David B. MacDonald

Safety of intraoperative transcranial electrical stimulation motor evoked potential monitoring

Summary This article reviews intraoperative transcranial electrical stimulation (TES) motor evoked potential (MEP) monitoring safety based on comparison with other clinical and experimental brain stimulation methods and clinical experience in more than 15,000 cases. Comparative analysis indicates that brain damage and kindling are highly unlikely. There have been remarkably few adverse events. Pulse train TES-induced or coincidental seizures (n = 5) are rare, probably because of very brief (<0.03 second) stimuli, anesthesia, and the general absence of predisposing cerebral conditions. Soft bite blocks may prevent tongue or lip laceration (n = 29) or mandibular fracture (n = 1). Rare cardiac arrhythmia (n = 5) and intraoperative awareness (n = 1) may be coincidental. Minor scalp burns (n = 2) are rare. Although possible, no spinal epidural recording electrode complications or injuries resulting from TES-induced movement were found. There have been no recognized adverse neuropsychological effects, headaches, or endocrine disturbances. Comprehensive relative contraindications include epilepsy, cortical lesions, convexity skull defects, raised intracranial pressure, cardiac disease, proconvulsant medications or anesthetics, intracranial electrodes, vascular clips or shunts, and cardiac pacemakers or other implanted biomedical devices. Otherwise unexplained intraoperative seizures and possibly arrhythmias are indications to abort TES. With appropriate precautions in expert hands, the well-established benefits of TES MEP monitoring decidedly outweigh the associated risks.

Intraoperative motor evoked potential monitoring – A position statement by the American Society of Neurophysiological Monitoring

The following intraoperative MEP recommendations can be made on the basis of current evidence and expert opinion: (1) Acquisition and interpretation should be done by qualified personnel. (2) The methods are sufficiently safe using appropriate precautions. (3) MEPs are an established practice option for cortical and subcortical mapping and for monitoring during surgeries risking motor injury in the brain, brainstem, spinal cord or facial nerve. (4) Intravenous anesthesia usually consisting of propofol and opioid is optimal for muscle MEPs. (5) Interpretation should consider limitations and confounding factors. (6) D-wave warning criteria consider amplitude reduction having no confounding factor explanation: >50% for intramedullary spinal cord tumor surgery, and >30-40% for peri-Rolandic surgery. (7) Muscle MEP warning criteria are tailored to the type of surgery and based on deterioration clearly exceeding variability with no confounding factor explanation. Disappearance is always a major criterion. Marked amplitude reduction, acute threshold elevation or morphology simplification could be additional minor or moderate spinal cord monitoring criteria depending on the type of surgery and the programs technique and experience. Major criteria for supratentorial, brainstem or facial nerve monitoring include >50% amplitude reduction when warranted by sufficient preceding response stability. Future advances could modify these recommendations.

Intraoperative facial motor evoked potential monitoring with transcranial electrical stimulation during skull base surgery

OBJECTIVE To address the limitations of standard electromyography (EMG) facial nerve monitoring techniques by exploring the novel application of multi-pulse transcranial electrical stimulation (mpTES) to myogenic facial motor evoked potential (MEP) monitoring. METHODS In 76 patients undergoing skull base surgery, mpTES was delivered through electrodes 1cm anterior to C1 and C2 (M1-M2), C3 and C4 (M3-M4) or C3 or C4 and Cz (M3/M4-Mz), with the anode contralateral to the operative side. Facial MEPs were monitored from the orbicularis oris muscle on the operative side. Distal facial nerve excitation was excluded by the absence of single pulse responses and by onset latency consistent with a central origin. RESULTS M3/M4-Mz mpTES (n=50) reliably produced facial MEPs while M1-M2 (n=18) or M3-M4 (n=8) stimulation produced 6 technical failures. Facial MEPs could be successfully monitored in 21 of 22 patients whose proximal facial nerves were inaccessible to direct stimulation. Using 50, 35 and 0% of baseline amplitude criteria, significant facial deficits were predicted with a sensitivity/specificity of 1.00/0.88, 0.91/0.97 and 0.64/1.00, respectively. CONCLUSIONS Facial MEPs can provide an ongoing surgeon-independent assessment of facial nerve function and predict facial nerve outcome with sufficiently useful accuracy. SIGNIFICANCE This method substantially improves facial nerve monitoring during skull base surgery.

Intraoperative spinal cord monitoring during descending thoracic and thoracoabdominal aneurysm surgery

BACKGROUND Postoperative paraplegia is one of the most dreaded complications after descending thoracic and thoracoabdominal aneurysm surgery. In this study, intraoperative monitoring was applied during resection of descending thoracic and thoracoabdominal aneurysms to detect spinal cord ischemia and help prevent paraplegia. METHODS Fifty-six patients (descending thoracic, 25; thoracoabdominal, 31) were monitored intraoperatively with both motor- (MEP) and somatosensory- (SSEP) evoked potentials. MEPs were elicited with transcranial electrical stimulation and recorded from the spinal epidural space (D wave) or peripheral muscles (myogenic MEP). SSEPs were obtained with median and tibial nerve stimulation. RESULTS A total of 16 patients (28.6%) showed MEP evidence of spinal cord ischemia, only 4 of whom had delayed congruent SSEP changes. In 13 patients (23.2%), ischemic changes in MEPs were reversed by reimplanting segmental arteries or increasing blood flow or blood pressure. None of these 13 patients suffered acute paraplegia regardless of the status of SSEP at the end of the procedure, but 1 of them developed delayed postoperative paraplegia after multisystem failure. Three patients (5.4%) who had persistent loss of MEPs despite of recovery of SSEPs awoke paraplegic. CONCLUSIONS The results demonstrate that compared with SSEP, MEP, especially myogenic MEP, is more sensitive and specific in detection of spinal cord ischemia, and that intraoperative monitoring can indeed help prevent paraplegia.

Neurologic features of horizontal gaze palsy and progressive scoliosis with mutations in ROBO3

Objective: To review the neurologic, neuroradiologic, and electrophysiologic features of autosomal recessive horizontal gaze palsy and progressive scoliosis (HGPPS), a syndrome caused by mutation of the ROBO3 gene on chromosome 11 and associated with defective decussation of certain brainstem neuronal systems. Methods: The authors examined 11 individuals with HGPPS from five genotyped families with HGPPS. Eight individuals had brain MRI, and six had electrophysiologic studies. Results: Horizontal gaze palsy was fully penetrant, present at birth, and total or almost total in all affected individuals. Convergence, ocular alignment, congenital nystagmus, and vertical smooth pursuit defects were variable between individuals. All patients developed progressive scoliosis during early childhood. All appropriately studied patients had hypoplasia of the pons and cerebellar peduncles with both anterior and posterior midline clefts of the pons and medulla and electrophysiologic evidence of ipsilateral corticospinal and dorsal column-medial lemniscus tract innervation. Heterozygotes were unaffected. Conclusions: The major clinical characteristics of horizontal gaze palsy and progressive scoliosis were congenital horizontal gaze palsy and progressive scoliosis with some variability in both ocular motility and degree of scoliosis. The syndrome also includes a distinctive brainstem malformation and defective crossing of some brainstem neuronal pathways.

An approach to intraoperative neurophysiologic monitoring of thoracoabdominal aneurysm surgery

Summary Thoracoabdominal aneurysm surgery carries an approximate 10% risk of intraoperative paraplegia. Abrupt cord ischemia and the confounding effects of systemic alterations and limb or cerebral ischemia challenges neurophysiologic spinal cord monitoring. This investigation sought a rapid differential monitoring approach to predict or help prevent paraplegia. Thirty-one patients were monitored with motor evoked potentials (MEPs) and median and tibial somatosensory evoked potentials (SSEPs). MEPs involved single-pulse transcranial electrical stimulation with D wave recording (n = 16), arm and leg muscle MEPs following multiple-pulse transcranial electrical stimulation (n = 12), or both (n = 3). D wave recordings required averaging, invasive epidural electrode insertion, and produced both false positives and false negatives. Muscle MEPs were instantaneous and reliably sensitive and specific for cord ischemia. Cortical and peripheral nerve SSEPs provided rapid detection of systemic alterations and cerebral or limb ischemia. Cord and subcortical SSEPs required excessive averaging time. In conclusion, bilateral arm and leg muscle MEPs with median and tibial peripheral nerve and cortical SSEPs provide sufficiently rapid detection and differentiation of cord ischemia from confounding factors. There were two predicted intraoperative spinal cord infarctions (6.5%) and nine circumstantial examples of possible contributions to deficit prevention.

Current opinions and recommendations on multimodal intraoperative monitoring during spine surgeries.

With the rapid development of imaging techniques and better understanding of structural and functional pathology of the spine and spinal cord there has been a worldwide increase in the number of spine surgeries performed, particularly in specialized interdisciplinary spine centers. In addition to the congenital and acquired deformities of the spine and relatively rare spinal cord tumors, common degenerative spine disease within the aging general population contributes to a growing number of pathologies with myelopathies. This is important because antecedent myelopathy increases spinal cord risk during surgical treatment. The possibility of having functional neurophysiological assessment during spine and spinal cord surgery was introduced in 1970s by applying somatosensory evoked potentials (SEPs) as well as spinal evoked potentials [15, 21, 32, 33]. Meanwhile these modalities and continuous EMG recording have been enhanced by the addition of corticospinal motor pathway monitoring through the use of motor evoked potentials (MEPs) elicited by transcranial electrical stimulation [3]. The application of multimodal intraoperative monitoring (MIOM) became routine in several spine centers, being documented by publications about the specificity and sensitivity as well as clinical experience and outcome measurements during different spinal surgical procedures [6, 9, 13, 14, 17, 22, 24, 26, 27]. In this supplement on intraoperative monitoring the Spine Center of the Schulthess Clinic presents their experience with the application of MIOM during spine surgery analyzing 1,017 operations in the years 2000–2005. The patients for monitoring were selected out of 11,356 who received spine surgery at the institution during the study period. The indication for each monitoring procedure was discussed and established within the monitoring and surgical team. The detailed analysis of this large patient population resulted in a sensitivity of 89% and specificity of 99%. Sutter et al. [31] conclude that MIOM is an effective method of monitoring the spinal cord functional integrity during spine surgery and therefore can lead to reduction of neurological deficits and consequently improve postoperative results. An independent series of 206 thoracolumbar surgeries also presented in this supplement supports this conclusion [19]. Sala et al. [27] discussed in their recent publication of a historical control study the ethical limitation for performing prospective randomized studies to assess the efficacy of MIOM while clearly documenting that monitoring improves outcome after surgery for intramedullary spinal tumors. The Spine Society of Europe (SSE) supported the development of MIOM by presentations of the results at its annual meetings and organized workshops to stimulate discussion and communication between the spine surgeons and clinical neuroscientists. The SSE has also introduced quality control management in spine surgeries by establishing Spine Tango, a web-based international registry that includes MIOM documentation (http://www.eurospine.org). Other international spine societies such as Scoliosis Research Society presented several original papers on MIOM at the 41st annual meeting in 2006 [2, 5, 23] illustrating its advantages for surgery of adolescent idiopathic and infantile scoliosis. Recently, the International Society of Intraoperative Neurophysiology (ISIN) was founded to stimulate interdisciplinary communication and collaboration between surgeons, neurologists, neurophysiologists and anesthetists (http://www.ptsroma.it/isin). The aim of a first consensus meeting on intraoperative monitoring during spine surgeries in Verona (28 September 2006) was to provide recommendations for the improvement and appropriate application of monitoring techniques during spine surgeries. Experts in the field were invited for a meeting with the support of the European Spine Journal (Max Aebi, MD, Editor-in-chief, Marek Szpalski, MD, Supplement Editor) to summarize the current state-of-the-art and prepare current opinions and recommendations. This consensus statement represents a work in progress and as with all other recommendations or proposals, it must be updated as new information is gained.

Tibial somatosensory evoked potential intraoperative monitoring: Recommendations based on signal to noise ratio analysis of popliteal fossa, optimized P37, standard P37, and P31 potentials

OBJECTIVE To compare the intraoperative signal-to-noise ratio (SNR), reproducibility and rapidity of popliteal fossa (PF), optimized P37, standard P37 and P31 potentials. METHODS Raw sweeps and 11 averages doubling sweep number from 2 to 2048 were compared in 37 patients undergoing scoliosis surgery. Optimized (highest amplitude or SNR) P37 derivations were Cz-CPc (22), CPz-CPc (27), Pz-CPc (7), iCPi-CPc (8), CPi-CPc (1), Cz-Pz (2) or Pz-FPz (3), and in two patients with non-decussation, Cz-CPi (1) or CPz-CPi (3). Standard P37 and P31 derivations were CPz-FPz and FPz-C5S. Signal amplitude was measured in 2048-sweep averages; peak noise was measured in raw sweeps and +/- averages; SNR was amplitude/noise. Visual superimposability and < 20-30% amplitude variation determined reproducibility. Sweeps to reproducibility determined rapidity. RESULTS The SNR order was PF >> optimized P37 > standard P37 > P31. Mean optimized P37 SNR advantages over the standard P37 and P31 were 2.1:1 and 4.9:1. SNR had powerful non-linear correlations to reproducibility and rapidity. Median sweeps to reproducibility were PF: 2, optimized P37: 128, standard P37: 512 and P31: 1024. EEG noise was greatest in FPz derivations. Burst-suppression increased scalp potential SNR and rapidity. CONCLUSIONS Optimized P37 and PF recordings are most rapidly reproducible due to superior SNRs and are recommended. FPz should be avoided. Burst-suppression may be desirable. SIGNIFICANCE CPz-FPz and FPz-C5S should no longer be standard.

Utility of motor evoked potentials for intraoperative nerve root monitoring.

Summary There is no entirely satisfactory way to monitor nerve root integrity during spinal surgery. In particular, standard free-running electromyography carries a high false-positive rate and some false-negative rate of injury. Stimulated electromyography to direct root stimulation can only be done intermittently, and roots are often inaccessible. This article reviews to what extent muscle motor evoked potential (MEP) monitoring might help. It presents background considerations, describes MEP methodology, and summarizes relevant experimental animal and clinical studies. Based on current evidence, root compromise can cause myotomal MEP deterioration that in some cases may be reversible. However, because of radicular overlap, limited sampling, confounding factors, and response variability, the effects range from no appreciable change to variable degrees of amplitude reduction to disappearance and some false-positive and false-negative results should be expected. For root monitoring, multichannel MEP recordings should span adjacent myotomes and avoid mixed myotome derivations. Only amplitude reduction warning criteria have been studied, but no percentage cutoff consensus has emerged, and this approach is troubled by response variability. There is some evidence that MEPs might reduce false electromyographic results. In conclusion, muscle MEPs could compliment electromyography but seem unlikely to completely solve the problem of nerve root monitoring.

ACNS Guideline: Transcranial Electrical Stimulation Motor Evoked Potential Monitoring.

Motor evoked potentials (MEPs) are electrical signals recorded from neural tissue or muscle after activation of central motor pathways. They complement other clinical neurophysiology techniques, such as somatosensory evoked potentials (SEPs), in the assessment of the nervous system, especially during intraoperative neurophysiologic monitoring (IONM). Somatosensory evoked potentials directly assess only a part of the spinal cord, the dorsal columns (Emerson, 1988), and also the medial lemniscus, the thalamocortical radiations, and somatosensory cortex. Because they provide indirect surveillance of the motor tracts, their use has been shown to improve neurologic outcomes during spinal surgery (Nuwer et al., 1995). However, SEPs can fail to detect damage to the spinal cord motor pathways when the dorsal columns are spared (Ben-David et al., 1987; Ginsburg et al., 1985; Jones et al., 2003; Krieger et al., 1992; Legatt et al., 2014; Zornow et al., 1990); this led to the development of techniques for directly monitoring the central motor pathways. Most often, this is accomplished using transcranial electrical stimulation (TES) of the brain and recording of evoked neural or myogenic activity caudal to the area that is at risk during surgery (Legatt, 2002). During TES, high-intensity stimuli must be delivered to the scalp to stimulate the brain through the intact skull, with stimulus voltage and current levels far above those used to elicit SEPs. If a craniotomy permits direct stimulation of motor cortex by electrodes placed on the brain surface, low-intensity direct cortical stimulation can also be used to elicit MEPs for IONM (Szelényi et al., 2007b; Taniguchi et al., 1993). Direct cortical stimulation is outside the scope of this guideline, but the recommendations herein for the recording of the MEPs that are elicited by transcranial electrical brain stimulation would also apply to recording of MEPs elicited by direct cortical stimulation. Transcranial magnetic stimulation has also been used to elicit MEPs by inducing electrical current flows within the brain tissue without passing large amounts of current through the scalp. This reduces stimulation of pain fibers in the scalp, skull, and meninges and makes it a practical technique for MEP studies in awake subjects (Chen et al., 2008). However, transcranial magnetic stimulation is not the optimal MEP technique for IONM because of the anesthetic suppression of transcranial magnetic stimulation– MEPs which are generated mainly by eliciting I-waves (see section on Definitions and Physiology, below) and difficulties in maintaining a constant position of the coil relative to the patient’s head (Legatt, 2004). Neither TES with single stimulus pulses nor transcranial magnetic stimulation consistently produces robust myogenic MEPs suitable for IONM. The commercial availability of stimulators that can deliver trains of high-intensity electrical pulses has made reliable MEP monitoring using TES possible in most patients. At this time, the techniques for recording and interpreting TES-MEPs have become sufficiently well established to warrant the formulation of these guidelines. Personnel performing TES-MEP monitoring must be cognizant of the technical challenges and risks of the technique.