Pediatric Anesthesia ISSN 1155-5645

REVIEW ARTICLE

Intraoperative neurophysiological monitoring in pediatric neurosurgery Veronica O. Busso & John J. McAuliffe Department of Anesthesiology, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

Keywords intraoperative neurophysiological monitoring; motor evoked potentials; somatosensory evoked potentials; auditory brainstem evoked response; electromyography; corticospinal tract Correspondence John J. McAuliffe, Department of Anesthesiology, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Ave, Cincinnati, 45229 OH, USA Email: [email protected]

Summary The use of intraoperative neurophysiological monitoring (IONM) in pediatric neurosurgery is not new; however, its application to a wider range of procedures is a relatively new development. The purpose of this article is to review the physiology underlying the commonly employed IONM modalities and to describe their application to a subset of pediatric neurosurgical procedures.

Section Editor: Sulpicio Soriano Accepted 10 April 2014 doi:10.1111/pan.12431

Background The use of intraoperative neurophysiological monitoring (IONM) in children was first described in 1979 (1) just 2 years after the first descriptions of the use of somatosensory evoked potentials (SSEPs) in adult spine surgery (2). Within 10 years of the adoption of SSEPs as a means to monitor scoliosis surgery, it was noted that postoperative deficits could occur despite unchanged SSEPs (3). In response, motor evoked potentials were introduced allowing assessment of the integrity of the large-diameter corticospinal tract (CST) axons and the alpha-motor neurons (aMNs). SSEPs, motor evoked potentials (MEPs), and electromyography are the main modalities used to monitor children undergoing certain neurosurgical procedures (4). The principle IONM modalities used for pediatric cases are SSEPs, transcranial MEPs, free-running and triggered electromyography (EMG), auditory brainstem evoked responses (ABR), direct cortical, and subcortical, stimulation (DCS, DsCS), and electroencephalography (EEG). In general, these modalities rely on transduction of time-locked signals through mono- or 690

polysynaptic pathways. All have some, possibly minimal, susceptibility to the effects of anesthetic agents. Volatile agents have the greatest impact, while the intravenous agents have less deleterious effects or may even enhance certain potentials, as in the case of etomidate. MEPs are the most susceptible to anesthetic effects, SSEPs are intermediate, and while the ABRs and EMG are resistant to anesthetic effects, neuromuscular blocking agents (NMBs) will ablate the MEPs and EMG but may improve the quality of SSEPs and ABRs by eliminating EMG artifact. Commonly used anesthetic agents and their effects on the common IONM modalities are summarized in Table 1 (5–12). The application of IONM to pediatric neurosurgical cases poses special problems. Infants and toddlers are neurologically immature; examples of this immaturity include incomplete myelination, reduced conduction velocities, and fewer monosynaptic connections between the corticospinal tract and alpha-motor neurons (13–17). These and other factors make obtaining intraoperative neurophysiological data challenging and contribute to extreme sensitivity of motor evoked potentials to volatile anesthetic agents in infants and toddlers. © 2014 John Wiley & Sons Ltd Pediatric Anesthesia 24 (2014) 690–697

V.O. Busso and J.J. McAuliffe

Pediatric IONM

Table 1 Anesthetic agents and their effects on IONM modalities SSEP (cortical) Desflurane Sevoflurane Propofol Etomidate Ketamine Dexmeditomidine Remi/Sufentanil NMBs

DDA/DDL DDA/DDL DDA/DDL LDE LDE NSE NSE NSEa

SSEP (p/sc)

TcMEP

ABR

EMG

NSE NSE NSE NSE NSE NSE NSE

DDAb DDAc DDAd LDE LDE DDA NSE DDAe

NSE NSE NSE NSE NSE NSE NSE

NSE NSE NSE NSE NSE NSE NSE DDAf

a

a

ABR, auditory brainstem evoked responses; DDA, dose-dependent depression of amplitude; DDL, dose-dependent increase in latency; LDE, low doses enhance amplitude (minimal effect on latency); NSE, no significant effect in clinically used doses; SSEP, somatosensory evoked potentials. a May improve signal quality by eliminating EMG artifact. b Effects significant above 0.5 MAC in older children. c Effects greater than desfluane; very low concentrations can ablate MEPs in children under 4 years of age. d Effects less than volatile agents, but bolus dosing or high blood levels will attenuate MEP amplitude. e Ideally avoided when obtaining TcMEPs, especially in young children. f To be avoided when performing CN EMG, especially CN VII.

As maturation proceeds, the sensitivity to anesthetics approaches that seen in young, healthy adults. The presence of comorbidities and genetic disease can also have a dramatic impact on the ability to acquire IONM data and the sensitivity to anesthetic agents. These same genetic conditions may also limit the choice of anesthetic techniques, adding to the challenge of acquiring IONM data. To understand the roll of IONM in pediatric neurosurgical procedures, it is necessary to have a basic appreciation for the origin of the potentials and the limitations of each modality used by the IONM team. To this end, a brief description of the commonly used modalities follows. Somatosensory evoked potentials Somatosensory evoked potentials are produced when mixed peripheral nerves are stimulated with brief pulses of current. The current needs to be sufficient to depolarize the large sensory fibers that transmit proprioception. The impulses move through the brachial (or sacral) plexus, the dorsal root entry zone, ascend in the ipsilateral dorsal column to the gracile (lower extremity) or cuneate (upper extremity) nucleus, cross the midline as the arcuate fibers, and travel in the medial lemniscus to the ventral posterior lateral thalamic tier and then to the primary sensory cortex. The stimulus and recording © 2014 John Wiley & Sons Ltd Pediatric Anesthesia 24 (2014) 690–697

windows are time locked to facilitate recording a signal. The typical cortical SSEP amplitude is on the order of a microvolt, against a background EEG signal, with an amplitude on the order of tens of microvolts. Signal averaging is also used to improve signal-to-noise ratio (18,19). The most commonly used nerves for stimulation are the ulnar, median, and posterior tibial nerves. Recording sites for ulnar or median nerve stimulation include Erb’s point, the fifth cervical spine, and three cephalic locations designated by their international 10– 20 nomenclature as Fz, C3’ and C4’. The electrodes at these recording sites can be montaged in different ways so that a standard set of active-reference electrode pairs are used to record signals. The signals will have a characteristic appearance depending on the montage used. A series of median nerve SSEPs are shown in Figure 1a, and the posterior tibial nerve SSEPs are shown in Figure 1b. The latency of each recorded peak has a characteristic time of appearance following the stimulus. Latency is a function of conduction velocity, length of the pathway, and number of synapses present; therefore, factors such as age, development, height, temperature, and anesthesia can affect latency. Peripheral and ‘subcortical’ latencies and amplitudes are generally insensitive to anesthesia effects, while the cortical latencies and amplitudes are affected by anesthetics. Transcranial motor evoked potentials Transcranial motor evoked potentials (TcMEPs) are recordings obtained from muscle groups in response to a train of electrical pulses flowing between two electrodes placed in the scalp overlying the motor cortex. (Figure 2) A single electrical pulse can elicit a motor response in an awake patient, but a train of pulses is necessary when general anesthetics are used. The pulses depolarize the largest axons of the CST, resulting in a series of D-waves. The axon may depolarize at the hillock or as deep in the brain as the pyramidal decussation depending on the stimulating voltage. In addition, there is a cortical response producing I-waves. A single transcranial pulse will produce a D-wave under anesthesia but not I-waves; multiple pulses are needed for I-wave production under anesthesia. Both the D- and I-waves travel down the large-diameter CST fibers to the aMNs. The aMNs will depolarize if the D- and I-waves generate sufficient excitatory postsynaptic potentials (EPSPs) to reach firing threshold (20,21). Anesthetics affect TcMEPs at multiple levels including suppression of I-wave generation, depression of aMN resting membrane potential, and reduction of 691

Pediatric IONM

V.O. Busso and J.J. McAuliffe

(a)

Figure 1 Somatosensory evoked potentials (SSEPs). (a) Ulnar Nerve SSEPs: Five different montages (or derivations) are shown with the latencies of significant peaks marked. The latencies indicate the time from stimulus to different points along the dorsal column sensory pathway from the brachial plexus (peripheral) to the primary sensory cortex. The signals were recorded from a 6-year-old presenting for spinal fusion. (b) Posterior tibial nerve SSEPs. The image displays three cortical montages, a cervical montage and a peripheral montage

EPSP voltage. The choice of anesthetic can affect the likelihood of a false-positive result, that is, predicting neurological deficit when none is present (22). In the case of infants, there are additional affects due to suppression of synaptic transmission between the CST fibers and the aMNs due to the small number of monosynaptic connections as well as poorly synchronized Dwaves (23). In general, infants and toddlers require greater delivered charge to obtain TcMEPs than adolescents as well as different stimulation protocols (24–26). Motor evoked potentials can also be obtained by directly stimulating the primary motor cortex. The stimulating conditions used are very different than used for transcranial stimulation as the resistance of the scalp, skull, and dura is absent. Direct cortical stimulation also results in activation of single or closely associated muscles as opposed to multiple muscles activated with transcranial stimulation (27,28). It is also possible to map motor tracts subcortically by eliciting motor evoked potentials by directly stimulating the CST axons in the white matter. There is a direct correlation between the stimulating current in milliamps and the distance between the stimulus and the CST. Thus, low stimulating currents are associated with proximity to the CST and potential for injury to motor pathways during resection of tumors or vascular malformations (29–31). 692

(b)

(recorded at the popliteal fossa). Each of the three cervical montages represents an (approximately) orthogonal orientation to the other two. This allows the orientation of the dipole generating the cortical potential to be determined. The cervical signal is useful because changes in the amplitude and latency of the cervical potential are very unlikely to be mediated by changes in the anesthetic management, whereas the cortical potentials are sensitive to changes in anesthesia. The peripheral potential confirms antegrade conduction of the stimulus.

Auditory brain stem responses Auditory brainstem evoked responses (ABRs) are typically divided into short-, medium-, and long-latency responses. The only relevant responses under anesthesia are the short-latency responses. The short-latency responses are known by their designation as waves I–V. These responses are thought to represent the activation of the distal cochlea (wave I), proximal cochlea (wave II), the cochlear nucleus (wave III), origin of lateral lemniscus (putative, but uncertain, origin of wave IV), and the entry of lateral lemniscus into the inferior colliculus (wave V). A repetitive click is presented to one ear and a masking noise to the other ear. The responses are recorded from the vertex with an earlobe or mastoid reference. The normal latencies are very short; the typical time window for recording is 10 ms. The ABRs are very low-amplitude signals in a high-voltage EEG background; thus, timelocking to stimulus and signal averaging is essential. It may be necessary to average as many as 2–4000 sweeps to achieve an adequate signal:noise ratio (32–34). In addition to a measure of auditory nerve function, the ABRs can be used as a surrogate marker for brainstem perfusion as waves III–V will decrease in amplitude with poor brainstem perfusion. Waves III–V can also be affected by retraction on the brainstem that causes stretch of the auditory nerve (35). © 2014 John Wiley & Sons Ltd Pediatric Anesthesia 24 (2014) 690–697

V.O. Busso and J.J. McAuliffe

Pediatric IONM

(a)

(b)

Figure 2 Motor evoked potentials. Motor evoked potentials from a 9-month-old elicited using two different trains of pulses separated by a 12-ms interval: (a) the responses from muscle groups on the left side of the body and (b) the responses from muscle groups on the right side of the body. The double-train methodology is frequently successful in eliciting MEPs from children 50% of baseline D-wave amplitude is associated with temporary neurological deficits; however, if the D-wave drops to 50% of baseline allows the surgeon to achieve a more complete resection than if guided by TcMEPs alone (49). Resection of intracranial tumors Intracranial tumors may lie in or near areas of the brain that are involved in the generation of the potentials measured by one or more IONM modalities. In other cases, the tumor may be in a region away from motor or sensory pathways, but the vascular supply of the motor or sensory cortex may be at risk of compromise during resection. IONM may be helpful in these two scenarios. Changes in cortical SSEPs in the absence of changes in the peripheral or cervical montages are potentially significant during intracranial surgery. Stable levels of anesthesia are highly desirable to avoid confusing anesthesia effects (which are generally bilateral and symmetric) with surgical causes of cortical SSEP changes (frequently but not always unilateral). The stimulation parameters used to obtain TcMEPs must be adjusted to avoid excessive stimulation that can result in false

Figure 4 D-wave Monitoring. A D-wave can be elicited from a single transcranial pulse as shown. The recorded D-wave is dwarfed by the stimulus artifact but is present and can be used to assess conduction in large CST fibers. Special filter settings are required in order to minimize the stimulus artifact. The fast latency (

Intraoperative neurophysiological monitoring in pediatric neurosurgery.

The use of intraoperative neurophysiological monitoring (IONM) in pediatric neurosurgery is not new; however, its application to a wider range of proc...
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