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With good reason neurosurgeons continue to have great respect for the spinal cord. In particular, the resection of intramedullary tumors is believed to carry a high risk for surgical damage and subsequent neurological dysfunction because the cord is such a delicate structure with tightly packed essential pathways and neural circuits. Surgical manipulation inside the cord involves the risk for selective damage to either the motor pathways, or the sensory pathways, or the cord’s intrinsic neural apparatus. Since paralysis, the loss of voluntary motor control and ambulation, is the most feared neurological complication, it is essential to have a tool that directly, selectively, and reliably monitors the functional integrity of the motor system during the resection of lesions in or close to the cord. Intraoperative neurophysiological monitoring with motor-evoked potentials (MEPs) is this tool. In this day and age it is widely and most often already routinely applied in all intrinsic surgery of the spinal cord: resection of intramedullary tumors and intradural–extramedullary tumors and drainage or fenestration of syringomyelia.
The first use of evoked potentials to assess functional aspects of the spinal cord during an operation came from orthopedic surgeons .
Somatosensory-evoked potentials (SEPs) were the only monitoring methodology available at that time. From the present technological perspective with portable devices, Apps, and the Cloud, the difficulties with slow recording hardware, difficult documentation, and lack of experience must have been formidable. In addition, a conceptual problem was associated with monitoring of SEPs: they reflect, of course, only the functional integrity of the sensory pathways and therefore provide only indirect information on the more relevant motor pathways. This may be acceptable for spinal surgery, where external cord compression would be the most likely mechanism of injury, which is likely to affect both pathways in a similar manner. SEP monitoring was, and probably still is, used in this sense of “overall” spinal cord monitoring when MEP monitoring was not available. And SEP monitoring has shown strong evidence to be beneficial in large numbers of spinal orthopedic operations . However, damage to the motor tract without changes in SEP recordings has been reported early in the monitoring experience . Furthermore, change in or loss of SEPs during intramedullary operations has been found to be common, most likely as a result of the need to enter the cord through the dorsal midline. In intramedullary surgery, SEP changes do not correlate to the motor outcome. The recording delay with averaging may allow identification of injury some significant time after the event.
With Merton’s first paper on electrically evoked MEPs , neurosurgeons understood the potential of this technique for the direct and selective intraoperative assessment of motor pathways in both the brain and the spinal cord. Building on concepts of the motor system developed since the 1950s , MEP monitoring became part of neurosurgical practice. First came the introduction of the D-wave to the operating room . In addition to this recording technique, which requires recording from the cord with an epidurally placed electrode, muscle recording techniques were introduced with magnetic and electric stimulation. Anesthesia posed a major problem, but the development of a multipulse, or train-stimulus technique resolved this difficulty.
In the 1990s the understanding of neurophysiological concepts, interpretation, and safety increased, the experience with practical application improved. Several series provided first evidence that intraoperative MEP monitoring really works and is indeed useful for the experienced neurosurgeon .
In the 2000s with the improvement of technology and subsequent widespread use of MEP monitoring brought itself into the mainstream neurosurgery for spinal cord procedures. Worldwide experience confirmed the initial concepts, and interpretation improved with the establishment of a warning hierarchy . The impact of the use of MEP monitoring on the outcome of spinal cord surgery extended this experience with a new level of evidence .
Based on this extensive experience and a growing body of evidence, this chapter aims to illustrate that MEP monitoring of the functional integrity of the motor pathways during surgery in or around the spinal cord is one of the most impressive, accurate, and useful neuromonitoring techniques in use today. MEP monitoring can be safely done, it represents the clinical “reality,” and its concept provides a warning window of reversible change, which allows for surgery with greater safety from neurological injury and confidence for radical tumor resection.
Motor potentials (D-waves and muscle MEPs) are evoked with transcranial electrical stimulation. Specific stimulus points are at C3, C4, C1, C2, Cz, and a point 6 cm in front of Cz (International 10/20 EEG electrode system) ( Fig. 26.1A ).
D-waves result from direct activation of fast-conducting thickly myelinated corticospinal nerve fibers through a single electrical stimulus (the “single-stimulus technique,” Fig. 26.1B ). The number of fibers determine the amplitude of this potential, thereby it serves as the pertinent measure intraoperatively . It is a nonsynaptic and linear response.
The activation of the axons occur in the subcortical white matter and is recorded by an epidural or subdural bipolar electrode, placed caudally of the intraspinal lesion after laminectomy ]. This single-stimulus tech2nique provides real-time feedback. Pulse intensity is kept between 80 and 200 mA with a pulse duration of 0.5 ms. Recordings can be repeated with a frequency of up to 2 Hz. Baseline recordings should be obtained before opening of dura and resection of lesion. The baseline should be defined as the D-wave with maximal amplitude, where further increase of stimulus intensity results in no further increase of amplitude. Usually no averaging is needed but averaging of 4–10 stimuli can improve signal-to-noise ratio. No muscle response is observed because lower motoneuron excitatory postsynaptic potential fails to reach firing threshold with a single impulse. The relevant parameter of the D-wave that is monitored is the peak-to-peak amplitude ( Fig. 26.1C ).
A reliable D-wave can only be obtained above and at the level of about Th10, due to a lack of enough corticospinal tract fibers further caudally .
A deterioration of 50% of D-wave amplitude has been commonly assumed as a warning criterion in intramedullary surgery and should not be exceeded. Preservation of a D-wave with at least 50% of the baseline amplitude is consistent with long-term preservation of walking ability, deterioration below 50% of baseline amplitude predicts postsurgical motor deficits .
Higher intensities of stimulation lead to shorter latencies, implying that fiber activation occurs deeper in with matter of the brain .
Specific circumstances exist for infants below 18 months of age. They show stable muscle MEPs, but no D-wave monitoring may be possible .
Muscle MEPs are also elicited with transcranial stimulation at the same points. Electrical stimulation is performed with pulse train stimuli consisting of five to seven pulses with a 4 ms interstimulus interval. Hence, this is called the “train-stimulus technique” ( Fig. 26.1B ). Each pulse has 0.5 ms duration and intensities between 20 and 250 mA .
Muscle action potentials are recorded with a pair of needle electrodes from target muscles ( Fig. 26.1D ).
Baseline MEP recording should always contain at least two muscles from different innervation groups with high pyramidal innervation, such as thenar muscles and flexor/extensors for upper extremity and tibialis anterior and abductor hallucis muscles for lower extremity .
Depending on the surgical level, muscle MEPs allow specific analysis of the functional integrity of descending motor tracts .
Baseline recordings are obtained before or sometimes during the initial stages of surgery. If strong neck inclination is required for surgery in the prone position recording baselines before and after patient positioning may be required to assure the surgeon that the chosen extent of inclination does not affect the cord. No averaging is needed. Muscle MEPs provide real-time feedback and can be repeated in a practically continuous fashion with up to 2 Hz frequency.
Primary stimulation sites are C1/2 or C2/1. In the case of difficulties C3/4, C4/3, or Cz/6 cm can be used as alternative stimulation points .
Each stimulation pulse creates a D-wave traveling down the corticospinal tract. The train of five to seven stimuli result in a subsequent depolarization of spinal alpha-motoneurons by reaching firing threshold .
MEPs are polysynaptic and the responses therefore nonlinear. As a consequence it is possible that a large decrement of MEP amplitude can result from a small reduction of corticospinal tract neurons .
Muscle MEP interpretation in relation to clinical examination and useful intraoperative warning criteria will be discussed later in this chapter.
Chapter 40 , Principles of anesthesia, is concerned with all aspects of general anesthesia in the context of intraoperative monitoring. Therefore this will only be touched very briefly here.
MEP monitoring is sensitive to anesthetic agents. Latencies and, particularly, amplitudes can change depending on the used agent. Usually continuous infusion of Propofol 40–75 µg/kg/min and Remifentanil 0.1–0.4 µg/kg/min is used for sufficient anesthesia and monitoring .
Up to 50 vol.% nitrous oxide can be added without significant response suppression . Sevoflurane causes a decrease in amplitude and cannot be used with MEP monitoring. Bolus injections of intravenous agents should be avoided since temporary disruption of muscle MEPs was observed .
Adding ketamine appears to stabilize MEPs and improve MEP monitoring .
Short-acting muscle relaxant is only used for intubation. A so-called balanced partial myorelaxation has been reported , but we do not consider the influence of an uncontrolled variable useful and do not see a notable benefit.
Other confounding factors, that is, nonsurgical causes for MEP deterioration are hypotension below the limit of blood flow autoregulation resulting in ischemia. Hypothermia may decrease axonal transmission, and intracranial air may result in increased stimulus threshold. Also, peripheral nerve conduction failure resulting from nerve compression due to poor positioning has been reported .
Usually pre- and postoperative motor function is classified as normal (no focal motor deficit), slightly paretic (motor deficit not exceeding 4/5 and not significantly impairing the extremity’s function, walking not impaired), severely paretic (motor deficit 3/5 or worse, significantly impaired function of extremity, or inability to walk), and plegic (0/5 or 1/5). This is consistent with the McCormick scale .
The extent of surgical resection is assessed as gross total resection (90% resection or more), subtotal resection (50%–90%), partial resection (<50%) or biopsy based upon the early postoperative MRI.
In a series of 100 consecutive operations of spinal cord tumors, 92 of the 100 patients had a normal or slightly impaired motor status before surgery . In all of these 92 cases, muscle MEPs could be recorded at the beginning of surgery (baseline). D-waves were recordable in 59 of the 86 cases not involving the conus medullaris.
Eight patients had severe motor deficits or were paralyzed preoperatively. None of them had recordable MEPs (neither epidural nor from muscle). In no preoperatively paralyzed extremity was there ever a muscle MEP recordable.
Postoperatively short-term motor status deterioration is noted in about every third patient [35 of 92 (38%) patients in the abovementioned series]. In only 2 of about 250 patients a severe permanent neurological dysfunction occurred as a direct result of the operation. Therefore the risk of paraplegia following resection of a spinal cord tumor is lower than expected.
These changes in clinical status are correctly reflected by the intraoperative MEP findings. This assessment has passed the test of time and has been largely confirmed by later experience and publications .
Electrodes are attached to the patient at the same time as the anesthesia preparations are done. Additional time, if any, required for monitoring preparation should be minimal. Electrodes must be carefully marked and secured when the patient is turned into the prone position to avoid delay and confusion. Baselines are obtained as soon as all electrodes and amplifiers are in place during final surgical preparations and initial incision and dissection. A structured positioning of wires without loops and for avoiding interference is important. Sometimes it may be required to obtain baselines prior to turning to secure a safe neck position. The epidural recording electrodes are placed by the surgeon from the surgical field after laminotomy once the dura is properly exposed and hemostasis achieved. The D-wave electrode is then connected to a preamplifier next to the operating table just outside the sterile field. This must be accomplished in a way that the surgical work is not disturbed. Placing the D-wave electrodes epidurally prior to dural opening is preferable, as the D-wave baseline can be established at this time before direct manipulation of the cord begins. This is significant because sometimes the spinal cord may swell upon dural opening and release of cerebrospinal fluid and neurological compromise may already occur at this stage, and placement of a subdural electrode would not be possible in such a situation. Occasionally fibrotic scar tissue from a previous surgery may prohibit insertion of a recording electrode. From a practical experience, all patients without severe preoperative motor deficits can be monitored with either D-wave or muscle MEPs or both.
The recordings are usually robust, between 10 and 70 µV amplitudes for D-waves and up to 2 mV in muscle MEPs. Changes due to nonsurgical influences, for example, intravenous bolus of anesthetic, temperature or blood pressure changes, can be recognized by following these parameters and closely communicating with the neuro-anesthesiologist.
During removal of intramedullary tumors, muscle MEPs indicate some even minor degree of functional compromise to the motor pathways at some point during the procedure in almost every other patient. In less than one-third, these changes remain until the end of surgery and then correlate to a temporary motor deficit. In the remainder of cases the changes are reversible and correlate to intact motor function when the patient awakes from anesthesia.
Two factors are important for interpretation of intraoperative D-wave recordings: the presence of the D-wave, and, if it is present, its peak-to-peak amplitude.
The presence and monitorability of the D-wave and the intraoperative significant decline of its amplitude have been shown to be of predictive value for long-term motor outcome after intramedullary surgery .
External factors, such as anesthetic changes, scalp edema, intracranial air, or electrode displacement during surgery, can result in amplitude changes. Therefore a cranially placed D-wave electrode provides comparative information of possible reasons for an amplitude reduction ; however, the extra expense of using a second electrode may be carefully weighed.
Amplitude reduction of more than 50% caused by surgical actions, confounding factors excluded, is considered evidence for significant damage to the corticospinal tract . Reduction of final amplitude below 50% of baseline predicts long-term motor deficits, whereas reduction of less that 50% indicates eventual recovery of early weakness.
This concept is well understood for intramedullary surgery and is applied to surgery for intradural–extramedullary tumors and syringomyelia. However, it has been shown to be possibly misleading in surgery for scoliosis correction . This same caveat may apply to surgery for intradural–extramedullary tumors, as their removal may also result in repositioning of the spinal cord vis-à-vis the epidural recording electrode.
Patients in whom no baseline recording for the D-wave can be obtained appear to have a higher risk of postoperative motor deficits than those with a recordable D-wave . Whether this is due to an inherent subclinical damage and “vulnerability” of the motor tract, or to the fact that there was no monitoring support for the surgery, is not known.
The mechanism of an unrecordable D-wave coinciding with intact motor status (and recordable muscle MEPs) is believed to be due to a chronic or inherent preexisting damage to the corticospinal tract resulting in a desynchronization of the wave .
Muscle MEPs are integrative responses of individual motor units. Each motor unit output is nonlinear. If the excitatory postsynaptic potential reaches threshold, a postsynaptic motor unit responds in an all-or-none fashion. Any stimulation below firing threshold results in no motor unit response and thus no response. Increase of muscle MEP amplitude with a set recording electrode position is a result of recruitment of more motor units, which then contribute to the “compound” muscle action potential, which constitutes the MEP ( Fig. 26.1 ).
It appears that this “all-or-nothing” response makes MEP monitoring sensitive to changes because a small reduction of conducting corticospinal fibers can result in a disproportionally large deterioration of MEPs .
Evidence and experience indicate that the presence or absence of MEPs correlates with the presence or absence of clinically relevant motor deficits .
The presence of muscle MEPs indicates intact functional integrity of the corticospinal tract in all instances, independent of the location of the lesion.
Occasionally, in patients with a moderate motor deficit, it may be difficult to obtain recordings from both lower extremities. If that occurs, usually responses in the weaker leg require higher stimulation intensities.
Warning criteria for MEP monitoring are dependent on monitoring circumstances. It is very important to emphasize that for cranial surgery, different criteria must be used than in spinal and spinal cord surgery!
For all circumstances, disappearance of a visible signal at consistent measurement parameters is the major criterion. MEPs can disappear slowly with previous deterioration of amplitudes and increase of threshold or can disappear abruptly. Irreversible disappearance predicts with high probability a temporary or even persistent paralysis or paresis .
If MEPs disappear during surgery, action is taken by the surgeon: irrigation, increase in mean blood pressure, or simply waiting a bit, and beginning dissection at a different location is most often sufficient to let MEPs recover. If MEPs do recover, their presence indicates intact motor control and this correlates with the clinical outcome . If MEPs do not recover in 9 out of 10 cases, a temporary motor deficit will be ensured . At this stage, it must be decided whether or not to continue the surgery. If the D-wave is unchanged, resection may be continued with the knowledge that a reversible motor deficit is likely.
Unilateral MEP loss results in unilateral deficit, which always recovers, a phenomenon described long ago in a different context .
Especially intramedullary dissection for access to intramedullary spinal cord tumors can injure descending and ascending tracts that also influence excitability of the lower motor neuron. This may result in deterioration of amplitude or loss of MEPs, due to inhibition, although the corticospinal tract may remain intact. This is one important reason that D-wave monitoring parallel to MEP monitoring is highly important in such cases .
Reduction of amplitude of 80% is a debated minor warning criterion for spinal cord surgery and a moderate warning sign for spine surgery. Even it may not be useful in intramedullary surgery from a practical perspective, amplitude reduction still indicates some degree of injury to the motor system. Amplitude deterioration of 80%, even if this injury may not reach clinical significance or only reaches it when the response disappears in spite of supramaximal stimulus intensity, must not be ignored in either intra- or extramedullary surgery, as it surely indicates an impending and subclinical damage to the motor system .
The third MEP parameter is threshold elevation. That more current is needed to obtain a response may be due to several reasons, only some of which are related to the surgical dissection. Theoretically the largest neuron has the lowest threshold but also the greatest disposition for injury. Therefore significant threshold elevation (over 100 mA) is seen by some as a sensitive early warning parameter especially for intramedullary spinal cord surgery . But spontaneous and poorly explained increase of threshold during surgery is often observed; hence, false positive warning can occur . The practical neurosurgical experience does point to threshold elevation as an important indicator of impending damage in a similar way as amplitude reduction. Therefore with the objective of finishing the complete resection of a tumor with the best possible function, the best possible MEP preservation is attempted. On the basis of experience, it is therefore recommended to use threshold elevation as a warning sign, and as a trigger to stop dissection, start irrigation, and check the blood pressure, rather than continue until the MEP is lost. As preserved MEPs, regardless of threshold and amplitude indicate preserved function, it makes sense to preserve MEPs and thus be sure that the patient recovers from surgery better and faster and needs no rehabilitation to treat a deficit.
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