Chapter 11 Electrodiagnostic Evaluation of Spinal Tumors
DIAGNOSTIC UTILITY OF ELECTROPHYSIOLOGY IN SPINAL TUMORS
Spinal cord tumors account for 15% of central nervous system neoplasms.1 The initial symptoms of spinal cord tumors may be vague 2 with patients presenting with myelopathies or radiculopathies. Thus, many of these patients may first be evaluated by neurologists. Even though physical examination provides useful information with regard to localization and etiology, non-invasive tests such as somatosensory evoked potentials (SSEPs), motor evoked potentials (MEPs), electromyography (EMG), or nerve conduction studies (NCS) may provide useful anatomical or physiological information. Practically, though, magnetic resonance imaging (MRI) is the diagnostic study of choice in the assessment of myelopathy and radiculopathy.3 This chapter will review the usefulness of electrodiagnostic testing in the assessment of spinal tumors and its application as a monitoring tool in the operating room.
TYPES OF ELECTRODIAGNOSTIC TECHNIQUES
Evoked Potentials
Evoked potentials (EPs) reflect a visual representation of multiple averages of sensory or electrical signals resulting from the stimulation of the nervous system. EPs that may be useful in the electrodiagnostic evaluation of patients with spinal tumors include SSEPs and MEPs. The advantages of EPs are that they are objective, can be more sensitive than a detailed neurological exam, and can be performed in an unconscious patient. However, disadvantages of EPs are that they are not disease specific and vary based on age, height, and the presence of comorbid disease (e.g., peripheral neuropathy).4 MRI has largely replaced EPs in the diagnostic evaluation of spinal tumors.
Somatosensory Evoked Potentials
SSEPs reflect the function of the somatosensory pathways. This is accomplished through the stimulation of a peripheral nerve—typically the median nerve at the wrist and the posterior tibial nerve at the ankle—to the point of muscle twitch. Electrical potentials generated by this stimulation can then be recorded at various points along the neural pathway, such as Erb’s point after a mixed peripheral nerve stimulation in the upper extremity and in the popliteal fossa after lower extremity stimulation at the ankle. These sensory-generated electrical volleys then orthodromically enter the spinal cord through dorsal roots at several levels. Typically, an EP recorded over the posterior neck can be recorded at a latency of approximately 13 ms after upper limb stimulation and 22 ms after lower limb stimulation. These volleys ascend in the axons of the white matter dorsal column pathways where they synapse in the medulla at the nucleus cuneatus and nucleus gracilis (for the upper and lower limbs, respectively).5,6 From here these second-order neurons cross the midline and ascend as the medial lemniscus where they terminate in the thalamus. Third-order neurons project to the primary somatosensory cortex of the parietal lobe where they can be recorded. The upper limb cortical SSEP occurs at a typical latency of 20 ms and is recorded as a negative potential. The lower limb SSEP occurs at a typical latency of 37 ms and is recorded as a positive potential.
Dermatomal Somatosensory Evoked Potentials
SSEPs record the responses elicited by stimulation of mixed motor and sensory nerves that are mediated by several cervical or lumbosacral nerve roots. Thus, they may be normal despite nerve root compromise, given that their abnormal function may be masked by the normal function of the other nerve roots comprising the nerve.7
To test the function of an individual sensory nerve root, dermatomal somatosensory evoked potentials (DSSEPs) can be recorded. The sensory dermatomes resulting from dorsal (sensory) nerve root innervation of the skin can be recorded by direct dermatomal electrical stimulation of the skin surface with surface electrodes and recorded as DSSEPs.7 Surface electrodes are placed over the dermatomal areas to be monitored and electrically stimulated, thus generating DSSEPs from that particular dermatome. The stimulation and recording parameters used are the same as those for SSEPs.
Practically, though, the reliability of DSSEPs in the diagnostic evaluation of patients with suspected radiculopathies is questionable.8,9 A report of the American Academy of Neurology’s Therapeutics and Technology Assessments Subcommittee recommended that the currently available evidence is insufficient to determine the appropriateness of DSSEPs. As a result, they should be regarded as investigational only.10
Transcranial Magnetic Stimulation
MEPs can be used to evaluate the functional integrity of the corticospinal tract system from the brain to the spinal cord or muscle. This can be accomplished by either magnetic or electric stimulation of the brain. However, in the awake patient only transcranial magnetic stimulation (TMS) is done because the transcranial electric motor evoked potentials (TcEMEPs) induce a current in the brain through a large stimulus that would activate pain fibers within the scalp and thus would not be tolerated by an awake patient.6
Magnetic activation of the corticospinal pathway can be accomplished by the placement of a magnetic coil that is held close to the patient’s head. This induces high-intensity current pulses within the patient’s brain, which stimulates the neurons of the cerebral cortex. This stimulation produces multiple D (direct) waves that are the result of multiple action potentials within the descending pyramidal tract neurons. After this initial D wave are I (indirect) waves, which are the result of synaptic activation of further pyramidal neurons via interneurons. Because the currents produced by magnets are predominantly tangential, I waves are the predominant WAVEFORM produced.6 Because TMS produces predominantly I waves, which are the result of synaptic activity within the cortex interneurons, it cannot be used in the anesthetized patient. Because anesthetics predominantly take effect at synapses, the I waves would be lost and, hence, there would be no recordable MEPs under general anesthesia.
These I waves must then synaptically transmit their impulses to the alpha motor neurons in the spinal cord, then to the peripheral motor nerve, and finally across the neuromuscular junction to muscle where compound muscle action potentials (CMAPs) can be recorded. Firing of the alpha motor neuron requires the temporal summation of multiple excitatory postsynaptic potentials. This can be accomplished by the multiple I waves elicited by a single transcranial magnetic stimulus.6
Because these I waves depend on cortical synaptic function, they can be lost with cortical lesions.6 However, for the evaluation of motor function resulting from lesions below the cortex (e.g., the descending axons in the spinal cord), this technique may still be useful when the spinal cord is the region to be assessed.
NERVE CONDUCTION STUDIES AND ELECTROMYOGRAPHY
Nerve Conduction Studies
NCS involve the electrical activation of nerves to provide functional assessment about the peripheral nervous system in the form of conduction and axonal integrity. They may provide diagnostic, descriptive, or prognostic information and are accomplished through the application of a depolarizing square wave electrical pulse over a peripheral nerve, which results in activation of both the sensory and motor axons of the mixed nerve. A nerve action potential is propagated, which can be recorded at a particular distance over the nerve, as well as a CMAP, which can be recorded over the target muscle. Components such as conduction velocity, amplitude, and shape are assessed. This is typically done with surface electrodes. Because peripheral nerves contain fibers of differing diameters, degrees of myelination, and amount of sensory or motor connections, NCS are designed to assess the fastest 20% of these fibers.11
H Waves
The H wave is the electrical representation of a monosynaptic spinal reflex. It assesses the S1 nerve root, as it is only consistently obtained from recording the gastrocnemius-soleus muscles after stimulation of the tibial nerve in the popliteal fossa. It is the EMG equivalent of the ankle deep tendon reflex. The amplitude can be compared with the contralateral side. It is beneficial in that it assesses the function of the sensory root fibers, including the segment proximal to the dorsal root ganglion (DRG). However, it can sometimes be normal in S1 radiculopathies, and its abnormality cannot always be attributed to the radiculopathy. It also can be abnormal in polyneuropathy cases and in patients older than 60 years.12
F Waves
F waves are a type of late motor response that may be able to be used to evaluate the motor nerve root. F waves are recorded from muscle after maximal stimulation of its nerve. When a motor nerve axon is stimulated, the action potential propagates in both directions so that an orthodromic potential can be directly recorded in muscle as a CMAP and an antidromic potential conducts proximally to the anterior horn cell. About 2% of axons then backfire, leading to a small additional orthodromic potential that can be recorded in muscle after the CMAP as an F wave. However, because a different population of anterior horn cells backfires with each stimulus, the F waves are variable in size, shape, and latency and are usually less than 5% of the CMAP amplitude.11,12
F waves initially were thought to be able to assess proximal nerve motor root segments inaccessible by conventional NCS. However, they have been found to be insensitive to this. The nerves stimulated contain innervation from usually more than one root, and they are mediated along a pathway that extends muscle, nerve, root, plexus, and spinal cord; thus, an abnormality anywhere along this pathway could lead to an abnormal F wave.12 When abnormal, they often offer little extra information, except in specific situations such as Guillain-Barré syndrome.
There is an exception in which both H waves and F waves may be clinically useful. In the case of an acute myelopathy, both F waves and H waves may disappear during the acute phase of spinal shock only to reappear thereafter.13
Needle Electromyography
EMG records the electrical activity in muscles. This is done by the insertion of a monopolar or concentric needle into a muscle and recording the observed and corresponding auditory response of spontaneous and recruited activity. It is used to differentiate myopathic from neurogenic disease and, by determining the distribution of neurogenic abnormalities, can localize the site of a lesion, such as differentiating nerve from plexus from radicular lesions.14,15
APPLICATION TO TUMORS
Myelopathy
Somatosensory Evoked Potentials
SSEPs can be used in the clinical diagnosis of neurological disease, in particular for multiple sclerosis.5 They may reveal dysfunction in the dorsal column/medial lemniscal thalamocortical sensory pathway or reveal subclinical involvement, help to define the anatomical involvement of a lesion, or be used to monitor a patient’s status over time.4 Even though SSEPs have been shown to be sensitive in detecting abnormalities in patients with intraspinal neoplasms, this technique is not as sensitive in detecting these tumors as MRI is.1
Motor Evoked Potentials
TMS can be used to measure central motor conduction time. Pyramidal tract dysfunction will result in slowing of central motor conduction time. MEPs are most often used in the assessment of multiple sclerosis or amyotrophic lateral sclerosis, conditions in which evidence of corticospinal tract involvement that may not be clinically evident is sought.14
For spinal cord lesions for which the predominant injury is demyelination leading to slowing of central motor conduction time, TMS can be useful in assessing the level of functional impairment. Through appropriate muscle sampling, the level of the lesion can be localized to a particular root.14
Radiculopathy
Dermatomal Somatosensory Evoked Potentials and Electromyography
Radiculopathies are usually caused by root compression. They are the most common cause of referral to the EMG laboratory.12 EMG has been shown to be of great utility and has been used in the evaluation of radiculopathies for more than 50 years.12
There are 31 pairs of spinal nerves attached to the spinal cord by dorsal (sensory) and ventral (motor) roots. The ventral roots originate from cells in the anterior and lateral gray columns of the cord; the dorsal roots originate from the DRG, which lie distal to the cord. Thus, sensory NCS, which do not assess the sensory roots proximal to the DRG, remain unchanged in radiculopathies. The dorsal and ventral roots join to form spinal nerves.12
The region of skin with sensory innervation from a single dorsal root constitutes a dermatome. The muscles that share innervation from a single ventral root constitute a myotome. Most muscles are made up of more than one myotome. Sensory fiber compromise alone is the most common clinical presentation of radiculopathies. Isolated motor dysfunction is the least common.12
However, in most patients with signs and symptoms of radiculopathy, the most efficient diagnostic test is MRI. Even though electrodiagnostic studies cannot provide an etiology, localization of the involved myotome can be detected by EMG.16
Although there are reports of DSSEPs being sensitive to changes in nerve root function,17 their value in diagnosing radiculopathy is questionable.8 For the detection of radiculopathies, EMG is more sensitive than DSSEPs.12 In the case of radiculopathies caused by spinal neoplasms, EMG may show early signs of denervation in the paraspinal musculature.18,19
Conus Medullaris
The conus medullaris comprises the S2–5 nerve roots. Intrinsic spinal cord tumors that invade the conus typically do so caudally, beginning with the S5 root. This leads to the usual presenting symptoms of dull pain with paresthesias in the perianal and genital regions followed by sphincter disturbance or impotence. As the lesion spreads rostrally, the ankle jerks may be lost. If the symptoms are initially unilateral, they will quickly spread to involve the contralateral side.20
EMG evaluation of conus medullaris lesions will often indicate bilateral and multiple radiculopathies. Anal sphincter EMG may show evidence of denervation. NCS may reveal abnormal motor potentials, but sensory nerve action potentials should be normal because the lesion is preganglionic.20
SSEPs may reveal abnormalities after lower extremity stimulation because the ascending dorsal column pathways are affected by the lesion. Similarly, TMS may be abnormal if the descending corticospinal tract is affected. However, these findings, too, would be limited to the lower extremities.20
Cauda Equina
Extramedullary spinal cord tumors below the level of the spinal cord can lead to a cauda equina syndrome. Depending on the affected nerve roots, the patient will typically present with pain, paresthesia, weakness, or diminished reflexes in an asymmetric radicular distribution. If the lesion compresses the cord, then upper motor neuron signs may appear. These lesions resemble conus medullaris lesions except that the distribution is more asymmetric, the pain is often more severe, and the sacral and lumbar roots will be affected.20
EMG is helpful in showing evidence of denervation involving the lumbar and sacral levels in an asymmetric radicular distribution. The paraspinal muscles and sphincter muscles also may be affected. NCS may reveal an asymmetric, side-to-side difference in amplitude of CMAPs. Sensory conduction studies will again be normal.20
INTRAOPERATIVE NEUROPHYSIOLOGICAL MONITORING OF SPINAL TUMORS
Why Use Monitoring?
The use of continuous intraoperative SSEP monitoring in one study was found to reduce the incidence of neurological injury in cervical surgery from 3.7% to 0%. This was likely a result, in part, of the early detection of vascular or mechanical compromise of the spinal cord or nerve roots and the subsequent rapid response in anesthesia or surgical management.21
The risk of postoperative paraplegia or paraparesis after scoliosis surgery is 0.72%.22 Nuwer et al23 performed a large multicenter survey in 1995 to compare SSEP changes to neurological function after scoliosis surgery. Out of 51,263 surgeries, they found a false negative rate of 0.063% and a false positive rate of 1.51%. However, their survey also included cases in which intervention by the surgeon may have occurred based on the changes in the SSEPs. There was a true negative rate of 97.4% and a true positive rate of 0.423%. Based on these findings, the sensitivity of SSEPs in scoliosis surgery was calculated to be 92%, the specificity 98.9%, the negative predictive value 99.33%, and the positive predictive value only 42%. Based on these findings, Nuwer et al concluded that SSEPs detected more than 90% of potential deficits. The factors that appeared to most affect the rate of new neurological deficits included the experience of the surgeon and the surgeon’s and technologist’s experience with SSEP monitoring.23
Intraoperative neurophysiological monitoring (IOM) can be used to monitor intramedullary1,2 and extramedullary,24 primary, or metastatic tumors.25 Intramedullary tumors are rare, and the majority are histologically benign.2 Thus, their radical removal will improve long-term survival with an acceptable morbidity.26 IOM techniques can aid in the degree of aggressiveness of tumor resection.
Occasional false positive cases have been reported in which there is a significant change in the EPs but no new postoperative neurological deficit. These cases could be the result of prompt surgical intervention or the sensitive detection of a subtle clinical change by the monitoring procedure. False negative cases also have been reported in the absence of EP changes. These possibly could be a result of delayed onset in symptomatology from effects such as latent vascular change or compression exacerbated by patient movement.27
Monitoring Techniques
Somatosensory Evoked Potentials
Electrophysiological monitoring of the spinal cord during surgery, which may carry a risk of spinal cord compromise, has been described for more than 30 years.28 SSEPs initially were used to provide warning of impending spinal cord compromise and to supplement the wake-up test to assess spinal cord function. SSEPs continue to be the most widely used monitoring modality.7 In particular, SSEP monitoring alone has been shown to improve neurological outcome after spinal surgery.23
Technical Aspects
Stimulation
SSEPs monitor the functional status of the somatosensory pathways.29 Stimulating electrodes are placed over the median or ulnar nerve at the wrist for upper extremity SSEPs and posterior tibial nerve at the ankle or peroneal nerve at the knee for lower extremity SSEPs. For median nerve stimulation, which encompasses the nerve roots originating from levels C6–T1, the anode is placed at the palmar crease and the cathode is placed between the palmaris longus and flexor carpi radialis tendons, 2–3 cm proximal to the anode to avoid “anodal block.”7 To assess the lower cervical spinal roots (C8–T1), the ulnar nerve is preferentially stimulated with the anode at the wrist crease on either side of the flexor carpi ulnaris tendon, 2–3 cm distal to the cathode. The superficial radial nerve at the wrist and the ulnar nerve at the elbow are other potential sites of stimulation.7 For posterior tibial nerve stimulation, the cathode is placed between the medial malleolus and the Achilles tendon, 2–3 cm proximal to the anode. For peroneal SSEPs, the common peroneal nerve is stimulated in the popliteal fossa, medial to the biceps femoris tendon with the cathode below the crease, 2–3 cm proximal to the anode. Posterior tibial nerves are the preferred SSEPs of the lower extremity because they are larger, less variable, produce smaller muscle contractions, are more easily accessible, and provide a peripheral response at the knee.
Contact impedance is limited to 5 kOhms or less. To reduce stimulus artifact, a ground electrode is placed on the stimulated limb. Either a constant voltage or a constant current stimulator is used. Constant current stimulators can compensate for changes in contact resistance; however, this is limited by the maximum output voltage of the stimulator. Alternatively, constant voltage stimulators will provide a constant stimulus intensity only if the contact resistance remains constant. Thus, constant current simulators are recommended. Monophasic rectangular pulse waves with a typical pulse duration of 100–300 μsec at a rate between 2–5 Hz should be given. Stimulus rates that are exact subharmonics of line frequency (60 Hz in North America) should be avoided (e.g., 6 Hz). Lower extremity stimulation rates between 1.5–3 Hz may improve the responses. Increasing the stimulus rate to greater than 5 Hz for the lower extremities and greater than 9 Hz for the upper extremities often degrades the cortical responses. Supramaximal stimulus intensity to more than the motor threshold should be used, though usually it should not be necessary to exceed 50 mA.5,7
Recording
Either needle electrodes or standard electroencephalographic disc electrodes are applied with either paste or collodion. If disc electrodes are used, collodion is preferred in the operating room setting because of its durability. Impedances are kept at less than 5 kOhms. A system bandpass with low frequency filters of 30 Hz and high frequency filters of 3 kHz are used.5 These filters optimize noise rejection while retaining the SSEP characteristics.27 The number of average sweeps required is usually between 300–500. However, this number depends on the signal-to-noise ratio and the time required to obtain a response. For example, at a stimulus rate of 4.7 Hz, it would take about 1 minute to acquire 300 sweeps. During temporary vessel occlusion, this amount of time may need to be reduced, thus acquiring fewer samples. However, to ensure that the responses are real and not artifact, verifying by repetition or odd and even averaging can be done.7
The time bases to acquire and display the SSEPs are usually set at approximately 50 ms for the upper extremities and 100 ms for the lower extremities. These values are based on the typical latencies for the peaks of interest (i.e., approximately 20 ms for the upper extremity and approximately 40 ms for the lower extremity). Factors such as age and size of the patient also need to be taken into account.7
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