• Users Online: 101
  • Print this page
  • Email this page


 
 
Table of Contents
REVIEW ARTICLE
Year : 2021  |  Volume : 4  |  Issue : 3  |  Page : 147-163

Intraoperative electrophysiological principles in neurooncological practice


1 Department of Neurosurgery, Yashoda Hospital, Secunderabad, Telangana, India
2 Department of Neuro-anaesthesia, Yashoda Hospital, Secunderabad, Telangana, India
3 Associate Staff Physician Anaesthesiologist, Anaesthesiology Institute, Cleveland Clinic, Abu Dhabi, UAE

Date of Web Publication02-Nov-2021

Correspondence Address:
Dr. Anandh Balasubramaniam
Department of Neurosurgery, Yashoda Hospitals, Alexander Road, Shivaji Nagar, Secunderabad - 500 003, Telangana
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/IJNO.IJNO_421_21

Rights and Permissions
  Abstract 


Intraoperative neurophysiological monitoring (IOMN) is an important adjunct in modern day neurosurgical practice. There has been a paradigm shift from functional preservation to maximal safe or total excision of a tumor along with functional preservation, aiming for a better quality of life to the patients. In neurosurgery, like in any other specialty, we have two extremes of tumors, benign and malignant. In malignant tumors, the extent of resection, along with molecular genetics of the tumor, play an important role in the survival of patients. Thus, one should target for complete resection, whenever feasible, in these types of tumors. In benign tumors, such as World Health Organisation (WHO) grade 2 gliomas, a good chance of long-term survival exists. IOMN is a valuable adjunct in neurosurgical practice that guides the surgeon and warns him/her of the important neurological structures in the vicinity, during surgery. The IOMN procedures, however, have their own limitations that everyone should be aware of. The technique has been used along with other adjuncts like a preoperative MRI (including the functional magnetic resonance imaging [MRI], diffusion tensor imaging of long tracts and perfusion studies), neuronavigation and intraoperative imaging to maximize the chances of a better outcome in the form of onco-functional balance. In this review, an overview of IONM has been discussed.

Keywords: Neuro-electrophysiology, intraoperative neurophysiological monitoring, neurooncology, brain tumors, surgery


How to cite this article:
Kumar G K, Pradeep K, Rajesh B J, Bhaire VS, Manohar N, Balasubramaniam A. Intraoperative electrophysiological principles in neurooncological practice. Int J Neurooncol 2021;4, Suppl S1:147-63

How to cite this URL:
Kumar G K, Pradeep K, Rajesh B J, Bhaire VS, Manohar N, Balasubramaniam A. Intraoperative electrophysiological principles in neurooncological practice. Int J Neurooncol [serial online] 2021 [cited 2021 Nov 27];4, Suppl S1:147-63. Available from: https://www.Internationaljneurooncology.com/text.asp?2021/4/3/147/329816




  Introduction Top


Maximal safe resection has become the gold standard in neurooncological surgery. This is done by utilizing a plethora of armamentarium to address preoperative, intraoperative and postoperative aspects. This article emphasizes the use of intraoperative neurophysiological monitoring (IONM). The most relevant oncological impact, both in terms of the amount of tissue removal and the functional preservation, could be achieved by the introduction of the brain mapping and monitoring techniques. The basic principle in functional guided neurosurgery is that before structural damage occurs, there will be alterations in physiology that can be rectified in a time-reversible fashion.

From the conventional brain organization of 'eloquence and dominance', there is a gradual shift to a global phenomenon inspired by the works on 'parcellation and connectomics'. Both these terms emphasize the concept that all parts of the brain, including the cortical and subcortical white matter, are important. However, it is beyond the scope of this article to describe the principles of IONM in entirety, and hence, the conventional concepts of IONM with an overview of the evolving concepts are described.

This article describes in a concise manner, the various modalities, their applications and flaws with a focus on practical issues of the most relevant and frequently performed IONM procedures. Some insights regarding the electrophysiological basis of stimulation and recordings, and techniques such as electromyography (EMG), electroencephalogram (EEG) and electrocorticogram (ECoG), evoked potentials including somato-sensory (SSEPs), auditory (BAEPs), visual (VEPs) and motor (MEPs), as well as stimulated EMG are provided.

Current concepts of IONM in functional neuro-oncology

The function-based surgical resection should be performed up to the individual functional boundaries, at both cortical and subcortical levels. The concept of detecting and preserving the essential functional cortical and subcortical structures according to functional boundaries is called as the “functional neuro-oncological approach”. Thus, there is a gradual shift from image-based surgery to function-based surgery. The functional approach exploits the functional reorganization of brain, permitting the removal of as much tumor as feasible, possibly extending the resection far beyond the visible tumor margins and detectable by conventional MR images, while preserving functional integrity.[1],[2]

Optimizing the onco-functional balance indicates that the extent of resection (EOR) will depend on whether or not neural circuits critical for brain functions are involved by the tumor.[3] When functionally possible, a complete supratotal resection is currently recommended.[4],[5] Neurophysiological monitoring can be broadly categorized into two groups, mapping and monitoring.[6],[7] Both these methodologies overlap in clinical practice and are used at different instances during surgery. The main difference between these two basic techniques is the duration of study, its objective and the inference derived by the surgeon from the results.

Functional mapping consists of topographic assessment of the cortical and subcortical structures to determine their function.[8] It also helps to understand the electrical activity (such as the seizure focus) in and around the lesion. Mapping is usually stopped as soon as the function is positively identified. This functional identification may include a positive effect (that is, eliciting a function) or a negative effect (that is, suppressing a function). Mapping helps to identify the functional area and its relationship to tumor, thereby allowing surgeons to identify the site of incision and to restrict the extent of surgery from the functional areas. The positive sites need to be marked and labelled. The two most important areas that need to be mapped on the cortex are the sensori-motor and language areas.

The main principle of functional monitoring is to perform surveillance of the functional state of structures. As these areas need to be monitored throughout surgery, the procedure takes a longer time, in contrast to the functional mapping procedure.[8] The former procedure also needs more expertise and commitment from the anesthetist, the neurophysiologist and the surgeon. Hence, the objective of functional monitoring is not just monitoring, but also involves mapping all through the surgery to preserve the functional integrity of structures in close vicinity that are likely to be compromised during the surgical procedure.


  IONM in Neuro-Oncological Tumors Top


Various types of IONM modalities are explained in [Figure 1]. Each of the modalities has been explained in brief and its application in the excision of neurooncological tumors has been defined[9],[10],[11],[12],[13],[14],[15],[16],[17] in [Table 1]. The stimulation and recording parameters with the alarm criteria of each of these modalities have been explained in [Table 2]. International standard 10-20 montages are utilized for cortical surface IONM [Figure 2].[18]
Figure 1: Intraoperative neurophysiological modalities

Click here to view
Table 1: Intraoperative neurophysiological monitoring modalities in relation to tumors

Click here to view
Table 2: Intraoperative neurophysiological monitoring modalities, parameters, and alarm criteria

Click here to view
Figure 2: Diagrammatic representation of the international standard 10-20 montage for stimulation and recording electrodes Fz (blue) for reference; C3', C4', Cz' (green) for stimulating MEP; C3, C4, Cz (orange) for recording SSEP; O1, O2, Oz (yellow) for recording VEP

Click here to view


Free running response

Electrocorticogram (ECoG)

Electrocorticogram is a measure of the electrical activity of the brain measured from the cortex. It can be done by using surface (strip or grid electrode) or depth electrodes. In neuro-oncological practice, it is used in tumors associated with seizures. Epileptogenic activity is noted in and around the tumor area. After tumor resection, the electrodes are placed again and electrical activity of the cortical region is recorded for at least for 5 minutes to confirm the completeness of resection of the epileptogenic foci. Apart from the ECoG, an electroencephalogram (EEG) can also be used to measure the depth of anesthesia, monitor the intraoperative seizure activity, and also assess for ischemic insults in the form of slowing of electrical waves.[19]

Free running electromyogram (EMG)

Free running EMG consists of continuous recording of the muscle activity without any stimulation. The corresponding muscle groups, chosen on the basis of the nerve root at risk, are continuously monitored and any mechanical irritation occurring during the resection can be recorded. EMG spikes, bursts, trains, and neurotonic discharges are used to alert the surgeon during tumor resection, regarding an impending neurological deficit caused by the surgical intervention [Figure 3].
Figure 3: Raw EMG. Blue arrow showing EMG bursts

Click here to view


Evoked potentials

Somatosensory evoked potentials (SSEP)

SSEPs are used to continuously monitor the integrity of large fiber sensory system, which constitutes the dorsal column (within the spinal cord), dorsal spinocerebellar tract (within the brainstem), the ventrolateral tract (within the subcortex) and the post-central gyrus (within the cortex) [Figure 4]. Stickers or needle electrodes placed over the peripheral nerves (median, ulnar, posterior tibial, or trigeminal nerve) are stimulated and the evoked potentials are recorded over the cervical spine and scalp through corkscrew electrodes. SSEPs are altered during damage in the pathway due to vascular compromise, compression, stretching, edema, inhalational anesthetics, hypothermia, acidosis and hypotension. It is not affected by muscle relaxation and total intravenous anesthesia (TIVA).[11],[12],[17],[20],[21].
Figure 4: SSEP of both upper and lower limbs; blue line shows latency, and orange line the amplitude

Click here to view


Visual evoked potential (VEP)

Visual evoked potentials are obtained using light stimulation (using a light emitting diode [LED]) through the retina, and the response is recorded from the occipital cortex, to monitor the excision of tumors that are involving the visual pathway, such as suprasellar and anterior skull base tumors. An electroretinogram (ERG) is recorded simultaneously with a VEP to ascertain that the flash stimuli to the retina has been adequately delivered [Figure 5]. Inability to identify the laterality, lack of a standard alarm criteria, non-reproducibility of the procedure, and a high anesthetic sensitivity, are some of the drawbacks of this modality. [22],[23]
Figure 5: VEP: Blue arrow shows P100 in the visual evoked potential waveform; and, orange arrow shows the electroretinogram, in a patient with anterior skull base tumor

Click here to view


Brainstem auditory evoked potentials (BAEP)

Brainstem auditory evoked potentials are obtained by applying sounds or clicks over the external auditory meatus and the response recorded from vertex. This brief auditory stimulus can assess conduction through the auditory pathway up to the midbrain. It comprises of 5 waves in 10 millisec, waves I to V. Parameters such as amplitude, interpeak latency, amplitude ratio of the V/I, or IV and V/I, and the inter-ear peak differences and interpeak latencies (I-V, I-III and III–V latencies) are commonly measured. While the main advantage of BAEP is that the waves are resistant to anesthetic agents, it does have a lot of disadvantages, such as, the presence of complex wave forms, the difficult interpretation, and the interference induced in them during surgical drilling and cauterization. [11],[12],[17],[20],[21],[24],[25]

Central sulcus mapping

Phase reversal is the technique used to identify the central sulcus electro-physiologically [Figure 6]. A change in polarity occurs across the central sulcus, when SSEPs are recorded directly on the cortex and when a strip or grid electrode is placed perpendicularly across the central sulcus. Though the lesions or its oedema distorts the anatomy, this technique allows for a precise assessment of functional-anatomic relationship. This modality can be used to preserve eloquence while operating on lesions around the central sulcus. [26],[27]
Figure 6: Phase reversal for central sulcus mapping marked by red circle peak and trough, from 2 and 3 contact points of strip electrodes, respectively, placed across the central sulcus with posterior tibial nerve stimulation

Click here to view


Dorsal column mapping

Inability to identify the neurophysiological midline while operating on an intramedullary spinal cord tumors, cord edema, cord rotation, or due to displacement of tracts, can be overcome using this modality. Bilateral posterior tibial nerves are stimulated and recorded over the width of spinal cord at the level of lesion. Physiological midline is the point in between the two highest amplitude waveforms obtained from a miniature strip electrode[28],[29],[30],[31].

Motor evoked potential (MEP)

MEPs are used to assess the integrity of corticospinal tract, triggered by transcranial electrical or magnetic stimulation [Figure 7] and [Figure 8]. Transcranial magnetic stimulation is very susceptible to anesthetics, thus transcranial electrical stimulation is used for intraoperative neuromonitoring. A constant electrical current is delivered transcranially (using corkscrew electrode: tcMEP); using direct cortical stimulation (using strip electrode: dcMEP); or, subcortically (using monopolar electrode: scMEP). This depolarizes the lateral corticospinal tract and action potentials are recorded from distal muscle groups. This modality can be used for spinal cord, supratentorial and infratentorial tumors. Direct cortical and subcortical stimuli use current intensity upto a maximum of 25mA, avoiding the deeper stimulation of motor tracts. This technique is useful for mapping motor tracts at the precentral gyrus, internal capsule, brainstem and spinal cord. Corticobulbar MEPs are used to monitor the functional integrity of the corticobulbar tract as well as the cranial nerves. In order to avoid stimulating nerves surrounding the tumor directly, which can happen when using a single train stimulus, a double train stimulus with a low current is given (so that the electricity is not dispersed).
Figure 7: Normal bilateral lower limb MEP

Click here to view
Figure 8: Blue arrow shows the corticobulbar MEP of lower cranial nerves in the cerebellopontine angle and brainstem tumors

Click here to view


D Wave

Epidural MEP or D wave is used to assess the integrity of the corticospinal tract [Figure 9]. Transcranial stimulation of the motor cortex elicits a response in the descending motor tract recorded from the surface of spinal cord through an electrode placed in the epidural or subdural space. The amplitude of D wave depends on the thickness of the corticospinal tract; hence, it is less reliable at the lumbar region. The disadvantages of D wave are that it does not have a laterality and is unreliable below the thoracic 10 level. One can proceed with surgery using D wave recording without using MEP, as D waves are more specific and resistant to inhalational anesthetics (as they do not involve synapses). While resecting spinal cord tumors, the D wave above the lesion is taken as a reference wave.[32],[33],[34],[35],[36],[37],[38].
Figure 9: Blue arrow shows the D wave in a patient with a thoracic intramedullary spinal cord tumor

Click here to view


Cortical and subcortical mapping

This modality is used during surgery for superficial cortical and subcortical tumors involving eloquent areas and the speech area. Speech mapping needs to be done in an awake state, while motor mapping can be done in both the awake state as well as general anesthesia. A constant current using a monopolar, bipolar or strip electrode placed over the cortex is delivered for mapping the motor area. A suction stimulator is used simultaneously to stimulate motor tracts while performing tumor resection in the subcortical area. Based on Coulomb's law, the rule of thumb is that with a 1 mA stimulation, the current spreads to a 1mm distance. Thus, one can assess the approximate distance of the surgical site from the vital structures using this technique. Certain disadvantages of this stimulation are the shock-like sensations that may be felt, a lack of cooperation by the subject, the occurrence of fatigue, exhaustion, or seizures, and the false alarms raised due to the subject's inability to perform the given tasks. During general anesthesia, motor mapping can done using the EMG recording over the respective muscle group; however, there is a high chance of negative mapping if all the muscle groups are not used for EMG recording.[39],[40],[41],[42],[43],[44],[45],[46],[47]

Triggered EMG

Current applied directly on the cranial motor nuclei or on the cranial nerve elicits a response in the corresponding muscle group. Monopolar probe stimulation is very sensitive, hence, it is used for identifying regional neural structures during tumor decompression; while bipolar probe stimulation is very specific and is used for identifying the precise location of neural structures, for example, stimulating on a fibre-like structure after tumour decompression [Figure 10]. It is used to assess the integrity, course and mapping of nerve roots and cranial nerves in the vicinity of tumors in areas such as the cerebellopontine angle and the brainstem.
Figure 10: Blue arrow shows triggered EMG of the facial nerve with 2.7mA current in a patient with a cerebellopontine angle tumor

Click here to view


Reflexes

This modality can continuously monitor the function of peripheral nerves, the plexi, and the nerve roots.

Bulbocavernous reflex (BCR) indicate the patency of the lower sacral reflex arc (S2, 3, 4 nerve roots). It is elicited by stimulating the dorsal nerve of penis/clitoris and recording the reflex in the external anal sphincter. A unilateral stimulation results in the elicitation of bilateral BCR reflexes. It can be used for real-time monitoring during excision of spinal cord tumors involving the sacral roots, during detethering of the cord [Figure 11]. The lacunae in literature of proper protocols, the limited data available, and the lack of standard alarm criteria, are the drawbacks of this modality.[48],[49]
Figure 11: Blue arrow shows bilateral bulbocavernous reflex (BCR) with raw EMG with unilateral stimulation of dorsal nerve of penis/clitoris

Click here to view


Blink reflex can monitor the integrity of the brainstem reflex arc with the sensory component of the reflex arc being the trigeminal nerve, and the motor component being the facial nerve. It is elicited by stimulating the supraorbital nerve to elicit a response in the orbicularis oculi muscle. This modality can be used during the resection of intrinsic brainstem lesions and cerebellopontine angle tumors.[50]

Laryngeal adductor reflex is the most crucial among all brainstem reflexes. It protects the airway from aspiration by adducting the vocal cords and by closing the laryngeal inlet. This modality can be used for brainstem tumors and cerebellopontine angle tumors.[51],[52],[53],[54],[55]

Masseter reflex is a trigemino-trigeminal reflex, which connects the midbrain and mid-pons. Unilateral stimulation of the masseter nerve causes jaw jerk. This modality can be during the excision of intra-axial brainstem tumors.[56],[57]


  Anesthesia and IONM Top


Inhalational anesthetics cause a dose-dependent increase in latency, and a decrease in amplitude by inhibiting the spinal motor neurons at the anterior grey column or by depressing the synaptic transmission in the cortex. A minimal alveolar concentration (MAC) value of more than 0.5 affects all evoked potentials. D waves are resistant to inhalational anesthetics as there are no synapses between the stimulating and recording electrodes. Intravenous opioids have little effect on evoked potentials. Propofol and thiopental depress the evoked potentials when given in a bolus, and have a minimal effect when given in a steady infusion state. Ketamine increases the amplitude of SSEP and MEP but has adverse effects such as raising the intracranial pressure and causing hallucinations. Muscle relaxants should be avoided if the muscle MEPs (EMG, MEP, reflex) are to be monitored. All evoked potentials, including MEP, SSEP, BAEP are sensitive to vascular compromise and mechanical compression. Stable hemodynamics, normal pH, normocarbia and normothermia should be maintained throughout the duration of performing the IONM procedure.[12],[58],[59]


  Special Consideration Top


IONM in awake patients

Patient selection, cooperation and good rapport between the patient and anesthesiologist are prime components for the conduction of a successful awake craniotomy. Anesthetist and neurophysiologist need to discuss in detail with the patient preoperatively the questions and the procedure that will be done during the procedure. Asleep-awake-asleep and monitored anesthesia care are the techniques that are used for tumors involving eloquent area and epilepsy surgeries. Scalp block with adequate analgesics and sedatives are titrated such that the patient is comfortable and co-operative throughout the procedure. Awake-asleep-awake is the most common technique used; however, whenever a longer duration surgery is performed, problems may arise in patient positioning, and in management of intraoperative seizures, blood loss and anxiety.[60],[61],[62],[63]

IONM in pediatric patients

It is challenging to do neurophysiological monitoring in the pediatric age group in view of the immature nervous system, as maturation occurs at about 13 years of age. Furthermore, the children are more prone to develop hypothermia, blood loss and hemodynamic fluctuations due to an immature nervous system, which can alter IONM responses.[13],[21],[24],[64],[65],[66],[67],[68],[69].

IONM in obstetric patients

Monitoring during pregnancy involves a multidisciplinary team approach involving neuroanesthesiologists, neurosurgeons, and obstetricians. Keeping the voltage minimum for MEP, reducing the number of MEP stimulation trains, and monitoring of fetal heart rate and uterine tone are some of the strategies considered in pregnant patients. Drugs crossing fetoplacental circulation and causing fetal depression should be used cautiously and only if needed to avoid unnecessary false alarm. Preoperative and postoperative fetal wellbeing should be documented. The risk of fetal loss and emergency cesarian section during the procedure should be explained.[70]


  Supratentorial Tumors Top


IONM in cortical surgery

IONM is indicated when the lesion is in or near an eloquent area, such as the sensorimotor cortex, the premotor cortex or the language area. Monitoring is used to identify the functional relationships between edge of the tumor and the surrounding areas. While ECoG is used to map and assess the electrical activity of the brain, SSEP is used to identify the central sulcus via phase reversal technique, and direct cortical stimulation is performed to map the vital structures and can be done either in awake or asleep state.[71]

The time used for cortical mapping includes the time spent on identification of functional landmarks, deciding working currents as well as entry points, and in the designing of extent of corticotomy. Consequently, the required time varies between 5 and 15 minutes.

Surgical nuances in cortical stimulation

Direct electrical stimulation of the brain produces excitation and inhibition in neuronal networks, synaptic connections and fibre tracts.[72] Subthreshold stimulation can falsely ''clear” tissue as being non-functional, leading to surgical deficits; and, suprathreshold stimulation may overstimulate the adjacent cortical areas to falsely produce functional signs or symptoms, leading to subtotal resection. A region might be considered resectable because its function would not have been tested by an appropriate intraoperative task.[73] Inadequate functional brain mapping has been associated with a lower incidence of gross total resection of tissue and a greater post-operative morbidity [74] The maximal current intensity applied during the stimulation that does not interfere with function or produce after-discharges (ADs) on ECoG is considered an endpoint for non-functional tissue. After-discharges detected by ECoG provide optimal stimulation intensity and signal a boundary where further current escalation could result in a seizure[75]. One common mistake that often occurs by an inexperienced team is that the team fails to reduce the current when stimulating the new adjacent area, or when stimulating after a break. Together, direct electrical stimulation and ECoG provide real-time electrophysiological feedback to neurosurgeons during the operation.[62] A meta-analysis showed evidence that cortical mapping revealed a significant decrease in the rate of severe persistent neurological deficits even in eloquent areas.[76] Mapping and monitoring under general anesthesia of the motor cortex and pyramidal pathways has become the standard of care for tumors in the vicinity of the Rolandic cortex or the insula.[77]

Cortical language mapping

Language mapping is unique compared to motor mapping as it always needs to be done under awake circumstances. One has to confirm the language mapping area three times before labelling it as eloquent. While the surgeon resects a lesion, a series of language tasks are carried out through the length of surgery. A 1-cm margin of tissue should be measured and preserved around each positive language site to protect the functional tissue during resection.[78] When operating on language areas, awake mapping has resulted in a decrease in post-operative permanent aphasias to less than 2%.[79]

IONM in subcortical surgery

It represents the most critical phase of tumor resection, since it significantly affects the extent of resection and the functional result of surgery. During the subcortical IONM, resection must be associated with consistent mapping, carried out either in an alternate or continuous manner. In this phase, with the aid of subcortical mapping methods, the functional limits of the tumor are identified. Limits of the eloquent area are sought at the periphery of the planned resection area, starting from the cortical areas that were judged as nonfunctional during the cortical phase of the procedure. The surgeon must have in his/her mind, the architecture of the functional map of the networks surrounding the tumor, adopting and varying the tests to be performed during the intraoperative mapping, to identify and recognize each of these networks during various stages of the procedure. In this way, a functional disconnection of the tumor is progressively obtained, and the resection is also precisely achieved according to functional limits. During the resection phase, particular attention must be paid not only to the identification and sparing of functional sites surrounding the tumor to define its functional limits, but also to carefully respect the vascular architecture within and around the tumor mass. The subcortical time for IONM has a variable duration depending on the area and the extent of resection, ranging from 20 minutes to a few hours.

With growing technology, with the realization of importance of subcortical white matter, and with the advent of techniques such as tractography, fibre dissection techniques and connectomics, the functional assessment of subcortical fibres is increasingly being deployed during routine neurosurgical procedures. It has become a standard practice to do a detailed subcortical monitoring especially near language areas and the motor cortex. With the evolution of connectomics and the concept of existence of meta networks, subcortical functions need to be assessed and to be monitored in an awake state.[71]

Common language pathways detected with reproducibility in the dominant hemisphere using stimulations should be surgically preserved to avoid definitive speech disturbances. These include the the subcallosal fibres (ScF) (eliciting initiation disorders during the stimulation), the periventricular white matter (PVWM) containing motor and sensory fibres of the face (inducing anarthria, when stimulated), the arcuate fasciculus (AF) and the insulo-opercular connections (generating anomia during stimulations).

The same techniques that are applied to the cortical assessment can be used at the subcortical level. For a surgeon, this assessment is more important than cortical mapping and monitoring, as there are multiple issues that need to be understood. Only with a sound anatomical knowledge can the surgeon decide when to start the subcortical monitoring. The concomitant usage of imaging techniques such as tractography, and operative assistance such as navigation, also help the surgeon. The strategy of immediately locating functional margins from early stages of subcortical resection reduces the time of awakening and collaboration.[80] With the surgeon's sound skill, he can start the monitoring when approximately 1 cm thickness of the tumor wall remains after an internal decompression, while some studies advocate the usage of high currents, up to 15 -20 mA along with a suction stimulator, while decompressing the tumor and then to start reducing the current as one starts getting positive signals. The methodology of stimulation parameters remains the same as for cortical stimulation, during the subcortical stimulation; however, monopolar cathodal stimulations are preferred. [81]

The safety margin for tumor resection has not been defined yet but most agree that one to three mm margin is sufficient.[82] Functional results can be evaluated either at an earlier (within 1 week) or later (from 1 to 3 months) time after surgery. Evaluation is generally performed with a detailed neurological examination, accompanied by a neuropsychological and psycho-oncological evaluation. [83],[84]

The purpose of brain mapping techniques is to identify and preserve at the time of surgery, the cortical and sub-cortical functional sites. Resection is in fact stopped when language and/or motor, or visuospatial, or cognitive cortical or subcortical areas are encountered. Evaluation of motor or language deficits during the postoperative course and at the follow-up visit showed that the chances of developing a new deficit or the worsening of a preexisting one in the immediate postoperative period varies between 65% and 92.8%. This is not surprising when the surgery is tailored to reach functional boundaries. In this situation, the chance of inducing permanent deficits is significantly high, because the surgeon reaches these functional limits in all cases in whom surgery is performed.[85] Most of the immediate deficits are transient and disappear within 1 month after surgery. MEP monitoring can help in monitoring and preventing the appearance of motor deficits due to vascular injury.[86] When subcortical stimulation was systematically applied during the resection of low grade gliomas located within language areas or pathways, only 2.3% patients showed a long-term impairment.[87] Similar or even lower numbers were observed during the resection of gliomas close to motor areas or pathways (0.5% of deficits).[85] These data support the relevance of subcortical stimulation as a useful surgical adjunct during removal of lesions involving motor or speech areas, as further demonstrated by the high percentage (95.8%) of patients who returned to work, 3 months after surgery.[1],[88]


  Infratentorial Tumors Top


Cerebello-pontine (CP) angle tumors

IONM techniques required for tumors located in the CP angle are free-run EMG and triggered EMG of 5th, 6th, 7th and lower cranial nerves, MEP that include both corticospinal and corticobulbar stimulation, SSEP, BAEP, and reflexes like the blink, masseter and laryngeal adductor reflex. Most common tumors in this location are vestibular schwannomas, epidermoids, and CP angle meningiomas. Baseline MEP, SSEP and BAEP monitoring should be done before proceeding with the actual surgery. Before dissecting the arachnoid from these extraaxial lesions, triggered EMG of 7th and lower cranial nerves should be done. During decompression of the tumor, the free-run EMG should be monitored. During tumor dissection, if there is presence of free-run EMG activity for ≥100 msec that indicates a particular cranial nerve in the vicinity, the surgeon should be alerted, and triggered EMG should be conducted using a constant-current stimulator to trace the course of the nerve (once the firing of free-run EMG has subsided)[89],[90] The BAEP and SSEP waveforms are continuously monitored, which are obtained from the neuronal pathways. If there is compromised vascular supply or traction in the proximity of the resection area, there will be reduction in amplitude and increased latency of the waveforms. MEP is carried out at every 5-30 min interval. Blink, masseter and laryngeal adductor reflex indicate the integrity of the local reflex arc in the brainstem.

Intrinsic brainstem lesions and fourth ventricular tumors

Mapping of the facial colliculus, the vagal and hypoglossal triangle should be done before making an entry into the floor of fourth ventricle for intrinsic brainstem lesions. After making an entry into the brainstem and during dissection of the tumor, both corticospinal and corticobulbar MEPs, SSEP and BAEP are monitored along with laryngeal adductor and blink reflex. For the fourth ventricular tumors like medulloblastoma/ependymoma, continuous SSEP and BAEP are monitored, and intermittently MEP of the corticospinal and corticobulbar tracts should also be done.

Performing IONM during the resection of infratentorial tumors detects early electrophysiological changes, which help in preventing permanent neurological deficits. Cranial nerves are very sensitive to any kind of direct or indirect manipulation, such as the use of mechanical forces causing stretching or compression; or the performance of irrigation, bipolar cauterization, or tumor removal with an ultrasonic surgical aspirator. These surgical techniques are very likely to result in nerve conduction block and/or any kind of spontaneous activity in free run EMG.[91]

Skull base tumors

For endonasal transsphenoidal approach for pituitary macroadenomas, VEP is monitored; however, it is not recommended as a routine procedure due to inconsistencies found during its conduction and because of the variable results obtained.[92] For clival chordomas, an extraocular muscle EMG, along with MEP and SSEP monitoring, has to be done. For petroclival meningiomas, the extraocular muscles, as well as the 5th, 6th 7th and lower cranial nerve activity should be monitored, along with MEP, SSEP and BAEP. The incidence of cranial nerve deficits without IONM during the resection of skull base tumors is reported to vary from 8-70% versus 2.8% when IONM is simultaneously performed.[69]

Spinal cord tumors

IONM is done for intramedulary, intradural extramedullary (IDEM), and extradural tumors. MEP and SSEP are done for all types of spinal cord tumors and the baseline waveforms should be monitored before and after positioning the patient. For monitoring during surgery for intramedullary and IDEM tumors, baseline direct spinal motor evoked potentials (D-waves) are measured before opening the dura. The D-wave electrode should be placed below the tumor in the epidural space for obtaining the baseline waveforms, and these waveforms should be compared with the ones obtained during and after the tumor resection. For intramedullary tumors, dorsal column mapping is done before conducting the midline myelotomy. These lesions distort the normal midline and one tends to injure the dorsal column while making the myelotomy, unless an IOMN is simultaneously performed. Triggered EMG is also of great use in spinal tumors during the stage of tumor resection. It is applied to monitor selective nerve root function, and it is a “real-time” recording from the peripheral musculature. This monitoring also prevents the development of postoperative radiculopathy during spinal instrumentation surgery, including pedicle screw placement. Anal sphincter reflex and bulbo-cavernous reflex are mainly done for tumors involving the conus and cauda equina. The role of IONM in spinal tumors has been well-documented for predicting the adverse events and for obtaining better neurological outcomes.[93],[94],[95],[96]


  Future of IONM Top


The functions to be mapped and preserved are not only limited to language or motor ones, but expand to haptic, visuospatial, visual, and cognitive functions, in order to maintain complete patient integrity and preserve his/her quality of life. Consequently, performing only the intraoperative motor and language mapping is not enough while removing a cerebral tumor. Identifying and sparing neural networks that subserve cognition (movement control, visuospatial cognition, executive functions, multimodal semantics, metacognition) and mentalization (theory of mind, which plays a key role in social cognition) in awake patients is essential to resume a normal way of life.

Using a functional approach, the management of a patient entering the out-patient clinic with a presumptive diagnosis of glioma must be aimed at defining the degree of functional reorganization achieved by the patient's brain surrounding the tumor.[2],[97] The general treatment plan is to be decided and tailored to the specific situation taking into consideration the patient symptoms, signs, and the nature of tumor, thereby assessing the feasibility of resection and the possible degree of tumor removal that can be achieved in that particular patient. A detailed neuropsychological evaluation needs to be integrated with the imaging. This knowledge should be utilized during the surgical resection of the tumor, with the simultaneous usage of intraoperative monitoring tailored to the needs of the patient, also being done to ensure a safe yet adequate resection of the tumor.

The disorders generated by surgical injuries of circuits underpinning nonmotor and nonspeech functions are usually not immediately visible on the postoperative standard clinical examination, leading the physician to believe that the patient has had no deficit following surgery. Yet, cognitive or emotional disturbances may subsequently prevent the patient's return to an active life and to his/her full-time working. A new connectome-based surgical approach should be more systematically considered in the management of cerebral tumors to preserve or to improve quality of life.

Redefining concepts of oncofunctional resections

An oncofunctional balance needs to be maintained by the neurosurgeon based on the patient's needs, imaging, and the genetic characteristics of the tumor. Patients should clearly formulate his wishes regarding the kind of functions that he/she wishes, should be primarily preserved. This will depend on the way of life, including profession, hobbies, and social interactions.[98] The degree of resection, tailored according to the patient's lifestyle, may be different for a patient who uses skills other than the pure motor or language ones, and a patient who is content with motor and language skills alone.

Troubleshooting and complications

The troubleshooting steps,[20],[25],[99],[100],[101] in the case of drop of any of the responses, have been depicted in [Figure 12]. Complications include tongue bite (0.2%); thermal skin and neural injury, burns around the electrode; the precipitation of seizures, muscle pain and hematoma, transient blood pressure changes, cardiac arrhythmia; wrong electrode placement; and displacement of electrodes due to patient movements.[102] The relative contraindications during the MEP monitoring include the presence of epilepsy, cortical lesions, skull defects, and the presence of intra-cranial electrodes, vascular clips or shunts, and biomedical implants.[103] Preexisting structural or physiological damage to eloquent areas/long tracts makes the IONM unreliable. For instance, if the grade of muscle power in the patient is less than 3, eliciting an MEP response will be difficult and unreliable. The drawback of IONM is that the simultaneous monitoring of all modalities is difficult and might miss alarming electrophysiological responses at critical points of resection.
Figure 12: Troubleshooting in IONM

Click here to view


We conclude that IONM is more relevant to achieve a good onco-functional neurosurgical outcome. An intraoperative MRI (IOMRI) as an adjunct to IONM, increased the extent of safe resection.[104] The widespread usage of and an improvement in these techniques have allowed a greater and safer removal of tumors, thereby reducing the risk of permanent postoperative neurological deficits and obtaining a better functional outcome.[105],[106],[107],[108]

Acknowledgement

We acknowledge (1) Mr. Bomma Umesh, Neurosurgery OT Electrophysiology Technician, Department of Neuroanaesthesia, Yashoda Hospitals, Secunderabad, [email protected], 9912152902, and (2) Mr. Chaitanya Srinivas Lanka Venkatachalam, PhD Student, Neurotech Lab, Biomedical Engineering Department, Indian Institute of Technology, Hyderabad, [email protected], 8297051156.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Silverstein J. Mapping the motor and sensory cortices: a historical look and a current case study in sensorimotor localization and direct cortical motor stimulation. Neurodiagn J 2012;52:54-68.  Back to cited text no. 1
    
2.
Pendleton C, Zaidi HA, Chaichana KL, Raza SM, Carson BS, Cohen-Gadol AA, et al. Harvey Cushing's contributions to motor mapping: 1902–1912. Cortex 2012;48:7-14.  Back to cited text no. 2
    
3.
Duffau H. Preserving quality of life is not incompatible with increasing overall survival in diffuse low-grade glioma patients. Acta Neurochir 2015;2:165-7.  Back to cited text no. 3
    
4.
Fountain DM, Allen D, Joannides AJ, Nandi D, Santarius T, Chari A. Reporting of patient-reported health-related quality of life in adults with diffuse low-grade glioma: a systematic review. Neurooncol 2016;18:1475-86.  Back to cited text no. 4
    
5.
Duffau HJ. Diffuse low-grade glioma, oncological outcome and quality of life: a surgical perspective. Curr Opin Oncol 2018;30:383-9.  Back to cited text no. 5
    
6.
Duffau HJ. Long-term outcomes after supratotal resection of diffuse low-grade gliomas: a consecutive series with 11-year follow-up. Acta Neurochir (Wien) 2016;158:51-8.  Back to cited text no. 6
    
7.
Li YM, Suki D, Hess K, Sawaya RJJ. The influence of maximum safe resection of glioblastoma on survival in 1229 patients: can we do better than gross-total resection? J Neurosurg 2016;124:977-88.  Back to cited text no. 7
    
8.
Bello L, Fava E, Casaceli G, Bertani G, Carrabba G, Papagno C, et al. Intraoperative mapping for tumor resection. Neuroimaging Clin 2009;19:597-614.  Back to cited text no. 8
    
9.
Bertani G, Fava E, Casaceli G, Carrabba G, Casarotti A, Papagno C, et al. Intraoperative mapping and monitoring of brain functions for the resection of low-grade gliomas: technical considerations. Neurosurg Focus 2009;27:E4.  Back to cited text no. 9
    
10.
Vega-Zelaya L, Sola RG, Pastor J. Intraoperative neurophysiological monitoring in neuro-oncology. Neurooncology-Newer Developments: IntechOpen 2016. https://www.intechopen.com/chapters/50999  Back to cited text no. 10
    
11.
Szelenyi A, Kothbauer KF, Deletis V. Transcranial electric stimulation for intraoperative motor evoked potential monitoring: Stimulation parameters and electrode montages. Clin Neurophysiol 2007;118:1586-95.  Back to cited text no. 11
    
12.
Park JH, Hyun SJ. Intraoperative neurophysiological monitoring in spinal surgery. World J Clin Cases 2015;3:765-73.  Back to cited text no. 12
    
13.
Kim SM, Kim SH, Seo DW, Lee KW. Intraoperative neurophysiologic monitoring: basic principles and recent update. J Korean Med Sci 2013;28:1261-9.  Back to cited text no. 13
    
14.
Nunes RR, Bersot CDA, Garritano JG. Intraoperative neurophysiological monitoring in neuroanesthesia. Curr Opin Anaesthesiol 2018;31:532-8.  Back to cited text no. 14
    
15.
Kim K, Cho C, Bang MS, Shin HI, Phi JH, Kim SK. Intraoperative neurophysiological monitoring: a review of techniques used for brain tumor surgery in children. J Korean Neurosurg Soc 2018;61:363-75.  Back to cited text no. 15
    
16.
Strike SA, Hassanzadeh H, Jain A, Kebaish KM, Njoku DB, Becker D, et al. Intraoperative neuromonitoring in pediatric and adult spine deformity surgery. Clin Spine Surg 2017;30:E1174-E81.  Back to cited text no. 16
    
17.
Sala F, Coppola A, Tramontano V, Babini M, Pinna G. Intraoperative neurophysiological monitoring for the resection of brain tumors in pediatric patients. J Neurosurg Sci 2015;59:373-82.  Back to cited text no. 17
    
18.
Francis L, Busso V, McAuliffe JJ. Intraoperative neuromonitoring in pediatric surgery. Monitoring the nervous system for anesthesiologists and other health care professionals. Cham: Springer; 2017. p. 633-49. https://doi.org/100.1007/978-3-319-46542-5_43  Back to cited text no. 18
    
19.
Bidkar PU, Thakkar A, Manohara N, Rao KS. Intraoperative neurophysiological monitoring (IONM) in pediatric neurosurgery. Int J Clin Pract 2021; e14160. doi: 10.1111/ijcp. 14160.  Back to cited text no. 19
    
20.
Silverman D. The rationale and history of the 10-20 system of the International Federation. Am J EEG Tech 1963;3:17-22.  Back to cited text no. 20
    
21.
Tran TA, Spencer SS, Javidan M, Pacia S, Marks D, Spencer DD. Significance of spikes recorded on intraoperative electrocorticography in patients with brain tumor and epilepsy. Epilepsia 1997;38:1132-9.  Back to cited text no. 21
    
22.
Vadivelu S, Sivaganesan A, Patel AJ, Agadi S, Schmidt RJ, Mani P, et al. Practice trends in the utilization of intraoperative neurophysiological monitoring in pediatric neurosurgery as a function of complication rate, and patient-, surgeon-, and procedure-related factors. World Neurosurg 2014;81:617-23.  Back to cited text no. 22
    
23.
Busso VO, McAuliffe JJ. Intraoperative neurophysiological monitoring in pediatric neurosurgery. Paediatr Anaesth 2014;24:690-7.  Back to cited text no. 23
    
24.
Gutzwiller EM, Cabrilo I, Radovanovic I, Schaller K, Boex C. Intraoperative monitoring with visual evoked potentials for brain surgeries. J Neurosurg 2018;130:654-60.  Back to cited text no. 24
    
25.
Feng R, Schwartz J, Loewenstern J, Kohli K, Lenina S, Ultakan S, et al. The predictive role of intraoperative visual evoked potentials in 27 visual improvement after endoscopic pituitary tumor resection in large and complex tumors: description and validation of a method. World Neurosurg 2019;126:e136-e43.  Back to cited text no. 25
    
26.
Sloan T. Anesthesia and intraoperative neurophysiological monitoring in children. Childs Nerv Syst 2010;26:227-35.  Back to cited text no. 26
    
27.
Lall RR, Lall RR, Hauptman JS, Munoz C, Cybulski GR, Koski T, et al. Intraoperative neurophysiological monitoring in spine surgery: indications, efficacy, and role of the preoperative checklist. Neurosurg Focus 2012;33:E10.  Back to cited text no. 27
    
28.
Jahangiri FR, Pautler K, Watters K, Anjum SS, Bennett GL. Mapping of the somatosensory cortex. Cureus 2020;12:e7332.  Back to cited text no. 28
    
29.
Simon MV, Sheth SA, Eckhardt CA, Kilbride RD, Braver D, Williams Z, et al. Phase reversal technique decreases cortical stimulation time during motor mapping. J Clin Neurosci 2014;21:1011-7.  Back to cited text no. 29
    
30.
Simon MV, Chiappa KH, Borges LF. Phase reversal of somatosensory evoked potentials triggered by gracilis tract stimulation: case report of a new technique for neurophysiologic dorsal column mapping. Neurosurgery 2012;70:E783-8.  Back to cited text no. 30
    
31.
Nair D, Kumaraswamy VM, Braver D, Kilbride RD, Borges LF, Simon MV. Dorsal column mapping via phase reversal method: the refined technique and clinical applications. Neurosurgery. 2014;74:437-46  Back to cited text no. 31
    
32.
Ramasubbu C, Flagg A, 2nd, Williams K. Principles of electrical stimulation and dorsal column mapping as it relates to spinal cord stimulation: an overview. Curr Pain Headache Rep 2013;17:315.  Back to cited text no. 32
    
33.
Yanni DS, Ulkatan S, Deletis V, Barrenechea IJ, Sen C, Perin NI. Utility of neurophysiological monitoring using dorsal column mapping in intramedullary spinal cord surgery. J Neurosurg Spine 2010;12:623-8.  Back to cited text no. 33
    
34.
Mehta AI, Mohrhaus CA, Husain AM, Karikari IO, Hughes B, Hodges T, et al. Dorsal column mapping for intramedullary spinal cord tumor resection decreases dorsal column dysfunction. J Spinal Disord Tech 2012;25:205-9.  Back to cited text no. 34
    
35.
Krieg SM, Shiban E, Droese D, Gempt J, Buchmann N, Pape H, et al. Predictive value and safety of intraoperative neurophysiological monitoring with motor evoked potentials in glioma surgery. Neurosurgery. 2012;70:1060-71.  Back to cited text no. 35
    
36.
Zhang M, Zhou Q, Zhang L, Jiang Y. Facial corticobulbar motor-evoked potential monitoring during the clipping of large and giant aneurysms of the anterior circulation. J Clin Neurosci 2013;20:873-8.  Back to cited text no. 36
    
37.
Walker CT, Kim HJ, Park P, Lenke LG, Weller MA, Smith JS, et al. Neuroanesthesia guidelines for optimizing transcranial motor evoked potential neuromonitoring during deformity and complex spinal surgery: A Delphi Consensus Study. Spine (Phila Pa 1976) 2020;45:911-20.  Back to cited text no. 37
    
38.
Tellez MJ, Ulkatan S, Urriza J, Arranz-Arranz B, Deletis V. Neurophysiological mechanism of possibly confounding peripheral activation of the facial nerve during corticobulbar tract monitoring. Clin Neurophysiol 2016;127:1710-6.  Back to cited text no. 38
    
39.
Morota N, Ihara S, Deletis V. Intraoperative neurophysiology for surgery in and around the brainstem: role of brainstem mapping and corticobulbar tract motor-evoked potential monitoring. Childs Nerv Syst 2010;26:513-21.  Back to cited text no. 39
    
40.
Macdonald DB, Skinner S, Shils J, Yingling C, American Society of Neurophysiological M. Intraoperative motor evoked potential monitoring-a position statement by the American Society of Neurophysiological Monitoring. Clin Neurophysiol 2013;124:2291-316  Back to cited text no. 40
    
41.
Legatt AD, Emerson RG, Epstein CM, MacDonald DB, Deletis V, Bravo RJ, et al. ACNS Guideline: Transcranial electrical stimulation motor evoked potential monitoring. J Clin Neurophysiol 2016;33:42-50.  Back to cited text no. 41
    
42.
Leroy HA, Strachowksi O, Tuleasca C, Vannod-Michel Q, Le Rhun E, Derre B, et al. Microsurgical resection of fronto-temporo-insular gliomas in the non-dominant hemisphere, under general anesthesia using adjunct intraoperative MRI and no cortical and subcortical mapping: a series of 20 consecutive patients. Sci Rep 2021;11:6994.  Back to cited text no. 42
    
43.
Ratha V, Sampath N, Subramaniam S, Kumar VRR. Technical considerations in awake craniotomy with cortical and subcortical motor mapping in preadolescents: pushing the envelope. Pediatr Neurosurg 2021:56:171-178.  Back to cited text no. 43
    
44.
Young JS, Lee AT, Chang EF. A review of cortical and subcortical stimulation mapping for language. Neurosurgery 2021. nyaa436.doi: 10.1093/neuros/nyaa436.  Back to cited text no. 44
    
45.
Domingo RA, Vivas-Buitrago T, Sabsevitz DS, Middlebrooks EH, Quinones-Hinojosa A. Awake craniotomy with cortical and subcortical speech mapping for supramarginal cavernoma resection. World Neurosurg 2020;141:260. doi: 10.1016/j.wneu.2020.06.094.  Back to cited text no. 45
    
46.
Pallud J, Mandonnet E, Corns R, Dezamis E, Parraga E, Zanello M, et al. Technical principles of direct bipolar electrostimulation for cortical and subcortical mapping in awake craniotomy. Neurochirurgie 2017;63:158-63.  Back to cited text no. 46
    
47.
Enatsu R, Kanno A, Ohtaki S, Akiyama Y, Ochi S, Mikuni N. Intraoperative subcortical fiber mapping with subcortico-cortical evoked potentials. World Neurosurg 2016;86:478-83.  Back to cited text no. 47
    
48.
Landazuri P, Eccher M. Simultaneous direct cortical motor evoked potential monitoring and subcortical mapping for motor pathway preservation during brain tumor surgery: is it useful? J Clin Neurophysiol 2013;30:623-5.  Back to cited text no. 48
    
49.
Carrabba G, Fava E, Giussani C, Acerbi F, Portaluri F, Songa V, et al. Cortical and subcortical motor mapping in rolandic and perirolandic glioma surgery: impact on postoperative morbidity and extent of resection. J Neurosurg Sci 2007;51:45-51.  Back to cited text no. 49
    
50.
Mikuni N. [Awake neurosurgery: usefulness of intraoperative cortical and subcortical functional mapping]. No Shinkei Geka 2004;32:1105-15.  Back to cited text no. 50
    
51.
Sindou M, Joud A, Georgoulis G. Usefulness of external anal sphincter EMG recording for intraoperative neuromonitoring of the sacral roots-a prospective study in dorsal rhizotomy. Acta Neurochir (Wien) 2021;163:479-87.  Back to cited text no. 51
    
52.
Skinner S, Chiri CA, Wroblewski J, Transfeldt EE. Enhancement of the bulbocavernosus reflex during intraoperative neurophysiological monitoring through the use of double train stimulation: a pilot study. J Clin Monit Comput 2007;21:31-40.  Back to cited text no. 52
    
53.
Aydinlar EI, Kocak M, Soykam HO, Mat B, Dikmen PY, Sezerman OU, et al. Intraoperative neuromonitoring of blink reflex during posterior fossa surgeries and its correlation with clinical outcome. J Clin Neurophysiol 2020. doi: 10.1097/WNP. 0000000000000777.  Back to cited text no. 53
    
54.
Tellez MJ, Mirallave-Pescador A, Seidel K, Urriza J, Shoakazemi A, Raabe A, et al. Neurophysiological monitoring of the laryngeal adductor reflex during cerebellar-pontine angle and brainstem surgery. Clin Neurophysiol 2021;132:622-31.  Back to cited text no. 54
    
55.
Satomaa AL, Vanttinen S, Mattila H. The intraoperative laryngeal adductor reflex (LAR) in brainstem tumor removal: A case of unilateral loss of LAR signal. Clin Neurophysiol 2019;130:1253-5.  Back to cited text no. 55
    
56.
Costa P, Gaglini PP, Tavormina P, Ricci F, Peretta P. A method for intraoperative recording of the laryngeal adductor reflex during lower brainstem surgery in children. Clin Neurophysiol 2018;129:2497-8.  Back to cited text no. 56
    
57.
Ulkatan S, Tellez MJ, Sinclair C. Laryngeal adductor reflex and future projections for brainstem monitoring. Reply to “A method for intraoperative recording of the laryngeal adductor reflex during lower brainstem surgery in children”. Clin Neurophysiol 2018;129:2499-500.  Back to cited text no. 57
    
58.
Pescador AM, Angeles Sanchez Roldan M, Tellez MJ, Sinclair CF, Ulkatan S. Unforeseen clinical outcome for laryngeal adductor reflex loss during intraaxial brainstem surgery. Clin Neurophysiol 2019;130:2001-2.  Back to cited text no. 58
    
59.
Gonzalez Otarula K, Barroso F. Masseter inhibitory reflex abnormality and brainstem lesion. Medicina (B Aires) 2013;73:451.  Back to cited text no. 59
    
60.
Ongerboer de Visser BW, Cruccu G, Manfredi M, Koelman JH. Effects of brainstem lesions on the masseter inhibitory reflex. Functional mechanisms of reflex pathways. Brain 1990;113 (Pt 3):781-92.  Back to cited text no. 60
    
61.
Tewari A, Francis L, Samy RN, Kurth DC, Castle J, Frye T, et al. Intraoperative neurophysiological monitoring team's communique with anesthesia professionals. J Anaesthesiol Clin Pharmacol 2018;34:84-93.  Back to cited text no. 61
[PUBMED]  [Full text]  
62.
Ali Z. Intraoperative neurophysiologic monitoring and anaesthetic implications. Indian J Anaesth 2019;63:81-3.  Back to cited text no. 62
[PUBMED]  [Full text]  
63.
Kulikov A, Lubnin A. Anesthesia for awake craniotomy. Curr Opin Anaesthesiol 2018;31:506-10.  Back to cited text no. 63
    
64.
Gravesteijn BY, Keizer ME, Vincent A, Schouten JW, Stolker RJ, Klimek M. Awake craniotomy versus craniotomy under general anesthesia for the surgical treatment of insular glioma: choices and outcomes. Neurol Res 2018;40:87-96.  Back to cited text no. 64
    
65.
Eseonu CI, ReFaey K, Garcia O, John A, Quinones-Hinojosa A, Tripathi P. Awake craniotomy anesthesia: a comparison of the monitored anesthesia care and asleep-awake-asleep techniques. World Neurosurg 2017;104:679-86.  Back to cited text no. 65
    
66.
Chowdhury T, Singh GP, Zeiler FA, Hailu A, Loewen H, Schaller B, et al. Anesthesia for awake craniotomy for brain tumors in an intraoperative mri suite: challenges and evidence. Front Oncol 2018;8:519.  Back to cited text no. 66
    
67.
Senkoylu A, Zinnuroglu M, Borcek A, Aktas E, Gungor I, Beyazova M. Comparison of multimodal intraoperative neurophysiological monitoring efficacy in early childhood and school aged children undergoing spinal surgery. Acta Orthop Traumatol Turc 2017;51:49-53.  Back to cited text no. 67
    
68.
Sala F, Krzan MJ, Deletis V. Intraoperative neurophysiological monitoring in pediatric neurosurgery: why, when, how? Childs Nerv Syst 2002;18:264-87.  Back to cited text no. 68
    
69.
Kim JH, Phi JH, Lee JY, Kim KH, Park SH, Choi YH, et al. Surgical outcomes of thalamic tumors in children: the importance of diffusion tensor imaging, neuro-navigation and intraoperative neurophysiological monitoring. Brain Tumor Res Treat 2018;6:60-7.  Back to cited text no. 69
    
70.
Kandil AI, Pettit CS, Berry LN, Busso VO, Careskey M, Chesnut E, et al. Tertiary pediatric academic institution's experience with intraoperative neuromonitoring for nonspinal surgery in children with mucopolysaccharidosis, based on a novel evidence-based care algorithm. Anesth Analg 2020;130:1678-84.  Back to cited text no. 70
    
71.
Jahangiri FR, Sayegh SA, Azzubi M, Alrajhi AM, Annaim MM, Al Sharif SA, et al. Benefit of intraoperative neurophysiological monitoring in a pediatric patient with spinal dysmorphism, split cord malformation, and scoliosis. Neurodiagn J 2017;57:295-307.  Back to cited text no. 71
    
72.
Elangovan C, Singh SP, Gardner P, Snyderman C, Tyler-Kabara EC, Habeych M, et al. Intraoperative neurophysiological monitoring during endoscopic endonasal surgery for pediatric skull base tumors. J Neurosurg Pediatr 2016;17:147-55.  Back to cited text no. 72
    
73.
Manohar N, Palan A, Manchala RK, Manjunath ST. Monitoring intraoperative motor-evoked potentials in a pregnant patient. Indian J Anaesth 2019;63:142-3.  Back to cited text no. 73
[PUBMED]  [Full text]  
74.
Duffau HJAN. Brain connectomics applied to oncological neuroscience: from a traditional surgical strategy focusing on glioma topography to a meta-network approach. Acta Neurochirur (Wein) 2021;163:905-917.  Back to cited text no. 74
    
75.
Ranck Jr. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res1975;98:417-40.  Back to cited text no. 75
    
76.
Ius T, Angelini E, de Schotten MT, Mandonnet E, Duffau HJN. Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a “minimal common brain”. Neuroimage 2011;56:992-1000.  Back to cited text no. 76
    
77.
Ritaccio AL, Brunner P, Schalk GJ. Electrical stimulation mapping of the brain: basic principles and emerging alternatives. J Clin Neurophysiol 2018;35:86-97.  Back to cited text no. 77
    
78.
Blume WT, Jones DC, Pathak PJ. Properties of after-discharges from cortical electrical stimulation in focal epilepsies. Clin Neurophysiol 2004;115:982-9.  Back to cited text no. 78
    
79.
Hamer PDW, Robles SG, Zwinderman AH, Duffau H, Berger MS. Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. J Clin Oncol 2012;30:2559-65.  Back to cited text no. 79
    
80.
Neuloh G, Pechstein U, Cedzich C, Schramm J. Motor evoked potential monitoring with supratentorial surgery. Neurosurgery 2004;54:1061-70.  Back to cited text no. 80
    
81.
Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 2001;95:190-8.  Back to cited text no. 81
    
82.
Duffau H, Gatignol P, Mandonnet E, Capelle L, Taillandier LJ. Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg 2008;109:461-71.  Back to cited text no. 82
    
83.
Duffau HJ. The usefulness of the asleep-awake-asleep glioma surgery. Acta Neurochir (Wien) 2014;156:1493.  Back to cited text no. 83
    
84.
Merrill DR, Bikson M, Jefferys JG. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J Neurosc Methods 2005;141:171-98.  Back to cited text no. 84
    
85.
Seidel K, Beck J, Stieglitz L, Schucht P, Raabe AJ. The warning-sign hierarchy between quantitative subcortical motor mapping and continuous motor evoked potential monitoring during resection of supratentorial brain tumors. J Neurosurg 2013;118:287-96.  Back to cited text no. 85
    
86.
Papagno C, Casarotti A, Comi A, Gallucci M, Riva M, Bello LJ. Measuring clinical outcomes in neuro-oncology. A battery to evaluate low-grade gliomas (LGG). J Neurooncol 2012;108:269-75.  Back to cited text no. 86
    
87.
Rofes A, Mandonnet E, Godden J, Baron MH, Colle H, Darlix A, et al. Survey on current cognitive practices within the European Low-Grade Glioma Network: towards a European assessment protocol. Acta Neurochir (Wien) 2017;159:1167-78.  Back to cited text no. 87
    
88.
Bello L, Riva M, Fava E, Ferpozzi V, Castellano A, Raneri F, et al. Tailoring neurophysiological strategies with clinical context enhances resection and safety and expands indications in gliomas involving motor pathways. Neuro Oncol 2014;16:1110-28.  Back to cited text no. 88
    
89.
Szelényi A, Bello L, Duffau H, Fava E, Feigl GC, Galanda M, et al. Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. Neurosurg Focus 2010;28:E7.  Back to cited text no. 89
    
90.
Bello L, Fava M, Gallucci M, Giussani C, Carrabba G, Acerbi F, et al. Intraoperative subcortical language tracts mapping guides surgical removal of gliomas involving speech areas 902. J Neurosurgery 2007;60:67-80.  Back to cited text no. 90
    
91.
Duffau H, Capelle L, Sichez N, Denvil D, Lopes M, Sichez JP, et al. Intraoperative mapping of the subcortical language pathways using direct stimulations: An anatomo-functional study. Brain 2002;125:199-214.  Back to cited text no. 91
    
92.
Thirumala PD, Mohanraj SK, Habeych M, Wichman K, Chang Y-F, Gardner P, et al. Value of free-run electromyographic monitoring of lower cranial nerves in endoscopic endonasal approach to skull base surgeries. J Neurol Surg B Skull Base 2012;73:236-44.  Back to cited text no. 92
    
93.
Slotty PJ, Abdulazim A, Kodama K, Javadi M, Hanggi D, Seifert V, et al. Intraoperative neurophysiological monitoring during resection of infratentorial lesions: the surgeon's view. J Neurosurg 2017;126:281-8.  Back to cited text no. 93
    
94.
Chung S-B, Park C-W, Seo D-W, Kong D-S, Park S-K. Intraoperative visual evoked potential has no association with postoperative visual outcomes in transsphenoidal surgery. Acta Neurochir (Wien) 2012;154:1505-10.  Back to cited text no. 94
    
95.
Charalampidis A, Jiang F, Wilson JR, Badhiwala JH, Brodke DS, Fehlings MG. The use of intraoperative neurophysiological monitoring in spine surgery. Global Spine J 2020;10:104S-14S.  Back to cited text no. 95
    
96.
Forster M-T, Marquardt G, Seifert V, Szelényi A. Spinal cord tumor surgery—importance of continuous intraoperative neurophysiological monitoring after tumor resection. Spine J 2012;37:E1001-E8.  Back to cited text no. 96
    
97.
Sala F, Palandri G, Basso E, Lanteri P, Deletis V, Faccioli F, et al. Motor evoked potential monitoring improves outcome after surgery for intramedullary spinal cord tumors: a historical control study. Neurosurgery 2006;58:1129-43  Back to cited text no. 97
    
98.
Jin SH, Chung CK, Kim CH, Choi YD, Kwak G, Kim BE. Multimodal intraoperative monitoring during intramedullary spinal cord tumor surgery. Acta Neurochir (Wien) 2015;157:2149-55.  Back to cited text no. 98
    
99.
Herbet G, Maheu M, Costi E, Lafargue G, Duffau H. Mapping neuroplastic potential in brain-damaged patients. Brain 2016;139:829-44.  Back to cited text no. 99
    
100.
Coello AF, Moritz-Gasser S, Martino J, Martinoni M, Matsuda R, Duffau H. Selection of intraoperative tasks for awake mapping based on relationships between tumor location and functional networks: A review. J Neurosurg 2013;119:1380-94.  Back to cited text no. 100
    
101.
Ziewacz JE, Berven SH, Mummaneni VP, Tu T-H, Akinbo OC, Lyon R, Mummaneni PV. The design, development, and implementation of a checklist for intraoperative neuromonitoring changes. Neurosurg Focus 2012; 33 (5): E11.  Back to cited text no. 101
    
102.
Rendahl R, Hey LA. Technical tips: a checklist for responding to intraoperative neuromonitoring changes. Neurodiagn J 2019;59:77-81.  Back to cited text no. 102
    
103.
Polly DW, Jr., Rice K, Tamkus A. What is the frequency of intraoperative alerts during pediatric spinal deformity surgery using current neuromonitoring methodology? A retrospective study of 218 surgical procedures. Neurodiagn J 2016;56:17-31.  Back to cited text no. 103
    
104.
Nitin Manohar Nitin BJR, K Pradeep K, Balasubramaniam A. Intraoperative neurophysiological monitoring in neurooncological cases: Thieme Publishing Group (India) 2020.  Back to cited text no. 104
    
105.
Mac Donald DB, Deletis V. Safety issues during surgical monitoring. Handbook of Clinical Neurophysiology. Netherlands: Elsevier; 2008; 8: 882-898.  Back to cited text no. 105
    
106.
Sala F, Dvorak J, Faccioli F. Cost effectiveness of multimodal intraoperative monitoring during spine surgery. Eur Spine J. 2007;16 (Suppl 2):S229-31.  Back to cited text no. 106
    
107.
Kombos T, Suess O, Brock M. Cost analysis of intraoperative neurophysiological monitoring (IOM)]. Zentralbl Neurochir 2002;63:141-5.  Back to cited text no. 107
    
108.
Kumar GK, Balasubramaniam A, Pradeep K, Manohar N. Intraoperative MRI in brain tumor surgeries. Neurosurgery; IntechOpen (London); 2021. https://www.intechopen.com/online-first/75966  Back to cited text no. 108
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10], [Figure 11], [Figure 12]
 
 
    Tables

  [Table 1], [Table 2]



 

Top
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
Abstract
Introduction
IONM in Neuro-On...
Anesthesia and IONM
Special Consider...
Supratentorial T...
Infratentorial T...
Future of IONM
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed78    
    Printed2    
    Emailed0    
    PDF Downloaded20    
    Comments [Add]    

Recommend this journal