segments of fresh. platelet-rich clot and atheroma were extracted from the junction of the tibial-peroneal vessels. Blood flow was restored to both distal limbs. Of interest, the SEPs returned to baseline values at the point in time that palpable popliteal pulses returned. Postoperatively. the patient was found to be neurologically normal and was

and amplitude changes, expressed as a change in latency and amplitude values from the baseline SEPs in standard deviation units, and/or millisecond change in latency and percent change in amplitude. A warning system was set to alarm when a latency or amplitude change of more than four standard deviations from baseline means occurred. Figure 1 depicts, in trajectory format, changes in SEP latency and amplitude for the entire operation. The stability of all SEPs for the second one-half hour before the cross-clamp period is noted. Five minutes after clamping the aorta, the posterior tibial-induced SEP latencies increased and amplitudes decreased by more than four standard deviations. The SEP responses were never completely attenuated during the 2%minute cross-clamp period. During this period, the mean femoral artery pressures were noted to decline to 11 mmHg. On reperfusion, the latency and amplitude changes returned to within 3 standard deviations in a period of 25 minutes following a return of mean femoral artery pressure to 60 mmHg or greater. After 1 hour of reperfusion, however, the posterior tibia1 SEP latencies again became prolonged with concomitant amplitude attenuation. The median nerve SEPs remained normal during this period. The femoral artery catheter had been removed prior to this event and, therefore, lower limb perfusion pressures were unavailable. This late prolongation of the lower limb SEPs peaked at 15 minutes. At this time, palpation of the femoral arteries bilaterally revealed absent pulses. As the skin was

discharged

on the ninth postoperative

day.

Case 2 An l&year-old man was operated on for coarctation of the aorta. which was surgically corrected 12 years earlier. Angiographic examination had demonstrated two areas of constriction in the thoracic descending aorta. Doppler echocardiography demonstrated a pressure gradient of 40 mmHg across the first constriction. The patient was premeditated with fentanyl and midazolam and induced with sufentanil (10 pgikg) and etomidate (0.5 mgikg), plus atracurium for intubation. Anesthetic maintenance included

STIM: L Post Tib Nerve; Record: SEPcx

STIM: R Post Tib Nerve; Record: SEPcx

STlM: R Median Nerve; Record: SEPcx

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Fig 1. Trajectories representing changes in cortical SEP (SEPcx) amplitudes and latency during Case 1. Boxes to the left of the figure show the postinduction baseline SEP responses resulting from stimulation of the left posterior tibia1 nerve (top), right posterior tibia1 nerve (middle). and right median nerve (bottom). The parallel vertical lines superimposed on the first SEP peaks represent 99% confidence limits for latency. The figurine below the SEP baselines depicts stimulation and recording sites used during Case 1. To the right of each baseline SEP is the trajectory for each monitored response. Changes in amplitude, expressed as percent change from baseline, are depicted by dashed lines. Latency change [solid lines) is expressed as milliseconds change from baseline monitored peak for each response. Critical events are lebelled on the elapsed time line beneath the trajectories. Negative voltage deflection is up for baseline responses. Ampliide calibration is located to the left at each baseline.

PERIPHERAL ISCHEMIA

AND EVOKED POTENTIALS

AWAKE

717

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3..LJqq Fig 2. Trajectories for right cortical SEPs and right anterior tibia1 CMAPs monitored during Case 2. The format for these trajectories is the same as for Fig 1, except that both awake and anesthetized cortical SEP responses elicited from stimulation of the right posterior tibia1 nerve are shown to the left of the trajectory. The CMAP baseline was obtained after induction. The dotted lines on the lower trajectories represent the initial period of the case prior to motor response monitoring. For clarity, only the trajectories showing right anterior tibialis CMAPs and posterior tibia1 nerve elicited cortical SEPs are shown. The left side CMAP and SEP changes were similar. Negative is up for CMAP baseline and down for SEP baseline.

STIM: R Post Tib Nerve; Record: SEPo

-----

LATENCY (change from &selins in meet) AMPLlTUDE (% change from gaseline)

LA’sss maec AYP 4ss.s “V STIM: Transcranial Magnetic; Record R CYAP lntrrs us

infusions of etomidate (0.8 mglkgihr), sufentanil (2 pgikgihr), and atracurium (0.3 to 0.5 mgikglhr) with oxygen. A Datex Relaxograph (Datex Instrumentation Corporation, Helsinki, Finland) was used for monitoring the degree of atracurium-induced muscle relaxation, which was maintained at a 50% to 60% block level. Spinal cord monitoring consisted of both somatosensory and motor evoked potentials. SEPs were monitored with stimulation of both left and right tibia1 nerves at the ankle. Square wave pulses of 100 ksec at 75 mA with a repetition rate of 3.71 Hz were used. The evoked potentials were recovered with scalp electrodes placed at Cz and Pz for both limbs. Analog filters were set with a lower limit of 10 Hz and an upper limit of 300 Hz. One hundred repetitive stimulations constituted a single average. Optimal digital bandwidths of 10 to 110 Hz were used for both posterior tibia1 nerve elicited cortical responses. Motor evoked potentials were elicited by transcranial magnetic stimulation. A Cadwell MES-10 magnetic stimulator (Cadwell Laboratories, Kennewick, WA) was used as the power source, and a specially designed cap with a magnetic coil built in was used as the stimulator. The cap was fixed to the patient’s head so that the posterior aspect of the coil was positioned over the precentral gyrus. The intensity of the magnetic stimulator was set at 80% of the maximal intensity allowed by the power source. This configuration was found by previous experience to allow for consistent magnetic stimulation with minimal magnetic cap position-related variation. The induced evoked potentials were recovered as bilateral compound muscle action potentials (CMAPs) from surface electrodes. The active electrodes were placed on the motor point of the anterior tibialis muscles, with the reference placed over the proximal insertion tendons. Analog filters for the recovered waveforms were set at a lower limit of 10 Hz and an upper limit of 10,000 Hz. Bilateral CMAPs were elicited by single transcranial magnetic stimuli. The digital filter bandwidth was set at 10 Hz to 1,000 Hz. The same automated evoked potential monitoring program that was used in Case 1 was used in this case. The automated program only allows four recording channels to be used; therefore, median nerve SEPs were not included. The monitoring program was

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allowed

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After a stable plane of anesthesia

surgical

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for

through

10 consecutive

the

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averages

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recordings.

the collected

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for MEPs were averaged

channels

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or latencies

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The evoked potential amplitudes and latency changes obtained from right posterior tibia1 stimulation and anterior tibialis CMAPs are depicted

in Fig 2. Although

left side, they were omitted of the coarctation complete performed.

5-minute After

similar changes

for purposes

sites at 3 hours test occlusion 3 minutes,

latencies

changed

45 minutes

into the surgery,

of the descending

MEPs were reduced

than 1% of original amplitudes) recovered from the left anterior waveform

were noted for the

of clarity. After exposure aorta

a

was

to 50 FV (less

on the right and could not be tibia1 muscle. The right MEP

by 2 usec (98% of original

latency).

Neither latency nor amplitudes of SEPs changed. The test clamps were then removed and the MEPs returned to 50% of the original amplitudes after 10 minutes. Based on the MEP amplitude reduction during the test clamp period, the surgeons elected to repair the coarctation with placement of a polytetrafluoro-ethylene bypass graft (Goretex, Inc, Houston, TX) across the constricted areas. At 3 hours and 20 minutes into the surgery, tangential aortic occlusion

clamps

were

placed

on the

aorta

to allow

for

the

placement of the implant and to allow partial aortic blood flow. At this time the mean femoral artery pressure dropped to 50 mmHg. During this time the amplitude of the MEPs remained lower than preocclusion values, though MEP latency and SEP waveforms remained unchanged. After the partial occlusion clamps were released and until the end of the surgery, the MEP amplitudes steadily increased. The patient recovered uneventfully without neurologic deficits.

718

GUGINO ET AL

DISCUSSION Any change in the physiologic status of the entire neurologic pathway being monitored will affect the recovered waveforms in evoked potential monitoring. This includes not only the central nervous system, but also the peripheral nerves and, in the case of MEPs, the myoneural junction. Research and clinical case reports have concentrated on the effects of aortic occlusion on SEPs with regard to the spinal cord.5-10Js-15 However, peripheral nerve ischemia may also contribute to the evoked potential changes. Both reported cases can be classified as Type I changes.” However, peripheral loss of conduction cannot be ruled out with the recording montage used. Grossi et al*’ studied the time course of peripheral and central SEP conduction failure of Type I changes during aortic cross-clamping. Stimulating electrodes were placed on the posterior tibia1 nerves as well as overlying the lower lumbar spinal cord in the epidural space. SEPs were recorded from the scalp. After aortic occlusion, they noted the cortical SEPs induced from peripheral stimulation failed before those obtained from epidural spinal cord stimulation. This suggested that peripheral nerve was more susceptible to ischemia than the spinal cord. It is known, however, that peripheral nerve is rather robust with respect to conduction of electrically induced action potentials. For example, WangZ2 has demonstrated that myelinated axons conduct action potentials up to 30 days after removal from the body as long as they were kept cold and in a balanced salt solution. Heinbecker et al*” have shown human peripheral nerves to conduct for several hours after removal from human legs. Because the SEPs are known to conduct over a continuous axonal pathway from the peripheral nerve to the dorsal column nuclei (rostra1 spinal cord), it is of interest to resolve these seemingly disparate results. If it is assumed that the periphery is cooler than the central nervous system during anesthesia, then it is reasonable that peripheral nerves are at a lower temperature than the spinal cord. Franz and Iggo24 have demonstrated lowered temperature to adversely affect myelinated axons. Because SEPs are conducted over peripheral myelinated axonal pathways from the site of stimulation to the caudal spinal cord, it is possible that during ischemia, and in the presence of a lower temperature, that the numerous nodes of Ranvier would experience conduction failure prior to conduction in the spinal cord. However, Stoneyz5 has demonstrated that conduction along the periphery has its lowest safety factor threshold at the dorsal root ganglia where action potentials travel both up into the dorsal ganglia soma and then down the axon to the spinal cord roots. Safety factor is defined as the ratio of local axonal current available during conduction to the local current necessary for exciting the next node of Ranvier. Thus, with Lassinger et al’s’” results, a combination of peripheral nerve temperature and dorsal ganglia low safety factor for conduction could explain the loss of peripheral conduction during aortic occlusion-induced ischemia occurring prior to central spinal cord conduction failure. With respect to failure of descending motor pathways during spinal cord ischemia, Owen et ali7 have demon-

strated a loss of conduction in a distal-to-proximal direction. They used transspinal stimulation in order to monitor descending motor pathway functional integrity during aortic occlusion in dogs. Stimulating electrodes were placed in the disk space adjacent to the left innominate artery with recordings made at the mid and low spinal cord as well as sciatic nerve. They showed that there was a distal to proximal loss of descending motor activity with aortic occlusion. This was explained as a gradient of distal to proximal ischemia. This sequence of loss mirrored the spatial order of sensory potential loss. Transspinal stimulation, however, as a means of eliciting pure descending motor path activity, is still controversial. It is possible that sensory fibers were stimulated antidromically down the spinal cord, where they could activate spinal cord segmental reflex neuronal circuits. Whether anterior horn cells are stimulated by descending motor fibers or by antidromic stimulation of sensory fibers, both pathways involve synaptic transmission through the grey matter. Konrad et alZh found similar results using direct electrical stimulation of the motor cortex in dogs. Global ischemia was produced by ventricular fibrillation. Again, peripheral responses were lost prior to spinal cord descending activity. Kraus et a1,i8 using transcranial electrical stimulation of the brain in an aortic occlusion model, also found similar results. It is the spinal cord grey matter that includes synaptically activated anterior horn cells, which are the most sensitive to ischemia, not peripheral nervesi Peripheral nerve rcsponses, which result from synaptically activated anterior horn cells (grey matter), would be expected to be lost prior to spinal cord descending motor pathway activity. Therefore, loss of peripheral motor responses prior to spinal cord descending motor activity is readily explained. In the second case reported, transcranial magnetic stimulation was used and recorded from peripheral muscles to assure that pure motor pathways were monitored. Of interest was the rapidity of motor CMAP loss over 5 minutes with no change in cortical SEPs. This loss was of amplitude rather than a prolongation of latency. Owen ct al,” using transspinal electrical stimulation, showed a similar amplitude attenuation of peripheral motor axonal responses, which were more pronounced than latency prolongation. Kraus et al,lx using transcranial electrical stimulation to produce MEPs in dogs, also showed that amplitudes of peripherally recorded MEPs were dramatically attenuated within the first 5 minutes of aortic occlusion without significant prolongation of latencies. Thus, early in ischemia, loss of anterior horn cell excitation would result in fewer anterior horn cell firings and rapid attenuation of amplitude measured in peripheral motor axons (peripheral nerve). Because conduction in axons is more robust during initial phases of ischemia, latencies would be expected to be less severely affected. The loss of SEPs in Case 1 may demonstrate dorsal root ganglion or distal peripheral nerve ischemia as the cause for

PERIPHERAL ISCHEMIA

719

AND EVOKED POTENTIALS

loss of SEPs. If the emboli to the femoral arteries had occurred during or soon after release of aortic crossclamping, the SEP changes may have been attributed to spinal cord, and not more distal nervous system structures. Stimulation of a peripheral nerve and recording from the cauda equina could have differentiated spinal cord and more distal nervous system structure ischemia. The loss of MEPs in Case 2 may reflect ischemia to the spinal cord descending fibers, grey matter of the spinal cord (including anterior horn cells), peripheral nerve, or the myoneural junction. Although the decision to use a conduit (ie, use of a bypass graft) was in part the result of sudden MEP attenuation with aortic test clamping, the etiology of the rapid change in MEPs is unknown because it may reflect ischemia of the spinal cord grey matter, peripheral nerve, or myoneural junction. Because the MEPs demon-

strated a sudden drop in amplitude without a significant latency change, it is possible that nerve impulses were adequately conducted to the anterior grey matter and peripherally to the myoneural junction. Initial ischemia may have affected synaptic excitation either at the spinal cord grey matter or peripherally at the myoneural junction. Again, peripheral ischemia and not critical spinal cord ischemia may account for the evoked potential changes. Stimulation of a leg nerve with recording from appropriately innervated muscles could have ruled out this possibility. Now that spinal cord motor system monitoring is becoming a reality, steps should be taken to localize the change that this monitoring depicts. Techniques should be used in both research and clinical monitoring, which will assess both the central as well as peripheral nerve structures.

REFERENCES

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