Transopercular Approach to Resection of Dominant Hemisphere Diffuse Insular Glioma Using Multimodal Intraoperative Strategy with Awake Mapping
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.344621
Source of Support: None, Conflict of Interest: None
Keywords: Awake surgery, cortical and subcortical mapping, insular glioma, sub-pial resection, transopercular approach
Insula, the fifth lobe of the cerebrum, is located deep in the sylvian fissure. In addition to the deep location and close proximity to the major blood vessels within the sylvian fissure, the area is surrounded by eloquent cortex as well as deep white matter tracts and nuclei of basal ganglia. Insula itself is involved in a wide range of functions involving sensory, autonomic, language, emotional, and cognitive modalities., This makes resection of gliomas arising in this region a technical challenge to neurosurgeons. A sound knowledge of the complex anatomy of this area, as well as use of intraoperative adjuncts like cortical and subcortical mapping with direct electrical stimulation (DES) and image guidance will help the surgeon to maximize resection while preserving important functions.
This video illustrates the anatomical relationships of a dominant hemisphere giant insular glioma and demonstrates the technique of performing a transopercular approach to resect a giant fronto-insular glioma using awake bipolar mapping, and neuropsychological as well as neurophysiological monitoring.
Clinical presentation: A 27-year-old lady presented with headache, executive dysfunction, and moderate phonemic fluency impairment. Magnetic resonance imaging (MRI) of the brain revealed a diffuse large fronto-insular glioma.
Surgery: Left frontotemporal awake craniotomy, transopercular approach and resection of left insular glioma under intraoperative neuromonitoring and navigated ultrasound guidance.
Anesthesia: Scalp block and initial sedation (dexmedetomidine) with laryngeal mask airway (LMA).
Position: Right lateral, neck neutral, head fixed by 3-pin fixator.
Incision: Left frontotemporal question mark incision.
Steps of surgery:
0:00–0:37 – Hello everyone! This is Dr Aliasgar Moiyadi, and I am going to be describing the procedure for resection of a dominant hemisphere insular glioma.
This is a case of a young lady who presented with a history of headache, no neurological deficits, though neuropsychological examination showed multidomain dysfunction.
As you can see, there is a large insular glioma involving all four zones and including the frontal opercular area. Preoperative functional MRI was done to map the relevant cortical eloquent areas.
0:37–1:57 – We planned an awake surgery. We prefer doing asleep–awake–asleep technique because of the length of the surgery. The essential steps in the surgery include positioning the patient for frontotemporal craniotomy under asleep conditions and awakening the patient at the time of durotomy, at which point of time a methodical and comprehensive cortical mapping is done with bipolar stimulation followed by resection of negatively mapped inferior frontal gyrus area, and then defining the superior and anterior limiting sulci of the insula. Also, deep subcortical stimulation to identify the deep boundaries of the tumor is important. This is followed by subpial resection of the insular component of the tumor. At the depth, the deep substrates are preserved. Finally, the superior temporal gyrus exposure to address the component near the temporal isthmus or stem is done. We prefer using a navigation and an intraoperative ultrasound, in addition to guiding the extent of resection.
1:57 2:28 – Preoperatively, the navigated images are shown here with the relevant anatomical structures for understanding the relationships. We can understand that there are many deep eloquent structures—subcortical white matter as well as deep nuclei—which have to be preserved. This exercise is a good learning tool, as well as gives an orientation to the surgeon during surgery.
2:28–2:42 – After the craniotomy, the patient is awakened and a methodical bipolar mapping is done. Here, you can see the bipolar mapping being done. The red marker shows the ventral premotor cortex, the black the M1 area, and the yellow the language areas.
2:42–3:31 – Having mapped the cortex, the entry into the inferior frontal gyrus is done through multiple corticectomies preserving the bridging vessels. The tumor encountered in the opercular area is resected. We also use motor evoked potential (MEP) monitoring putting in a strip. The inferior frontal gyrus is resected and subcortical stimulation is done early on at the posterior and superior margins of the resection to identify anarthria, as well as aphasia, which may be present in the terminations of the inferior fronto-occipital fasciculus (IFOF). This is followed by sub-pial resection of the opercular component of the tumor.
3:31–3:57 – We can see the insular surface being exposed, and the superior insular sulcus is coming into view. This is an important boundary. Going deeper than this will endanger the deep white matter tracts. The tumor in the opercular area is removed.
3:57–4:37 – Another cortical window is made in the pars orbitalis to identify the anterior limiting sulcus. Working between these two cortical windows, the tumor in the insula is dissected sub-pially, preserving the vessels on the insular surface. Here we are addressing the anterior component of the tumor which is extending along the limen. Because of the bulk of the insular tumor, a small window is made in the anterior insular surface to debulk the tumor and reach the limen safely.
4:37–4:48 – Superior temporal gyrus exposure is also created to identify the inferior limiting sulcus, and this is on the extra-pial surface of the insula.
4:48–5:20 – The insular component of the tumor is now isolated completely all around, and is sub-pially dissected off the vessels in the middle cerebral artery (MCA) complex on the surface of the insula. All the while, the patient is being monitored awake, performing multiple tasks monitored by the neuropsychologist intraoperatively.
5:20–5:49 – At the depth near the limen, we stimulate for the IFOF and look for semantic paraphasias. The last component of the tumor in the limen is removed and this exposes the sylvian cistern near the vallecula, beyond which the M1 and the origin of the lenticulostriate arteries are seen, which marks the boundary of the dissection.
5:49–6:12 – The tumor is completely isolated and is dissected off the bed of the insula which is formed by the IFOF and the lentiform nucleus. Here, constant MEP monitoring is also performed because of the proximity to the corticospinal tracts.
6:12–6:35 – We prefer removing the tumor en bloc as far as possible. Of course, given the size, often part debulking is advisable. The tumor is then removed. We inspect for remnants, especially those stuck under the pial surfaces. We also perform an ultrasound to check for residue which has been missed.
6:35–6:47 – A gross total resection was achieved. Patient had no neurological deficits.
Outcome: Gross total resection of the insular glioma was achieved (immediate postoperative MRI done within 24 hours) without any fresh neurological deficits. Histopathology was reported as anaplastic astrocytoma, isocitrate dehydrogenases (IDH) mutant, WHO grade III. The patient was further planned for adjuvant radiotherapy and chemotherapy.
Pearls and pitfalls: A good understanding of the functional anatomy of the insular region is indispensable for the surgeon performing insular glioma surgery. As the functional anatomy is highly variable, especially with respect to the cortical opercular regions in the context of a giant insular glioma, it becomes extremely important to rely on awake mapping. A sufficiently large craniotomy to provide a wide exposure of the brain surface in order to perform systematic mapping is recommended. Sleep–awake technique with laryngeal mask airway (LMA) for airway protection is preferable, especially for large tumors requiring longer surgical times. Though we prefer a sleep-awake format, a completely awake format is also possible. Subpial resection of the insular tumor, staying outside the complex maze of vessels on the insular surface is the key to avoid vascular injury. Use of bipolar diathermy should be minimized to avoid thermal injury to critical neurovascular substrates. Subcortical mapping allows for accurate demarcation of the functional boundaries which serve as the limits of the resection at the depth in addition to intraoperative tumor margins, thereby optimizing oncological and functional outcomes. Dynamic subcortical mapping (monopolar motor mapping) can also be performed using a suction monopolar or ultrasonic aspirator coupled with a monopolar stimulator. The posterosuperior quadrant (zone II of Berger-Sanai classification) is the most difficult to resect. A separate parietal opercular window can be utilized to access this area, again necessitating awake cortical mapping. The lenticulostriate vessels need to be carefully preserved. MEP monitoring allows for continuous evaluation of the integrity of the motor pathways during surgery. Anatomically, the Lenticulostriate arteries (LSAs) are located medial to the IFOF and mapping the IFOF serves as a reliable landmark indicating the location of the LSAs which can be preserved. Therefore, direct visualization of the LSAs is not always necessary, minimizing handling of the LSAs and thereby leading to lesser risk of ischemia in its territory. Removal of the superior temporal gyrus is invariably required to access the tumor in the temporal stem, even when there is no direct extension of the tumor into the temporal lobe. Tumor extending medial to the LSAs (into the anterior perforated substance) is unresectable and should not be attempted to avoid permanent deficits.
Even after Yaşargil et al. popularized the transsylvian approach to insular and paralimbic gliomas three decades ago, many surgeons remained reluctant to operate on these rumours. Simon et al. and Sanai et al. demonstrated that survival can be significantly improved by resective surgery for insular glioma. In addition to this, maximizing the extent of resection improves seizure control. Neurocognitive outcomes after surgery are comparable with gliomas at other locations.
Transsylvian approach, however, requires sacrificing some of the branches of the superficial sylvian bridging veins and retraction of the opercula even if the sylvian fissure is widely opened. A significant proportion of postoperative neurological deficits are secondary to ischemia. In a “closed” type of sylvian fissure, as was the case in our patient, this becomes even more challenging. More recently, with the advancement in the understanding of functional anatomy of the brain, and cortical and subcortical mapping with bipolar stimulation, transopercular approaches to insular and paralimbic tumors has been advocated using strategically placed cortical windows in the frontoparietal and temporal opercula. Many of the large insular gliomas show infiltration of the opercular regions which anyways would require removal to ensure complete excision. Moreover, staying below the insula pia (sub-pial dissection) minimizes direct handling of the MCA branches on the insula surface, reducing the risk of vasospasm and subsequent deficits. Objective assessment of trajectories and working angles has also shown that the transopercular approach allows for better exposure to large insular tumors especially those involving the posterior quadrants of the insula (zone II in Berger-Sanai classification) without sacrificing the superficial sylvian bridging veins.
The technique of transopercular removal involves identifying the functional boundaries (cortically and subcortically) through awake mapping, resecting the negatively mapped (for language and motor functions) operculum, pefrorming sub-pial dissection along the pia of sylvian fissure and the insula surface without exposing its contents. Using multiple cortical windows for opercular resection and sub-pial resection avoids vessels that are passing over the involved cortex to supply eloquent areas. Understanding the complex three-dimensional anatomy of the insula and its surrounding regions is critical. The deeper limits of resection are (i) posterior limb of internal capsule in the posterior insular quadrant (ii) the dorsal language pathway: arcuate fasciculus/superior longitudinal fasciculus complex (DES results in speech apraxia, phonological paraphasia and repetition difficulty) in the depths of the frontal exposure, (iii) the ventral semantic pathway underlain by IFOF (DES results in semantic paraphasia in dominant hemisphere, and non-verbal semantic disturbances in non-dominant hemisphere) in the anterior insular and temporal step, (iv) lentiform nucleus (identified by greyish nutmeg appearance; DES induces articulatory disturbances) forming the base of the insular tumor, and (v) anterior perforated substance with the lenticulostriate vessels, medially.
Transient neurological deficits are not uncommon after attempted maximal resection, but usually resolve over time as long as long as there is no vascular insult and the subcortical tracts are preserved. The transopercular approach has been shown to have lower morbidity and by providing better angles for approach, may be a good alternative to the classical transsylvian approach. A staged approach to resect giant tumors can be attempted in slow-growing gliomas as there occurs functional reorganization of the brain due to neuroplasticity.
Ours is a case of large glioma involving all the four quadrants of the insula as well as a large area of the frontal opercula on the dominant side. Transopercular approach under awake setting with cortical and subcortical mapping using DES provided a safe route for gross total resection of the tumor with no significant functional deficits.
A sound knowledge of the complex anatomy of insular and paralimbic region, as well as utilizing a transopercular route with awake mapping and monitoring using appropriate intraoperative adjuncts like DES for mapping and image guidance, will help the surgeon maximize resection while preserving major cerebral functions.
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