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Monitoring spinal epidural potentials to peripheral nerve stimulation
Intraoperative Monitoring of Neural Function Handbook of Clinical Neurophysiology, Vol. 8 M.R. Nuwer (Ed.) # 2008 Elsevier B.V. All rights reserved
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CHAPTER 13
Monitoring spinal epidural potentials to peripheral nerve stimulation Steve Jones* Department of Clinical Neurophysiology, National Hospital for Neurology and Neurosurgery, London WC1N 3BG, UK
13.1. Background The first recordings of sensory evoked activity in the human spinal cord were made in the 1930s (Gasser and Graham, 1933). With only one or two intervening publications, it was not until the 1970s that a number of groups in Japan started to exploit the experimental and clinical possibilities of the “evoked spinal cord potentials” (e.g., Shimoji et al., 1972; Tsuyama et al., 1978). These studies involved inserting an electrode at the end of a flexible lead into the epidural space. When located at the appropriate level, the electrode was used to record localized “segmental” activity generated in the dorsal columns and dorsal horn, following stimulation of the dorsal roots or a nerve trunk in the upper or lower limb. It was the realization that an electrode at cervical level could be used to record “conducted” activity following stimulation of a nerve in the lower limb, or of the spinal cord at a lower level, that led to the exploitation of this technique in investigating and monitoring the integrity of long spinal cord tracts during surgery (Tamaki et al., 1981). In Japan, it was generally the surgeons themselves who were responsible for all aspects of the recording procedure. This, I believe, is the reason why the methodology most widely used in Japan today involves both stimulating and recording electrodes located in the dorsal epidural space. Elsewhere, the involvement of neurophysiologists, accustomed to methods of peripheral nerve stimulation used for the clinical application of somatosensory evoked potentials (SEPs), resulted in the importation of their *
Correspondence to: Steve Jones, Ph.D., Department of Clinical Neurophysiology, The National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK. Tel.: þ44-20-7837-3611, ext. 4109; fax: þ44-20-7713-7743. E-mail: [email protected] (S. Jones).
methods into the operating theater. The epidural SEP (ESEP) method appears to have been introduced concurrently and independently in the UK and Australia (Jones et al., 1982; Macon and Poletti, 1982). 13.2. Applicability In the UK, the ESEP method is used almost exclusively by orthopedic surgeons concerned with the treatment of spinal deformities, in particular kyphoscoliosis, occurring in adolescents and young adults. Most of the patients, therefore, are otherwise healthy and neurologically normal. A minority will have kyphoscoliosis of neurogenic origin; when associated with peripheral neuropathy or combined peripheral/central conditions such as Friedreich’s ataxia, the degeneration of large diameter peripheral sensory fibers may be so extensive that it is impossible to record a reliable ESEP. In these cases, cortical SEPs may sometimes be better preserved, but this is not necessarily to be relied upon. In cases of severe neuropathy, therefore, the Japanese method of recording evoked spinal cord potentials to stimulation of the spinal cord at a rostral or caudal level is probably the only one which can be resorted to. In Friedreich’s ataxia, the fact that the sensory pathways of the spinal cord, specifically the dorsal columns, are also affected may thwart even this technique. The fixation and instrumentation used for the correction of scoliosis (Harrington rods and compression/distraction systems attached via sublaminar wires or pedicle screws) are all applied from the dorsal side, so the initial placement of an electrode in the dorsal epidural space is straightforward. When the operation also involves treatment of lumbar kyphosis, it is clearly not possible to insert an electrode via the surgical field. However, a number of publications describe methods for inserting the electrode percutaneously in the anesthetic room (e.g., Anderson et al., 1990) which can also be exploited in other contexts.
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ESEPs are less frequently used for spinal cord monitoring during neurosurgical procedures. This is probably because the insertion of an electrode into the epidural space can be difficult or undesirable in patients with a narrow spinal canal (stenosis), or in whom the canal is otherwise distorted by tumor, subluxation (displacement of one vertebral body relative to the adjacent one), or fracture. When performed at multiple levels, ESEPs offer the opportunity of detecting not only the occurrence but also the level of conduction failure in the spinal cord. Multi-level recordings are not performed routinely, on account of the obstruction caused by the presence of leads in the surgical field, but additional electrodes can be rapidly inserted by the surgeon if and when a problem is identified. 13.3. Recording electrodes The recording electrode consists of a cylindrical sleeve of a chemically inert conducting material (stainless steel or platinum) whose diameter is the same as that of the lead whose end it forms. The diameter is usually around 1 mm and the length of the sleeve is around 3–5 mm. A second sleeve, at least 1 cm and no more than 5 cm along the same lead, may be used in conjunction with the first sleeve in order to obtain bipolar recordings. Alternatively, for monopolar recordings, a reference electrode (for example, a stainless steel needle) can be placed in the body tissue outside the surgical zone, as close as possible to the epidural electrode in order to avoid excessive pickup of extraneous noise. In most centers, disposable electrodes are now generally preferred to reusable types, but there is no reason, in principle, why an epidural electrode, properly constructed so there is no point of potential weakness or seepage between the conductive sleeve and the rest of the lead, should not be sterilized and used on multiple occasions. When under the control of the surgeon, the lead is introduced to the epidural space at the upper end of the surgical field, after exposure of the spine. It can be inserted directly when the dura is exposed by a laminectomy. Alternatively, the surgeon may choose to make a small hole in the interspinous ligament and insert the lead directly. A third option is to use the needle of a catheter of the appropriate diameter to pierce the interspinous ligament. The needle is then withdrawn leaving the catheter in place and the lead is introduced. Secured by a suture, the rest of the lead can then be
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routed out of the surgical field in the direction of the head. The natural angle of the dorsal processes means that the lead will be introduced aslant, the electrode tip pointing in the direction of the head. This is desirable, because on entry into the epidural space, it will then naturally tend to proceed in a cephalad direction. Obviously, recordings of evoked sensory activity need to be made from a level above any that are considered to be at risk during surgery. If the lead is introduced, for example, at the T1/2 level, there will usually be no obstruction to advancing the electrode to a low- or mid-cervical level comfortably above those segments of the cord that are likely to be at risk during surgery for kyphoscoliosis. Critical for the successful placement of the electrode, however, is the material of the lead. The advantage of making the lead as thin as possible is obvious, but if the conducting core and insulating sleeve are too flexible, this may result in unpredictable deviations as the lead is advanced. Small deviations from the midline are unimportant and probably inevitable, but clearly the surgeon needs to be confident that the lead is not so flexible that the tip finishes up altogether on one side of the cord or the other. In some centers, the surgeon or anesthetist will be confident to introduce the epidural electrode percutaneously in the anesthetic room, after induction of anesthesia (e.g., Anderson et al., 1990). This has the advantage that the ESEP technique can then be used to monitor operations performed from the anterior side of the spine. 13.4. Recording parameters The ESEP recorded at low cervical level to stimulation of the posterior tibial nerve at the level of the knee (popliteal fossa) has a latency of around 15 ms (depending, of course, on the age and height of the patient) and a duration of around 5–8 ms. It therefore demands a recording epoch (window) of at least 25 ms starting at the time of stimulus delivery. Most evoked potential (EP) recording machines today offer a wide range of epochs including 30 ms which is probably the ideal. There is usually no means of varying the digital sampling rate independently of the recording epoch. To obtain accurate representation of the briefest peaks in the response, a sampling rate of at least 10 kHz is desirable; with an epoch of 30 ms, this will almost certainly be comfortably exceeded.
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Since the ESEP largely comprises brief, polyphasic potentials rather than broad, slow waves, it is not necessary to amplify the signals over the full frequency range at the lower end of the spectrum. This is highly advantageous, since it means that mains-related noise frequencies of 50 or 60 Hz can be excluded by the use of a high-pass filter at 100 or even 200 Hz. In order faithfully to reproduce the high frequencies in the waveform, the low-pass filter needs to be set no lower than 2 kHz. The number of responses that need to be averaged in order to get an accurate measure of the signal depends on the level of background noise. Two hundred may be adequate in many circumstances, with the option of adding further responses to the average when noise levels are relatively high. 13.5. Bipolar versus monopolar recording The choice of monopolar (one epidural electrode referred to a needle or some other electrode alongside the spine) or bipolar epidural recording is probably best left to personal preference, since there seems to be an approximately equal weight of opinion on both sides. Monopolar recordings have the advantage that the individual components of the response can all be distinguished and are not confused with one another. This is perhaps of greatest value to neurophysiologists interested in exactly which tracts of the spinal cord are responsible for each component. Bipolar recordings are generally less noisy, because the close proximity of the two electrodes means that a larger proportion of the background noise is excluded by “common mode rejection.” In principle, it should be possible to construct a bipolar electrode pair in which the separation is chosen so as to maximize the amplitude of the response. For example, a typical ESEP waveform might consist of three negative and three positive peaks, the consecutive peaks of opposite polarity being about 0.5 ms apart. Their mean conduction velocity in the spinal cord is in the order of 60 m/s; so, in 0.5 ms, the waveform would travel approximately 3 cm. In theory, then, a 3-cm separation between the two electrodes should result in the largest recorded amplitude, since a peak of negativity recorded by one electrode would be amplified relative to a peak of positivity recorded by the other. Having the electrode separation less than 3 cm (as is usually the case) will undoubtedly reduce the amplitude of the response, but the components of the waveform should still be distinguishable and the
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background noise should be less. Separations of more than 3 cm should result in the waveform becoming more polyphasic, which is probably not desirable, and noisier. 13.6. Stimulating electrodes Many types of stimulating electrodes have been used for SEP studies outside the operating theater, but most are unsuitable for intraoperative use. In particular, stimulating electrodes that need to be moistened with water or saline may be prone to drying out during a long procedure. The use of straps around the limb is also strongly advised against, since this might cause constriction of the blood circulation. Stick-on type electrocardiographic (ECG) electrodes have the advantage that their contact area of gel is largely protected from evaporation. They can be effectively used to stimulate virtually any peripheral nerve that does not run too deep in the limb muscles, without the use of elastic straps. Needle electrodes should be equally effective, although they should only be inserted when the patient is finally positioned for surgery and removed if repositioning is necessary. 13.7. Stimulation sites The largest lower limb nerve running close enough to the surface to be easily stimulated transcutaneously is the posterior tibial nerve at the level of the popliteal fossa. The best way of discovering the most effective site for locating the stimulating cathode is to try it on oneself. The posterior tibial nerve contains the majority of large diameter (therefore, fast-conducting and with a low threshold for electrical excitation) group II cutaneous sensory fibers deriving from the sole of the foot, where the density of innervation is probably higher than elsewhere in the limb. It also contains large diameter proprioceptive fibers (group I muscle spindle and Golgi tendon organ afferents) from muscles responsible for flexion of the foot and the toes. The general experience is that this is the best nerve to stimulate for intraoperative monitoring of ESEPs. Cortical SEPs, however, are usually better produced by stimulation of the posterior tibial nerve at the level of the ankle. The reason for this is unclear, but it may be related to inhibitory interaction at cortical or subcortical level between the cutaneous projection and the muscle afferents projecting to different regions of the cortex. ESEPs can be recorded to stimulation of other nerves in the leg,
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but generally it is only the posterior tibial nerve at the popliteal fossa that gives rise to the large amplitude, fast-conducted responses which are most easily measured. In the literature it is often advised that the stimulating cathode for SEP recordings be placed proximal to the anode, in order to avoid “anodic conduction block” (i.e., failure of the nerve volley originating at the cathode to progress past the anode on account of hyperpolarization of the axonal membrane). In practice, however, this possibility can be discounted. It is certainly important to locate the cathode in as close proximity to the nerve as possible. The anode then needs to be reasonably close by, since if it is too distant, the stimulus artifact conducted through the body and detected by the recording electrodes may be unmanageably large. The anode does not have to be in close proximity to the nerve, although either a distal or a proximal location may be found to be convenient. If the anode and cathode are reversed, the response will usually be found to be degraded, but this is simply due to the sub-optimal location of the cathode and has nothing to do with “anodic block.” 13.8. Stimulation parameters All the large diameter (groups I and II) sensory fibers in the posterior tibial nerve can be activated by a square-wave cathodic (negative) electrical pulse 0.1 or 0.2 ms in duration. The threshold is lowest for the fibers of largest diameter; the earliest components of the ESEP may, therefore, be elicited by pulses of only a few milliamperes (mA), while it may require 25 mA or more in order to produce maximal amplitude of the later peaks. One of the advantages of epidural as compared with cortical SEPs is that they can be recorded without loss of amplitude or definition at stimulation rates as high as 20 pulses/s, whereas the optimal rate for cortical SEPs, trading some loss of amplitude for higher speed of acquisition, is probably around 5 pulses/s. Even with stimulation at 50 pulses/s the ESEP was found to be only minimally attenuated (Jones et al., 1982). However, at the highest rates it may be found that the ESEP gradually decreases in size when stimuli are applied for long periods. For that reason, it is recommended that the standard rate be no higher than 20 pulses/s, and that a few seconds of rest be allowed after the completion of each average of 200 or 500 responses. Another hazard that has
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been noted is that very high stimulation rates have caused mild burns to the skin. This is probably only a significant factor if the stimulating electrode has become dry (old stock?) or is otherwise defective. A very useful facility offered by most, if not all, of today’s EP recording machines is the ability to record separate responses to stimuli alternating between one stimulus site and another. Consequently, it is possible to record ESEPs separately but concurrently to stimulation of the left and right legs, each leg being stimulated at 10 or even 20 pulses/s. At higher rates, the stimulus artifact associated with stimulation on one side will occur before the response to the last stimulus on the other side has completed. 13.9. Intervention criteria As with cortical SEPs, the figures of 50% amplitude reduction and 10% latency reduction are applied as rough guidelines for the degrees of change that are considered to be “significant”. It should be remembered, however, that these are arbitrary figures which are not based on statistical evidence. In retrospect, it has been generally found that only those patients whose responses diminish by rather more than 50% as compared with the initial “baseline” figure have a substantially increased risk of neurological complications. One problem is the slight tendency (probably less marked for epidural as compared with cortical SEPs) for amplitudes to decline steadily throughout the course of surgery. There is also a tendency for latencies to gradually increase on account of the cooling effect on the spinal cord when the vertebral column is surgically exposed. For these reasons, it is not recommended that the 50% amplitude and 10% latency criteria be rigidly applied, literally or metaphorically, as triggers for “alarm bells”. Since ESEPs are far more immune to systemic factors associated with changes in blood pressure and/or anesthetic agents than cortical responses, any relatively sudden changes that occur in amplitude or (more rarely) latency can be confidently ascribed to surgical events. One is far less worried about a response which hovers around 50% amplitude as compared with the initial baseline value, perhaps occasionally dipping slightly below 50%, than one in which a sudden reduction of, say, 30% occurs, even though this may not cause the overall amplitude to fall below the non-magical 50% criterion. Another important difference of the epidural as compared with the cortical SEP is that parts of the
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response (paradoxically, the earlier rather than the later peaks, see below) are due to postsynaptic spinal cord axons. Since the effects of cord ischemia are likely to impact first on the gray matter rather than the axonal tracts, there are circumstances in which the postsynaptic components may be affected before the later, asynaptic peaks. We (Jones et al., 1983) reported one case in which the initial component of the waveform was temporarily lost on one side after mild trauma to the conus medullaris, suggesting perhaps a mild ischemia causing impaired synaptic processes in the dorsal horn at this level. 13.10. Generators of ESEPs Although it is not part of my brief to cover the clinical aspects of ESEP monitoring, it is not possible entirely to dissociate the practical issues of monitoring from those pertaining to the normal neurophysiology of the sensory pathways of the spinal cord. This was the object of our study (Halonen et al., 1989) which examined the responses recorded at various levels of the cord posteriorly and anteriorly (the latter using needle electrodes inserted in the intervertebral discs) and stimulating various nerves in the lower limbs at a range of stimulus intensities. The study first examined the changing waveform as the electrode was placed at different levels of the dorsal epidural space. Plotting the latency of each peak against distance along the spine revealed a complex pattern of conduction in which different peaks traveled at different velocities. The relatively simple, triphasic positive-negative-positive (PNP) waveform recorded at lumbar and low thoracic levels appeared to be delayed by about 1 ms at the level of the lumbar enlargement, before splitting into two and eventually three or even four negative peaks, overlapping in time and conducted at different velocities ranging from about 40 to 80 m/s (Fig. 1). In addition to the peaks whose latency increased in the rostral direction, there was one whose latency was apparently constant from low to high thoracic levels, probably a “far-field” potentials due to the change in volume conductor characteristics as the volley in the dorsal roots entered the spinal cord. At thoracolumbar levels, there was also a peak whose latency increased in the caudal direction, perhaps a reflex efferent volley associated with the F-wave or H-reflex. A second experiment looked at the lateralization of the peaks by deliberately placing the recording electrode toward the left or right side of the epidural
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space, as well as on the midline. This revealed a tendency for all the peaks to be larger on the side ipsilateral to the stimulated limb, although the degree of lateralization was greatest for the first and least for the third component identified at T4 level. Varying the stimulus intensity also had the effect of dissociating the three negative peaks of the ESEP. It was consistently found that the first peak had the lowest electrical excitation threshold and the third peak the highest. As the intensity was further increased, all the peaks recorded at upper thoracic level eventually reached a plateau of maximal amplitude, while the major negativity recorded at the level of the lumbar enlargement apparently did not. Clearly, the relationship of threshold with stimulus intensity suggests that the later components in the upper thoracic waveform were due to peripheral sensory fibers of smaller diameter, which is also compatible with their longer latency and (presumably) slower conduction velocity. In addition to its lower threshold and faster conduction velocity, evidence was obtained for a postsynaptic origin of the first and possibly also the second component of the ESEP. When the posterior tibial nerve was stimulated at the knee with a relatively low stimulus intensity, a delay of 1–2 ms was evident between the single negative peak recorded at thoracolumbar level and the first peak recorded more rostrally, extrapolated back to estimate its latency at thoracolumbar level (Fig. 2). At this low intensity, two or three peaks were recorded at higher levels, all having a similar, fast conduction velocity suggesting a repetitive volley in postsynaptic axons. Also, when stimuli were given in pairs separated by 2–6 ms, a differential effect was sometimes noted on the three components, all three being present at longer intervals, but the first being relatively attenuated or absent at intervals of 4 ms or less. In order to further establish which afferent fiber types were responsible for the response, ESEPs were recorded to stimulation of different nerve trunks in the lower limb. All amplitudes were reduced and latencies, of course, increased when the posterior tibial nerve was stimulated at the level of the ankle rather than the knee, consistent with a mean peripheral conduction velocity of around 50 m/s (Fig. 3). However, the morphology of the response was also altered, the initial component recorded at upper thoracic level being relatively reduced as compared with the later peaks. When the stimulus was delivered to the sural nerve at the ankle, the response was further reduced in amplitude, and the initial peak was apparently
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1 2 3 T11
T1 T4
T12
T5 T6
L1-upper
T7 L1-lower
T8 L2 T9 4 µV
2 µV
L3 T10
0
10
20
30 ms
0
10 Pt
20
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2
30 3
C7 Ps T4 T5 T6 T7 T8 T9 T10 T11 T12 L1
F/H?
L2 P
N
L3 10
12
14
16
18
ms
Fig. 1. Epidural SEPs (ESEPs) recorded at multiple spinal levels following posterior tibial nerve stimulation at the popliteal fossa (adapted from Halonen et al., 1989). The plot of peak latencies against spinal level (scaled according to the relative size of the vertebrae) reveals a number of features as described in the text.
completely absent. Since the sural nerve contains only cutaneous sensory fibers, while the posterior tibial nerve also contains muscle afferents which are likely to be more numerous at the level of the knee
than the ankle, this led us to conclude that the initial, fastest conducted component of the ESEP was likely to be due to the projection of group I muscle spindle and Golgi tendon organ afferents, while the third
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Level:
Stimulus: 25 ma cm 30
T2
67
44
38 m/s
T5 20
T9 10
T12
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20
Stimulus: 7 ma
2 µV 30 ms
10
cm 30
Level:
77
T2
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20
T9
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15
20 ms
70 83 m/s
T12
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20
1 µV 30 ms
10
15
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Fig. 2. Epidural SEPs (ESEPs) simultaneously recorded at four levels following posterior tibial nerve stimulation at two intensities (adapted from Halonen et al., 1989).
component was due to group II afferents of cutaneous origin. The second component with an intermediate conduction velocity was more difficult to characterize. ESEPs recorded at four spinal levels to stimulation of the posterior tibial and sural nerves at the ankle, and the tibial nerve at the knee, showed a clear pattern of differences (Fig. 3). The first, fastest conducted component was only clearly visible in the
response to tibial nerve stimulation at the knee, and was conducted at around 80 m/s. Responses to stimulation of the same nerve at the ankle mainly consisted of two components, conducted respectively at around 55 and 45 m/s, similar to components two and three of the knee response. The sural nerve response consisted of multiple small peaks, all except possibly the first apparently conducted at velocities of around 40 m/s.
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Level:
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Tibial (knee)
cm 30
T3
80
T6
57
45 m/s
20 T11 10 L3 15
10
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Tibial (ankle) 30
T3
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45 m/s
20 T11
10 L3
1 µV 25
20
30
Sural (ankle) 30
T3 T6
56
37 m/s
20 T11
10 L3
10
20
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40
0.5 µV 50 ms
20
25
30 ms
Fig. 3. Epidural SEPs (ESEPs) simultaneously recorded at four levels following stimulation of the posterior tibial nerve at the knee and the ankle and the sural nerve at the ankle (adapted from Halonen et al., 1989).
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The model to which these various lines of evidence all contribute is one in which the first component of the ESEP is generated in a postsynaptic, fast-conducting sensory tract located relatively laterally in the spinal cord on the side ipsilateral to the stimulus. The fact that this component is not elicited by stimulation of the purely cutaneous sural nerve suggests that the fibers concerned are muscle afferents of group I, and the tract is the dorsal spinocerebellar tract which has its synaptic origin in Clarke’s column, located in lamina VII at the base of the dorsal horn. The third component, due to a more medially located tract and due to fibers of slower conduction velocity with no intervening synapse, is almost certainly the dorsal columns which convey mainly cutaneous activity. 13.11. Advantages and disadvantages of epidural as compared with cortical SEPs From a practical perspective, the advantages of recording ESEPs to stimulation of the posterior tibial nerve at the knee are that the activity of more than one afferent spinal cord pathway can be distinguished, and that one of the major constituents of the response is postsynaptic and may, therefore, provide a sensitive indicator of ischemia in the cord at the level of the lumbar enlargement. Further advantages are the virtual immunity of ESEPs to anesthetic agents and variations in blood pressure (unless this becomes catastrophically low), and the high speed of acquisition. The most significant disadvantage of ESEPs is the invasiveness of the method and the fact that the technique cannot be applied in all circumstances where spinal cord monitoring is indicated. The technique is generally found to be safe in patients whose spinal canal is unobstructed; very rarely, however, insertion of the electrode may cause rupture of the dura and leakage of cerebrospinal fluid. One factor which has been noted to impair the recording of ESEPs is pooling of blood in the vicinity of the recording electrode. Another factor is that responses may be lost when the lead is inserted too far, such that the recording tip deviates too far from the midline of the spinal cord. Both of these problems may require the electrode to be temporarily removed and reinserted, and this will invalidate the “baseline” amplitude and latency values used to identify subsequent changes. Finally, it should be noted that the application of high stimulus intensities at fast
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rates and for long periods may risk the occurrence of a “compartment” syndrome. For this reason, the use of muscle relaxants, at least in low concentrations, may be considered advisable. In adolescent patients undergoing surgery for kyphoscoliosis, it is often possible to record spinal SEPs of good quality from the skin of the neck at mid-to-high cervical level. Consequently, it may be argued that the use of invasive epidural electrodes is not entirely necessary. Of course, it is possible to record a cervical response concurrently with cortical potentials, but drawbacks to this are that the optimal rate of stimulation for cortical SEPs is much lower, and that whereas the cervical response is best recorded to stimulation at the popliteal fossa, cortical SEPs tend to be better defined and of larger amplitude to stimulation of the same nerve at the ankle.
References Anderson, SK, Loughnan, BA and Hetreed, MA (1990) A technique for monitoring evoked potentials during scoliosis and brachial plexus surgery. Ann. R. Coll. Surg. Engl., 72(5): 321–323. Gasser, HS and Graham, HT (1933) Potentials recorded in the spinal cord by stimulation of the dorsal roots. Am. J. Physiol., 103: 303–320. Halonen, JP, Jones, SJ, Edgar, MA and Ransford, AO (1989) Conduction properties of epidurally recorded spinal cord potentials following lower limb stimulation in man. Electroencephalogr. Clin. Neurophysiol., 74(3): 161–174. Jones, SJ, Edgar, MA and Ransford, AO (1982) Sensory nerve conduction in the human spinal cord: epidural recordings made during scoliosis surgery. J. Neurol. Neurosurg. Psychiatry, 45(5): 446–451. Jones, SJ, Edgar, MA, Ransford, AO and Thomas, NP (1983) A system for the electrophysiological monitoring of the spinal cord during operations for scoliosis. J. Bone Joint Surg. Br., 65(2): 134–139. Macon, JB and Poletti, CE (1982) Conducted somatosensory evoked potentials during spinal surgery. Part 1: control conduction velocity measurements. J. Neurosurg., 57(3): 349–353. Shimoji, K, Kano, T, Higashi, H, Morioka, T and Henschel, EO (1972) Evoked spinal electrograms recorded from epidural space in man. J. Appl. Physiol., 33: 468–471. Tamaki, T, Tsuji, H, Inoue, SI and Kobayashi, H (1981) The prevention of iatrogenic spinal cord injury utilizing the evoked spinal cord potential. In Orthop., 4: 313–317. Tsuyama, N, Tsuzuki, N, Kurokawa, T and Imai, T (1978) Clinical application of spinal cord action potential measurement. In Orthop., 2: 39–46.
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CHAPTER 13
Monitoring spinal epidural potentials to peripheral nerve stimulation Steve Jones* Department of Clinical Neurophysiology, National Hospital for Neurology and Neurosurgery, London WC1N 3BG, UK
13.1. Background The first recordings of sensory evoked activity in the human spinal cord were made in the 1930s (Gasser and Graham, 1933). With only one or two intervening publications, it was not until the 1970s that a number of groups in Japan started to exploit the experimental and clinical possibilities of the “evoked spinal cord potentials” (e.g., Shimoji et al., 1972; Tsuyama et al., 1978). These studies involved inserting an electrode at the end of a flexible lead into the epidural space. When located at the appropriate level, the electrode was used to record localized “segmental” activity generated in the dorsal columns and dorsal horn, following stimulation of the dorsal roots or a nerve trunk in the upper or lower limb. It was the realization that an electrode at cervical level could be used to record “conducted” activity following stimulation of a nerve in the lower limb, or of the spinal cord at a lower level, that led to the exploitation of this technique in investigating and monitoring the integrity of long spinal cord tracts during surgery (Tamaki et al., 1981). In Japan, it was generally the surgeons themselves who were responsible for all aspects of the recording procedure. This, I believe, is the reason why the methodology most widely used in Japan today involves both stimulating and recording electrodes located in the dorsal epidural space. Elsewhere, the involvement of neurophysiologists, accustomed to methods of peripheral nerve stimulation used for the clinical application of somatosensory evoked potentials (SEPs), resulted in the importation of their *
Correspondence to: Steve Jones, Ph.D., Department of Clinical Neurophysiology, The National Hospital for Neurology and Neurosurgery, Queen Square, London WC1N 3BG, UK. Tel.: þ44-20-7837-3611, ext. 4109; fax: þ44-20-7713-7743. E-mail: [email protected] (S. Jones).
methods into the operating theater. The epidural SEP (ESEP) method appears to have been introduced concurrently and independently in the UK and Australia (Jones et al., 1982; Macon and Poletti, 1982). 13.2. Applicability In the UK, the ESEP method is used almost exclusively by orthopedic surgeons concerned with the treatment of spinal deformities, in particular kyphoscoliosis, occurring in adolescents and young adults. Most of the patients, therefore, are otherwise healthy and neurologically normal. A minority will have kyphoscoliosis of neurogenic origin; when associated with peripheral neuropathy or combined peripheral/central conditions such as Friedreich’s ataxia, the degeneration of large diameter peripheral sensory fibers may be so extensive that it is impossible to record a reliable ESEP. In these cases, cortical SEPs may sometimes be better preserved, but this is not necessarily to be relied upon. In cases of severe neuropathy, therefore, the Japanese method of recording evoked spinal cord potentials to stimulation of the spinal cord at a rostral or caudal level is probably the only one which can be resorted to. In Friedreich’s ataxia, the fact that the sensory pathways of the spinal cord, specifically the dorsal columns, are also affected may thwart even this technique. The fixation and instrumentation used for the correction of scoliosis (Harrington rods and compression/distraction systems attached via sublaminar wires or pedicle screws) are all applied from the dorsal side, so the initial placement of an electrode in the dorsal epidural space is straightforward. When the operation also involves treatment of lumbar kyphosis, it is clearly not possible to insert an electrode via the surgical field. However, a number of publications describe methods for inserting the electrode percutaneously in the anesthetic room (e.g., Anderson et al., 1990) which can also be exploited in other contexts.
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ESEPs are less frequently used for spinal cord monitoring during neurosurgical procedures. This is probably because the insertion of an electrode into the epidural space can be difficult or undesirable in patients with a narrow spinal canal (stenosis), or in whom the canal is otherwise distorted by tumor, subluxation (displacement of one vertebral body relative to the adjacent one), or fracture. When performed at multiple levels, ESEPs offer the opportunity of detecting not only the occurrence but also the level of conduction failure in the spinal cord. Multi-level recordings are not performed routinely, on account of the obstruction caused by the presence of leads in the surgical field, but additional electrodes can be rapidly inserted by the surgeon if and when a problem is identified. 13.3. Recording electrodes The recording electrode consists of a cylindrical sleeve of a chemically inert conducting material (stainless steel or platinum) whose diameter is the same as that of the lead whose end it forms. The diameter is usually around 1 mm and the length of the sleeve is around 3–5 mm. A second sleeve, at least 1 cm and no more than 5 cm along the same lead, may be used in conjunction with the first sleeve in order to obtain bipolar recordings. Alternatively, for monopolar recordings, a reference electrode (for example, a stainless steel needle) can be placed in the body tissue outside the surgical zone, as close as possible to the epidural electrode in order to avoid excessive pickup of extraneous noise. In most centers, disposable electrodes are now generally preferred to reusable types, but there is no reason, in principle, why an epidural electrode, properly constructed so there is no point of potential weakness or seepage between the conductive sleeve and the rest of the lead, should not be sterilized and used on multiple occasions. When under the control of the surgeon, the lead is introduced to the epidural space at the upper end of the surgical field, after exposure of the spine. It can be inserted directly when the dura is exposed by a laminectomy. Alternatively, the surgeon may choose to make a small hole in the interspinous ligament and insert the lead directly. A third option is to use the needle of a catheter of the appropriate diameter to pierce the interspinous ligament. The needle is then withdrawn leaving the catheter in place and the lead is introduced. Secured by a suture, the rest of the lead can then be
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routed out of the surgical field in the direction of the head. The natural angle of the dorsal processes means that the lead will be introduced aslant, the electrode tip pointing in the direction of the head. This is desirable, because on entry into the epidural space, it will then naturally tend to proceed in a cephalad direction. Obviously, recordings of evoked sensory activity need to be made from a level above any that are considered to be at risk during surgery. If the lead is introduced, for example, at the T1/2 level, there will usually be no obstruction to advancing the electrode to a low- or mid-cervical level comfortably above those segments of the cord that are likely to be at risk during surgery for kyphoscoliosis. Critical for the successful placement of the electrode, however, is the material of the lead. The advantage of making the lead as thin as possible is obvious, but if the conducting core and insulating sleeve are too flexible, this may result in unpredictable deviations as the lead is advanced. Small deviations from the midline are unimportant and probably inevitable, but clearly the surgeon needs to be confident that the lead is not so flexible that the tip finishes up altogether on one side of the cord or the other. In some centers, the surgeon or anesthetist will be confident to introduce the epidural electrode percutaneously in the anesthetic room, after induction of anesthesia (e.g., Anderson et al., 1990). This has the advantage that the ESEP technique can then be used to monitor operations performed from the anterior side of the spine. 13.4. Recording parameters The ESEP recorded at low cervical level to stimulation of the posterior tibial nerve at the level of the knee (popliteal fossa) has a latency of around 15 ms (depending, of course, on the age and height of the patient) and a duration of around 5–8 ms. It therefore demands a recording epoch (window) of at least 25 ms starting at the time of stimulus delivery. Most evoked potential (EP) recording machines today offer a wide range of epochs including 30 ms which is probably the ideal. There is usually no means of varying the digital sampling rate independently of the recording epoch. To obtain accurate representation of the briefest peaks in the response, a sampling rate of at least 10 kHz is desirable; with an epoch of 30 ms, this will almost certainly be comfortably exceeded.
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Since the ESEP largely comprises brief, polyphasic potentials rather than broad, slow waves, it is not necessary to amplify the signals over the full frequency range at the lower end of the spectrum. This is highly advantageous, since it means that mains-related noise frequencies of 50 or 60 Hz can be excluded by the use of a high-pass filter at 100 or even 200 Hz. In order faithfully to reproduce the high frequencies in the waveform, the low-pass filter needs to be set no lower than 2 kHz. The number of responses that need to be averaged in order to get an accurate measure of the signal depends on the level of background noise. Two hundred may be adequate in many circumstances, with the option of adding further responses to the average when noise levels are relatively high. 13.5. Bipolar versus monopolar recording The choice of monopolar (one epidural electrode referred to a needle or some other electrode alongside the spine) or bipolar epidural recording is probably best left to personal preference, since there seems to be an approximately equal weight of opinion on both sides. Monopolar recordings have the advantage that the individual components of the response can all be distinguished and are not confused with one another. This is perhaps of greatest value to neurophysiologists interested in exactly which tracts of the spinal cord are responsible for each component. Bipolar recordings are generally less noisy, because the close proximity of the two electrodes means that a larger proportion of the background noise is excluded by “common mode rejection.” In principle, it should be possible to construct a bipolar electrode pair in which the separation is chosen so as to maximize the amplitude of the response. For example, a typical ESEP waveform might consist of three negative and three positive peaks, the consecutive peaks of opposite polarity being about 0.5 ms apart. Their mean conduction velocity in the spinal cord is in the order of 60 m/s; so, in 0.5 ms, the waveform would travel approximately 3 cm. In theory, then, a 3-cm separation between the two electrodes should result in the largest recorded amplitude, since a peak of negativity recorded by one electrode would be amplified relative to a peak of positivity recorded by the other. Having the electrode separation less than 3 cm (as is usually the case) will undoubtedly reduce the amplitude of the response, but the components of the waveform should still be distinguishable and the
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background noise should be less. Separations of more than 3 cm should result in the waveform becoming more polyphasic, which is probably not desirable, and noisier. 13.6. Stimulating electrodes Many types of stimulating electrodes have been used for SEP studies outside the operating theater, but most are unsuitable for intraoperative use. In particular, stimulating electrodes that need to be moistened with water or saline may be prone to drying out during a long procedure. The use of straps around the limb is also strongly advised against, since this might cause constriction of the blood circulation. Stick-on type electrocardiographic (ECG) electrodes have the advantage that their contact area of gel is largely protected from evaporation. They can be effectively used to stimulate virtually any peripheral nerve that does not run too deep in the limb muscles, without the use of elastic straps. Needle electrodes should be equally effective, although they should only be inserted when the patient is finally positioned for surgery and removed if repositioning is necessary. 13.7. Stimulation sites The largest lower limb nerve running close enough to the surface to be easily stimulated transcutaneously is the posterior tibial nerve at the level of the popliteal fossa. The best way of discovering the most effective site for locating the stimulating cathode is to try it on oneself. The posterior tibial nerve contains the majority of large diameter (therefore, fast-conducting and with a low threshold for electrical excitation) group II cutaneous sensory fibers deriving from the sole of the foot, where the density of innervation is probably higher than elsewhere in the limb. It also contains large diameter proprioceptive fibers (group I muscle spindle and Golgi tendon organ afferents) from muscles responsible for flexion of the foot and the toes. The general experience is that this is the best nerve to stimulate for intraoperative monitoring of ESEPs. Cortical SEPs, however, are usually better produced by stimulation of the posterior tibial nerve at the level of the ankle. The reason for this is unclear, but it may be related to inhibitory interaction at cortical or subcortical level between the cutaneous projection and the muscle afferents projecting to different regions of the cortex. ESEPs can be recorded to stimulation of other nerves in the leg,
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but generally it is only the posterior tibial nerve at the popliteal fossa that gives rise to the large amplitude, fast-conducted responses which are most easily measured. In the literature it is often advised that the stimulating cathode for SEP recordings be placed proximal to the anode, in order to avoid “anodic conduction block” (i.e., failure of the nerve volley originating at the cathode to progress past the anode on account of hyperpolarization of the axonal membrane). In practice, however, this possibility can be discounted. It is certainly important to locate the cathode in as close proximity to the nerve as possible. The anode then needs to be reasonably close by, since if it is too distant, the stimulus artifact conducted through the body and detected by the recording electrodes may be unmanageably large. The anode does not have to be in close proximity to the nerve, although either a distal or a proximal location may be found to be convenient. If the anode and cathode are reversed, the response will usually be found to be degraded, but this is simply due to the sub-optimal location of the cathode and has nothing to do with “anodic block.” 13.8. Stimulation parameters All the large diameter (groups I and II) sensory fibers in the posterior tibial nerve can be activated by a square-wave cathodic (negative) electrical pulse 0.1 or 0.2 ms in duration. The threshold is lowest for the fibers of largest diameter; the earliest components of the ESEP may, therefore, be elicited by pulses of only a few milliamperes (mA), while it may require 25 mA or more in order to produce maximal amplitude of the later peaks. One of the advantages of epidural as compared with cortical SEPs is that they can be recorded without loss of amplitude or definition at stimulation rates as high as 20 pulses/s, whereas the optimal rate for cortical SEPs, trading some loss of amplitude for higher speed of acquisition, is probably around 5 pulses/s. Even with stimulation at 50 pulses/s the ESEP was found to be only minimally attenuated (Jones et al., 1982). However, at the highest rates it may be found that the ESEP gradually decreases in size when stimuli are applied for long periods. For that reason, it is recommended that the standard rate be no higher than 20 pulses/s, and that a few seconds of rest be allowed after the completion of each average of 200 or 500 responses. Another hazard that has
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been noted is that very high stimulation rates have caused mild burns to the skin. This is probably only a significant factor if the stimulating electrode has become dry (old stock?) or is otherwise defective. A very useful facility offered by most, if not all, of today’s EP recording machines is the ability to record separate responses to stimuli alternating between one stimulus site and another. Consequently, it is possible to record ESEPs separately but concurrently to stimulation of the left and right legs, each leg being stimulated at 10 or even 20 pulses/s. At higher rates, the stimulus artifact associated with stimulation on one side will occur before the response to the last stimulus on the other side has completed. 13.9. Intervention criteria As with cortical SEPs, the figures of 50% amplitude reduction and 10% latency reduction are applied as rough guidelines for the degrees of change that are considered to be “significant”. It should be remembered, however, that these are arbitrary figures which are not based on statistical evidence. In retrospect, it has been generally found that only those patients whose responses diminish by rather more than 50% as compared with the initial “baseline” figure have a substantially increased risk of neurological complications. One problem is the slight tendency (probably less marked for epidural as compared with cortical SEPs) for amplitudes to decline steadily throughout the course of surgery. There is also a tendency for latencies to gradually increase on account of the cooling effect on the spinal cord when the vertebral column is surgically exposed. For these reasons, it is not recommended that the 50% amplitude and 10% latency criteria be rigidly applied, literally or metaphorically, as triggers for “alarm bells”. Since ESEPs are far more immune to systemic factors associated with changes in blood pressure and/or anesthetic agents than cortical responses, any relatively sudden changes that occur in amplitude or (more rarely) latency can be confidently ascribed to surgical events. One is far less worried about a response which hovers around 50% amplitude as compared with the initial baseline value, perhaps occasionally dipping slightly below 50%, than one in which a sudden reduction of, say, 30% occurs, even though this may not cause the overall amplitude to fall below the non-magical 50% criterion. Another important difference of the epidural as compared with the cortical SEP is that parts of the
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response (paradoxically, the earlier rather than the later peaks, see below) are due to postsynaptic spinal cord axons. Since the effects of cord ischemia are likely to impact first on the gray matter rather than the axonal tracts, there are circumstances in which the postsynaptic components may be affected before the later, asynaptic peaks. We (Jones et al., 1983) reported one case in which the initial component of the waveform was temporarily lost on one side after mild trauma to the conus medullaris, suggesting perhaps a mild ischemia causing impaired synaptic processes in the dorsal horn at this level. 13.10. Generators of ESEPs Although it is not part of my brief to cover the clinical aspects of ESEP monitoring, it is not possible entirely to dissociate the practical issues of monitoring from those pertaining to the normal neurophysiology of the sensory pathways of the spinal cord. This was the object of our study (Halonen et al., 1989) which examined the responses recorded at various levels of the cord posteriorly and anteriorly (the latter using needle electrodes inserted in the intervertebral discs) and stimulating various nerves in the lower limbs at a range of stimulus intensities. The study first examined the changing waveform as the electrode was placed at different levels of the dorsal epidural space. Plotting the latency of each peak against distance along the spine revealed a complex pattern of conduction in which different peaks traveled at different velocities. The relatively simple, triphasic positive-negative-positive (PNP) waveform recorded at lumbar and low thoracic levels appeared to be delayed by about 1 ms at the level of the lumbar enlargement, before splitting into two and eventually three or even four negative peaks, overlapping in time and conducted at different velocities ranging from about 40 to 80 m/s (Fig. 1). In addition to the peaks whose latency increased in the rostral direction, there was one whose latency was apparently constant from low to high thoracic levels, probably a “far-field” potentials due to the change in volume conductor characteristics as the volley in the dorsal roots entered the spinal cord. At thoracolumbar levels, there was also a peak whose latency increased in the caudal direction, perhaps a reflex efferent volley associated with the F-wave or H-reflex. A second experiment looked at the lateralization of the peaks by deliberately placing the recording electrode toward the left or right side of the epidural
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space, as well as on the midline. This revealed a tendency for all the peaks to be larger on the side ipsilateral to the stimulated limb, although the degree of lateralization was greatest for the first and least for the third component identified at T4 level. Varying the stimulus intensity also had the effect of dissociating the three negative peaks of the ESEP. It was consistently found that the first peak had the lowest electrical excitation threshold and the third peak the highest. As the intensity was further increased, all the peaks recorded at upper thoracic level eventually reached a plateau of maximal amplitude, while the major negativity recorded at the level of the lumbar enlargement apparently did not. Clearly, the relationship of threshold with stimulus intensity suggests that the later components in the upper thoracic waveform were due to peripheral sensory fibers of smaller diameter, which is also compatible with their longer latency and (presumably) slower conduction velocity. In addition to its lower threshold and faster conduction velocity, evidence was obtained for a postsynaptic origin of the first and possibly also the second component of the ESEP. When the posterior tibial nerve was stimulated at the knee with a relatively low stimulus intensity, a delay of 1–2 ms was evident between the single negative peak recorded at thoracolumbar level and the first peak recorded more rostrally, extrapolated back to estimate its latency at thoracolumbar level (Fig. 2). At this low intensity, two or three peaks were recorded at higher levels, all having a similar, fast conduction velocity suggesting a repetitive volley in postsynaptic axons. Also, when stimuli were given in pairs separated by 2–6 ms, a differential effect was sometimes noted on the three components, all three being present at longer intervals, but the first being relatively attenuated or absent at intervals of 4 ms or less. In order to further establish which afferent fiber types were responsible for the response, ESEPs were recorded to stimulation of different nerve trunks in the lower limb. All amplitudes were reduced and latencies, of course, increased when the posterior tibial nerve was stimulated at the level of the ankle rather than the knee, consistent with a mean peripheral conduction velocity of around 50 m/s (Fig. 3). However, the morphology of the response was also altered, the initial component recorded at upper thoracic level being relatively reduced as compared with the later peaks. When the stimulus was delivered to the sural nerve at the ankle, the response was further reduced in amplitude, and the initial peak was apparently
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1 2 3 T11
T1 T4
T12
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L1-upper
T7 L1-lower
T8 L2 T9 4 µV
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C7 Ps T4 T5 T6 T7 T8 T9 T10 T11 T12 L1
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ms
Fig. 1. Epidural SEPs (ESEPs) recorded at multiple spinal levels following posterior tibial nerve stimulation at the popliteal fossa (adapted from Halonen et al., 1989). The plot of peak latencies against spinal level (scaled according to the relative size of the vertebrae) reveals a number of features as described in the text.
completely absent. Since the sural nerve contains only cutaneous sensory fibers, while the posterior tibial nerve also contains muscle afferents which are likely to be more numerous at the level of the knee
than the ankle, this led us to conclude that the initial, fastest conducted component of the ESEP was likely to be due to the projection of group I muscle spindle and Golgi tendon organ afferents, while the third
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Level:
Stimulus: 25 ma cm 30
T2
67
44
38 m/s
T5 20
T9 10
T12
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Stimulus: 7 ma
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70 83 m/s
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Fig. 2. Epidural SEPs (ESEPs) simultaneously recorded at four levels following posterior tibial nerve stimulation at two intensities (adapted from Halonen et al., 1989).
component was due to group II afferents of cutaneous origin. The second component with an intermediate conduction velocity was more difficult to characterize. ESEPs recorded at four spinal levels to stimulation of the posterior tibial and sural nerves at the ankle, and the tibial nerve at the knee, showed a clear pattern of differences (Fig. 3). The first, fastest conducted component was only clearly visible in the
response to tibial nerve stimulation at the knee, and was conducted at around 80 m/s. Responses to stimulation of the same nerve at the ankle mainly consisted of two components, conducted respectively at around 55 and 45 m/s, similar to components two and three of the knee response. The sural nerve response consisted of multiple small peaks, all except possibly the first apparently conducted at velocities of around 40 m/s.
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Level:
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Tibial (knee)
cm 30
T3
80
T6
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45 m/s
20 T11 10 L3 15
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Fig. 3. Epidural SEPs (ESEPs) simultaneously recorded at four levels following stimulation of the posterior tibial nerve at the knee and the ankle and the sural nerve at the ankle (adapted from Halonen et al., 1989).
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The model to which these various lines of evidence all contribute is one in which the first component of the ESEP is generated in a postsynaptic, fast-conducting sensory tract located relatively laterally in the spinal cord on the side ipsilateral to the stimulus. The fact that this component is not elicited by stimulation of the purely cutaneous sural nerve suggests that the fibers concerned are muscle afferents of group I, and the tract is the dorsal spinocerebellar tract which has its synaptic origin in Clarke’s column, located in lamina VII at the base of the dorsal horn. The third component, due to a more medially located tract and due to fibers of slower conduction velocity with no intervening synapse, is almost certainly the dorsal columns which convey mainly cutaneous activity. 13.11. Advantages and disadvantages of epidural as compared with cortical SEPs From a practical perspective, the advantages of recording ESEPs to stimulation of the posterior tibial nerve at the knee are that the activity of more than one afferent spinal cord pathway can be distinguished, and that one of the major constituents of the response is postsynaptic and may, therefore, provide a sensitive indicator of ischemia in the cord at the level of the lumbar enlargement. Further advantages are the virtual immunity of ESEPs to anesthetic agents and variations in blood pressure (unless this becomes catastrophically low), and the high speed of acquisition. The most significant disadvantage of ESEPs is the invasiveness of the method and the fact that the technique cannot be applied in all circumstances where spinal cord monitoring is indicated. The technique is generally found to be safe in patients whose spinal canal is unobstructed; very rarely, however, insertion of the electrode may cause rupture of the dura and leakage of cerebrospinal fluid. One factor which has been noted to impair the recording of ESEPs is pooling of blood in the vicinity of the recording electrode. Another factor is that responses may be lost when the lead is inserted too far, such that the recording tip deviates too far from the midline of the spinal cord. Both of these problems may require the electrode to be temporarily removed and reinserted, and this will invalidate the “baseline” amplitude and latency values used to identify subsequent changes. Finally, it should be noted that the application of high stimulus intensities at fast
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rates and for long periods may risk the occurrence of a “compartment” syndrome. For this reason, the use of muscle relaxants, at least in low concentrations, may be considered advisable. In adolescent patients undergoing surgery for kyphoscoliosis, it is often possible to record spinal SEPs of good quality from the skin of the neck at mid-to-high cervical level. Consequently, it may be argued that the use of invasive epidural electrodes is not entirely necessary. Of course, it is possible to record a cervical response concurrently with cortical potentials, but drawbacks to this are that the optimal rate of stimulation for cortical SEPs is much lower, and that whereas the cervical response is best recorded to stimulation at the popliteal fossa, cortical SEPs tend to be better defined and of larger amplitude to stimulation of the same nerve at the ankle.
References Anderson, SK, Loughnan, BA and Hetreed, MA (1990) A technique for monitoring evoked potentials during scoliosis and brachial plexus surgery. Ann. R. Coll. Surg. Engl., 72(5): 321–323. Gasser, HS and Graham, HT (1933) Potentials recorded in the spinal cord by stimulation of the dorsal roots. Am. J. Physiol., 103: 303–320. Halonen, JP, Jones, SJ, Edgar, MA and Ransford, AO (1989) Conduction properties of epidurally recorded spinal cord potentials following lower limb stimulation in man. Electroencephalogr. Clin. Neurophysiol., 74(3): 161–174. Jones, SJ, Edgar, MA and Ransford, AO (1982) Sensory nerve conduction in the human spinal cord: epidural recordings made during scoliosis surgery. J. Neurol. Neurosurg. Psychiatry, 45(5): 446–451. Jones, SJ, Edgar, MA, Ransford, AO and Thomas, NP (1983) A system for the electrophysiological monitoring of the spinal cord during operations for scoliosis. J. Bone Joint Surg. Br., 65(2): 134–139. Macon, JB and Poletti, CE (1982) Conducted somatosensory evoked potentials during spinal surgery. Part 1: control conduction velocity measurements. J. Neurosurg., 57(3): 349–353. Shimoji, K, Kano, T, Higashi, H, Morioka, T and Henschel, EO (1972) Evoked spinal electrograms recorded from epidural space in man. J. Appl. Physiol., 33: 468–471. Tamaki, T, Tsuji, H, Inoue, SI and Kobayashi, H (1981) The prevention of iatrogenic spinal cord injury utilizing the evoked spinal cord potential. In Orthop., 4: 313–317. Tsuyama, N, Tsuzuki, N, Kurokawa, T and Imai, T (1978) Clinical application of spinal cord action potential measurement. In Orthop., 2: 39–46.