6.1 Somatosensory Evoked Potentials

Somatosensory evoked potentials (SSEPs) are a common intraoperative neurophysiological monitoring (IONM) modality utilized in skull base surgery where there is a risk of neurovascular damage. During endoscopic endonasal approach (EEA), ulnar/median nerves from the upper extremities and tibial/peroneal nerves from the lower extremities are stimulated bilaterally via subdermal needle electrodes. Recordings are made along the ascending neural axis from the Erb’s point, cervical spine, and contralateral somatosensory cortex from the scalp (International 10–20 system for scalp recording electrodes). This allows simultaneous assessment of the integrity of peripheral nerves, spinal cord dorsal column tracts, brainstem medial lemniscal pathways, and somatosensory thalamocortical connections. ¹ Alterations in SSEP amplitude and latency have been noted secondary to patient positioning, ischemia/infarction of somatosensory pathways in the cervical spine or medial lemniscal pathways in the brainstem, and/or cortical generators of SSEPs including the somatosensory cortex and thalamus. ² Thus, SSEPs are a sensitive diagnostic tool for the detection of neurovascular damage along the somatosensory pathway during EEA procedures.

While EEA has reduced the morbidity and mortality in pediatric skull base tumor resection relative to conventional open techniques, there is still a risk of vascular damage. Juvenile nasopharyngeal angiofibromas (JNAs), which are highly vascular tumors that are commonly treated via EEA in pediatric patients, carry the risk of significant hemorrhage and cerebral ischemia during resection (▶ Fig. 6.1). Tumors of the clival region, such as chordomas, can compress the brainstem and impair vascular perfusion. ³ SSEP monitoring during resection of such tumors helps identify intraoperative vascular compromise. In studies on adult EEA, SSEP monitoring was found to have positive and negative predictive values of 80% and 99.79%, respectively, in predicting neurological deficits. ² SSEP changes indicative of deficits are manifested as real-time sudden or insidious changes in SSEP waveforms indicating neurological compromise. ²

The parameters of interest in SSEP waveforms during IONM are response amplitude and latency of the cortical and subcortical waveforms. ¹ The American Society of Neurophysiological Monitoring (ASNM) has recommended a 50% decrease in the amplitude and/or 10% increase in the latency of SSEP response as a significant change, which should be communicated to the surgical team as a sign of possible neurological compromise. ⁴ When significant changes in the SSEPs are noted, localization of the cause of change and appropriate surgical maneuvers can be performed to prevent neurological deficits. In our experience from adult EEA, patients who experienced significant changes that were reversed during the procedure had lower chance of neurological deficit. Factors affecting nerve conduction such as nerve fiber diameter, degree of myelination, or synaptogenesis impact SSEP amplitude and latency. ⁵ These factors are in flux during the early years of life and must be considered in the pediatric patient population. Because of these physiological maturational effects, interpretation of baseline data as well as changes in SSEPs during the procedures should be evaluated, taking the factors into consideration.

Cortical and subcortical recordings obtained simultaneously can often differentiate the origin of SSEP changes. For example, cortical ischemia, which can occur secondary to surgical manipulation, manifests as a change in the cortically recorded potential without any major changes in SSEPs at the cervical level. In contrast, a change in patient positioning or perturbation of the surgical environment, such as drilling or dissection, may result in SSEP changes from both recording sites.

Sensitivity of SSEPs to cortical and subcortical ischemia has been well established in animal models. In animal experiments, a decrease in cerebral blood flow (CBF) below 10 to 20 mL/100 g/min has been shown to cause a reversible decrement in the amplitude of SSEP responses. Animal studies also show that an increase in mean arterial pressure (MAP) and, subsequently, CBF restores depressed SSEP amplitudes to normal. ⁶ Similarly, reduction in CBF in humans to approximately 14 mL/100 g/min has been shown to result in a 50% reduction in SSEP amplitude. ⁷ An important concept to understand is that during IONM, disappearance of SSEP responses (electrical failure) occurs before the “ion pump failure” or cellular death. ⁸ Thus, real-time continuous SSEP collection and interpretation during EEA can present situations where the decrease in SSEP amplitude secondary to cerebral ischemia can be reversed by restoration of perfusion prior to the development of significant perioperative neurological injury. ²

To our knowledge, the utility of SSEP recording in pediatric EEA is limited to just one study performed by our group. We have reported the use of SSEP monitoring in 129 pediatric patients who underwent EEA for resection of skull base tumors. ³ SSEP monitoring was conducted as described earlier. ▶ Fig. 6.2 shows example SSEPs obtained from a pediatric patient undergoing EEA skull base surgery. While changes in SSEPs due to anesthesia and changes in MAP were noted preoperatively, no intraoperative SSEP changes were observed in any of the patients. These correlated with absence of postoperative neurological deficits. ³

Given the demonstrated efficacy of SSEPs in adult skull base surgery and its successful execution in the aforementioned pediatric study, SSEPs are likely valuable in pediatric EEA as well. As a method of continuous neurophysiological monitoring, a significant decrease in amplitude and increase in latency can be particularly useful for identifying ischemia-induced damage in somatosensory pathways. However, SSEPs provide no information regarding motor pathways, requiring the need for a multimodality approach to protect descending brainstem pathways from ischemic damage.

6.2 Brainstem Auditory Evoked Potentials

Brainstem auditory evoked potentials (BAEPs) have become a routine component of IONM during skull base surgeries involving manipulation of the brainstem, cochlear nerve, and vertebrobasilar vasculature. BAEPs are recorded from the scalp following the unilateral delivery of auditory stimuli (clicks consisting of 100-μs-long pulses of an 85- to 99-dB intensity delivered at a frequency range of 9.1–17.5 Hz via foam earbuds placed in the external auditory canal). BAEPs monitor the functional integrity of ascending auditory pathways beginning at the distal aspect of the vestibulocochlear nerve, progressing to cochlear nuclei, superior olivary nuclei, the lateral lemniscus, and ending at the inferior colliculi in the midbrain. ⁹ In addition to assessing cochlear nerve conduction, BAEPs are also sensitive to ischemic changes in component structures along these pathways. Further, BAEPs are used to assess the degree of cerebellar retraction and its effects on cochlear nerve function as well as cochlea and brainstem perfusion in the auditory pathways during EEA procedures.

JNAs and clival tumors, which increase susceptibility to vascular injury, warrant the addition of BAEPs during EEA procedures. BAEP monitoring can help identify intraoperative vascular compression and injury by detecting impaired propagation of auditory signals to and through the brainstem. The use of SSEPs and BAEPs together provides a multimodality approach with the monitoring of auditory tracts (by BAEPs) in the brainstem in addition to somatosensory pathways utilizing SSEPs.

Baseline BAEPs should be obtained following the initiation of anesthesia and positioning of the patient but before surgically accessing brainstem structures. The resultant waveform typically consists of five peaks, each corresponding to the distal auditory nerve, proximal auditory nerve, cochlear nucleus, superior olivary complex, and inferior colliculus, respectively. ⁹ Each of these anatomical structures serves as a generator of neuronal activity and allows for localization of ischemia. ▶ Fig. 6.3 shows example BAEP waveforms obtained from a pediatric patient undergoing EEA.

The amplitudes of each peak and the latencies from one peak to the next (interpeak latency) are used in evaluation of BAEP responses. Given that most EEA procedures involve the brainstem at or above the level of the superior olivary sulcus, alterations in amplitude and latency of peak V represent the majority of changes observed. ⁹ In general, surgeons should be informed of changes in BAEP following a consistent decrease in amplitude or increase in latency, as these indicate impaired impulse transmission along auditory neurons. The American Society of Neurophysiological Monitoring (ASNM) recommend alerting the surgeon of a 10% (1-ms) increase in latency and/or a 50% decrease in the amplitude of peak V compared to baseline. ⁴ However, these guidelines are not specific to the pediatric population, and a controlled study is required to establish alarm criteria for pediatric patients.

Similar to SSEPs, vascular compromise is expected to cause alterations in BAEP waveforms. A more distal vascular occlusion in the posterior circulation (e.g., posterior cerebral artery) could result in disappearance of later BAEP peaks, while a proximal vascular occlusion would prevent the auditory stimulus from propagating to the cochlea or cochlear nucleus, resulting in disappearance of all BAEP peaks. Studies in primates have shown that brainstem ischemia, due to reduced brainstem blood flow (12–15 mL/100 g/min), increases the latency of BAEP waveforms. ¹⁰ Similarly, reversible changes in BAEPs correlating with reduction in MAP have also been observed in humans during EEA procedures. ¹ Significant changes in the peak V response during EEA procedures are indicative of neurological compromise due to reduced perfusion or compressive forces. ⁹

Reported use of BAEPs in pediatric EEA procedures is very limited. Our group ³ has described BAEP monitoring in 16 pediatric patients. We noted transient wave V amplitude changes that improved with increases in MAP in two patients, neither of whom developed postoperative deficits. The two cases with changes in BAEPs were both in patients with JNAs. ³ As such, BAEPs can be useful in evaluating the cerebellopontine angle (CPA) structures and brainstem perfusion during EEA.