Introduction
Endoscopic surgery of the cranial base is frequently utilized for pathologies such as pituitary adenoma, craniopharyngioma, chordoma, and chondrosarcoma. Such operations involve working in close proximity to critical neurovascular structures. Insult to these vital structures can result in postoperative neurological deficits that drastically impact the patient’s quality of life. It becomes imperative for the neurosurgeon to not only perform optimum resection of the lesion but also preserve the structural and functional integrity of surrounding neurovascular structures.
Cranial nerves are routinely encountered during cranial base surgeries. They are delicate, meandering, and lack an epineurium; factors that make them susceptible to injury. Intraoperative neurophysiologic monitoring of cranial nerves enables the surgeon to confidently operate on offending lesions with continuous feedback on the integrity of cranial nerves. Depending on the location of the lesion and the cranial nerves involved, the choice of neuromonitoring techniques can vary. Here we present discussions of neuromonitoring techniques most commonly used in endoscopic endonasal skull base surgery. Particular focus will be made on the use of triggered and free-running electromyography (EMG) of extraocular muscles for lesions around the cavernous sinus and superior orbital fissure.
Neuromonitoring Modalities
Electromyography (EMG)
EMG was first used intraoperatively in the 1960s for the monitoring of facial nerve function during exploratory parotid surgery. During endoscopic skull base surgery, EMG can be used for monitoring of any cranial nerve with motor function including cranial nerves III-VII and X-XII. The pathologies involving the cavernous sinus and/or superior orbital fissure often threaten cranial nerves III, IV, & VI. They are monitored by performing an EMG of the extraocular muscles. Because of their relative frequency of use in endoscopic skull base surgery, EMG monitoring of the extraocular muscles will be a particular focus of this chapter. For transclival approaches to prepontine or cerebellopontine angle pathologies, the facial nerve, vagal nerve, accessory nerve, and hypoglossal nerve may additionally be monitored. The functional status of the facial nerve is monitored by recording EMG of the orbicularis oris and orbicularis oculi muscles. Similarly for the monitoring of glossopharyngeal, vagus, accessory, and hypoglossal nerves, EMGs of stylopharyngeus, laryngeal muscles, trapezius, and tongue are recorded, respectively.
Two types of EMG activity are recorded: free running and triggered EMG. Free running EMG continuously records the motor unit potentials (MUP) of the muscle fibers. It has high specificity and negative predictive value regarding postoperative cranial nerve deficits. This provides some degree of confidence to the surgeon that these cranial nerves are not being disrupted during tumor exposure and removal. Based on the amplitude and frequency of discharges, the free running EMG signals can be classified into spikes, bursts, trains and neurotonic discharges. A single MUP wave is called a “spike.” A short chain of MUPs firing at 30–100 Hz and less than 200 ms in duration is called a “burst.” When a persistent chain of MUPs is recorded, it is referred to as a “train.” Bursts and spikes are typically triggered by touching, rubbing, or other mechanical manipulations of the nerve with no correlation to nerve injury. Trains are elicited by mechanical stimuli, saline irrigation, and possibly nerve ischemia
The neurotonic discharges are of primary interest to the neuromonitoring technician. They were first described in the 1980s and are defined as a train of MUPs at high frequency (> 30 Hz) recorded from a muscle in response to mechanical or metabolic stimulation. Since neurotonic discharges are triggered by mechanical stimulation of motor axons, they act as sensitive indicators of nerve injury. But absence of neurotonic discharges doesn’t necessarily exclude nerve injury and presence of neurotonic discharge doesn’t always signify nerve injury. Sharp transection of a nerve elicits negligible neurotonic discharges as compared to mechanical irritation or manipulation. The signal voltage is set between 50 and 200 μV, the frequency filter between 30 Hz to 20 kHz, and the sweep speed is at 100 ms per division for recording the responses.
Triggered EMG activity is seen when the cranial nerve is electrically stimulated. This leads to recording of compound muscle action potentials (CMAPs) from the muscle fibers. Triggered EMGs are needed to check the integrity of peripheral motor axons. CMAPs can be produced by either bipolar or monopolar stimulation. In bipolar stimulation both the cathode and anode are directly on the nerve, which reduces current spread to adjacent nerves leading to localized flow of current. But the localized flow of current may lead to submaximal stimulation if fluid causes current shunting. In monopolar stimulation the cathode is directly on the nerve and the anode is kept away from the nerve by at least several centimeters. This lowers the chances of current shunting but increases the probability of activating nearby neural structures by current spread. Nevertheless, monopolar stimulation is mostly preferred as it is easier to use in confined spaces of the brain. A current of very low intensity (0–2 mA) and duration (0.05– 0.1 ms) is typically used for cranial nerve stimulation during surgery. Higher intensities may be needed if the nerve is less responsive due to damage, insulated by tissue or fluid, or at a distance from the stimulating electrodes. Intensities stronger than 5 mA can spread and lead to unintended activation of nerves. The anesthetic regimen has to be optimized before recording intraoperative EMG. After the induction of anesthesia, muscle relaxants (e.g., vecuronium or pancuronium) are ceased once intubation has been performed, and a train of four should be performed to confirm absence of physiologic muscle relaxant.
Somatosensory Evoked Potentials (SSEP)
Intraoperative monitoring of somatosensory evoked potentials (SSEPs) is one of the most commonly used modalities for predicting and preventing postoperative neurological deficits. SSEPs have been reported to detect the presence of cortical ischemia during cerebrovascular procedures, and their utility during skull base procedures is well recognized. In endoscopic skull base surgery, SSEPs are most commonly utilized when working very closely on the carotid artery. In the event of a carotid artery injury, SSEPs can notify the surgeon if cerebral ischemia is occurring during use of temporary clipping or if too much packing or compression has been performed. SSEPs monitor the integrity of the spinal cord dorsal columns, medial lemniscus pathways to the thalamus, and its connections to the primary sensory cortex by detecting a stimulus—administered to a peripheral nerve—at the somatosensory cortex.
After the induction of anesthesia, baseline SSEPs are recorded. It can be recorded prior to patient positioning or after positioning when lateral, three-quarter, or prone positioning is used. Recording baseline before positioning is preferable, as pressure on the brachial plexus or peripheral nervous system can be detected and corrected. For upper extremity SSEP recording, bilateral stimulation of the median or ulnar nerve is performed in an alternate fashion at the wrist with a pair of subdermal needle electrodes. For the lower extremities, bilateral alternate stimulation of the tibial nerve is performed. In case one cannot elicit a reliable tibial nerve response, the peroneal nerve can be stimulated. The stimulation of the tibial nerve is performed by a pair of subdermal needle electrodes placed at the medial malleolus of the ankle with a proximal cathode and distal anode separated by a gap of 1 cm. The stimulation of the peroneal nerve is carried out by a pair of subdermal needle electrodes placed at the head of the fibula and medially in the popliteal fossa.
The SSEPs resulting from the stimulation of ulnar or median nerves are recorded by P4/Fz and P3/Fz scalp electrodes (cortical) and a cervical electrode localized at the C7 spinous process (subcortical) and referenced to Fz. The SSEPs resulting from the stimulation of peroneal or tibial nerve are recorded by Pz/Fz and P4/P3 scalp electrodes, and a cervical electrode is localized at the C7 spinous process and referenced to Fz. Band-pass filters set at 30 to 300 Hz are used for cortical recordings, and band-pass filters set at 30 to 1000 Hz are used for subcortical (cervical) recordings. The alarm threshold is a sustained 50% decrease in primary somatosensory cortical amplitude or an increase in response latency by > 10% from baseline. Changes in amplitude or latency of SSEPs in > 2 averaged trials qualify as sustained changes. SSEPs have certain limitations including their inability to detect subcortical ischemia and lack of information about the integrity of motor pathways.
Brainstem Auditory Evoked Potentials (BAEP)
BAEPs were first described by Jewett and Williston in 1971 and have increasingly assumed an important role in modern neurosurgery. BAEPs are more commonly used in lateral skull base surgery for posterior fossa lesions such as meningiomas, vestibular schwannomas, and microvascular decompression for hemifacial spasm and trigeminal neuralgia. Intraoperative monitoring of brainstem auditory evoked potentials (BAEPs) has greatly reduced the risk of hearing loss during the aforementioned surgeries. BAEP is used much less commonly in endoscopic skull base surgery. The normal BAEP in humans comprises seven vertex positive submicrovolt waves originating within 10 milliseconds of an auditory stimulus. The first five components of the BAEP are designated waves I through V, out of which wave V is of primary interest for monitoring BAEPs. After induction of anesthesia and positioning the patient, the baseline BAEP is established. The right and left ears are independently stimulated throughout the surgery by delivering a click stimulus of 85 decibels (dB). The rate of the click stimulus is 17.5 Hz. White noise of 65 dB hearing level is applied to the contralateral ear. The observation duration is 12 milliseconds, averaging at least 256 responses. Subdermal needle electrodes are used for BAEP recording and are inserted at vertex to left ear mastoid (Cz/A1); vertex to right ear mastoid (Cz/A2); and vertex to cervical C2 (Cz/Cv2). The amplifier bandpass is 100 to 1000 Hz. The alarm criteria that mandate warning to the surgeon are > 50% decrease in wave V amplitude or prolongation of wave V latency to 0.5 or 1.0 millisecond. Loss of wave V is usually synonymous with postoperative hearing loss. BAEP has been shown to be a reliable and effective modality to prevent postoperative hearing loss.
Visual Evoked Potentials (VEP)
Endoscopic skull base surgeries often involve exploration and dissection around the optic nerve, chiasm, and tracts. Common pathologies that occur adjacent to the optic nerves include pituitary adenomas, craniopharyngiomas, and tuberculum sella meningiomas. Due to close proximity, many patients with these pathologies present with visual disturbances. Although the goal of surgery is visual preservation and restoration, there is a real risk of new or worsened postoperative visual impairment. Thus an important goal of the surgery is to also prevent postoperative visual deterioration. Intraoperative monitoring of visual evoked potentials (VEPs) was designed as a way to try and monitor optic function during surgeries around the cisternal and intracanalicular segments of the optic nerve and the optic chiasm and tracts.
Intraoperative monitoring of VEPs was pioneered in the 1970s and has been through refinements and critical evaluations. Although its use has increased among some centers, overall its use is uncommon due to concerns about reliability. Prior to the recording of VEPs, total intravenous anesthesia is induced and maintained throughout the surgery. The technical aspects of the anesthetic regimen have been laid out by Wiedemayer et al . Flash VEPs have been recommended as the best method for the intraoperative monitoring of VEPs. Once the anesthesia is induced, the closed eyes are covered with transparent eye patches. Then the light-stimulating device is placed on the eyelids and they are covered with another transparent eye patch. Obviously, the setup of VEP precludes its use in transorbital surgery. The light stimulating device is usually an array of high-luminosity LEDs (light-emitting diodes) set in goggles or soft round silicone discs. The color of the LEDs can have an influence on the recordings. The red LEDs stimulate only the cones of the macula whereas using white LEDs will stimulate both rods and cones, thus leading to larger activation of optic pathways and occipital cortex and enabling more comprehensive neuromonitoring. The electrodes for measurement of VEPs are needle electrodes that are placed subcutaneously at Oz, O1, O2, and the ground electrodes are placed subcutaneously in the mastoid process bilaterally (A1 and A2). These locations are according to the international 10/20 EEG system. Band pass filters of 2 to 500 Hz are employed and can be streamlined according to the stimulation artifact. The LEDs deliver a stimulus at the rate of 1 Hz with each stimulus having duration of 8 msec to 20 msec. The signals are averaged over typically 50 to 100 sweeps to record a single VEP. Braiding of the recording wires improves the signal-to-noise ratios of recordings and maintenance of interhemispheric symmetry with reference to electrode impedance (≤ 5 kΩ) and ensures a better quality of recordings. A decrease in amplitude from baseline by 50% or more initiates the alarm. Appearance of these signs alert the surgeon to potential functional damage to the optic pathways. A limitation of using the cutoff of 50% decrease in amplitude is that though it can detect postoperative hemianopsia, it frequently cannot detect a new quadrantanopsia. This can be overcome by redefining the alarm criteria as “reproducible and permanent change of 20% or more” in the amplitude of the baseline. A major factor that limits the use of VEPs for predicting postoperative visual impairment is that its response varies with stimulus delivery and the anesthetic regimen used.
Extraocular Muscle Monitoring
Anatomy
The extraocular muscles comprise the superior oblique, inferior oblique, and four rectus muscles. As the periorbita thickens posteriorly, it gives rise to the common tendinous ring or the annulus of Zinn. It is this annulus that serves as the origin of the four rectus muscles. The superior oblique also arises from this ring, but it loops via the trochlea on the medial side of the orbital roof before terminating on the globe. The extraocular muscles are supplied by three cranial nerves: oculomotor (CN III), trochlear (CN IV), and abducens (CN VI). The oculomotor nerve is a pure motor nerve that arises from the rostral midbrain near the cerebral peduncle and innervates all the extraocular muscles except the superior oblique and lateral rectus and also supplies the sphincter pupillae and ciliary muscles. The trochlear nerve is the thinnest and longest cranial nerve, and the only cranial nerve to originate from the dorsum of the brainstem. It arises immediately lateral to the inferior colliculus and then exits on the contralateral side, coursing around the cerebral peduncle, and ends in the superior oblique muscle. The abducens nerve arises from the pontomedullary sulcus and supplies the lateral rectus. Since these nerves are purely motor, free running EMG for monitoring plus direct stimulation is the preferred intraoperative monitoring (IOM) technique.
Intraoperative Technique
There are three types of electrodes that are used to record EMG activity: surface, subcutaneous, or intramuscular. Surface and subcutaneous electrodes are generally not preferred because these electrodes do not come in close contact with the muscle fibers and thus miss out on many distant MUPs (motor unit potentials). Intramuscular electrodes are the electrodes of choice. They are of two types: needle electrodes and ring electrodes. Ring electrodes are cumbersome as well as more invasive to use, as they need to be sutured epiconjunctivally to the corresponding muscle while a surgical adhesive tape robustly secures its other ends. They are also limited by lower-specificity EMG recordings. For intraoperative monitoring, the needle electrodes are inserted into the superior rectus/inferior rectus (CN III), superior oblique (CN IV), and lateral rectus (CN VI) muscles, and the signals are recorded ( Figure 40.1 ). Before placing electrodes, a corneal eye shield with ophthalmic ointment are first placed. The needle electrodes are placed in the direction of their targets through the eyelid while simultaneously displacing the globe in the opposite direction with the contralateral hand. A reference electrode can be placed near the vertex. The recording and interpretation is performed as described in the section on EMG.
