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Insular glioma surgery: an evolution of thought and practice

JNSPG 75th Anniversary Invited Review Article

Shawn L. Hervey-Jumper and Mitchel S. Berger

OBJECTIVE

The goal of this article is to review the history of surgery for low- and high-grade gliomas located within the insula with particular focus on microsurgical technique, anatomical considerations, survival, and postoperative morbidity.

METHODS

The authors reviewed the literature for published reports focused on insular region anatomy, neurophysiology, surgical approaches, and outcomes for adults with World Health Organization grade II–IV gliomas.

RESULTS

While originally considered to pose too great a risk, insular glioma surgery can be performed safely due to the collective efforts of many individuals. Similar to resection of gliomas located within other cortical regions, maximal resection of gliomas within the insula offers patients greater survival time and superior seizure control for both newly diagnosed and recurrent tumors in this region. The identification and the preservation of M2 perforating and lateral lenticulostriate arteries are critical steps to preventing internal capsule stroke and hemiparesis. The transcortical approach and intraoperative mapping are useful tools to maximize safety.

CONCLUSIONS

The insula’s proximity to middle cerebral and lenticulostriate arteries, primary motor areas, and perisylvian language areas makes accessing and resecting gliomas in this region challenging. Maximal safe resection of insular gliomas not only is possible but also is associated with excellent outcomes and should be considered for all patients with low- and high-grade gliomas in this area.

In Journal of Neurosurgery Volume 130: Issue 1 (Jan 2019)

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Intraoperative mapping during repeat awake craniotomy reveals the functional plasticity of adult cortex

Derek G. Southwell, Shawn L. Hervey-Jumper, David W. Perry, and Mitchel S. Berger

OBJECT

To avoid iatrogenic injury during the removal of intrinsic cerebral neoplasms such as gliomas, direct electrical stimulation (DES) is used to identify cortical and subcortical white matter pathways critical for language, motor, and sensory function. When a patient undergoes more than 1 brain tumor resection as in the case of tumor recurrence, the use of DES provides an unusual opportunity to examine brain plasticity in the setting of neurological disease.

METHODS

The authors examined 561 consecutive cases in which patients underwent DES mapping during surgery forglioma resection. “Positive” and “negative” sites—discrete cortical regions where electrical stimulation did (positive) or did not (negative) produce transient sensory, motor, or language disturbance—were identified prior to tumor resection and documented by intraoperative photography for categorization into functional maps. In this group of 561 patients, 18 were identified who underwent repeat surgery in which 1 or more stimulation sites overlapped with those tested during the initial surgery. The authors compared intraoperative sensory, motor, or language mapping results between initial and repeat surgeries, and evaluated the clinical outcomes for these patients.

RESULTS

A total of 117 sites were tested for sensory (7 sites, 6.0%), motor (9 sites, 7.7%), or language (101 sites, 86.3%) function during both initial and repeat surgeries. The mean interval between surgical procedures was 4.1 years. During initial surgeries, 95 (81.2%) of 117 sites were found to be negative and 22 (18.8%) of 117 sites were found to be positive. During repeat surgeries, 103 (88.0%) of 117 sites were negative and 14 (12.0%) of 117 were positive. Of the 95 sites that were negative at the initial surgery, 94 (98.9%) were also negative at the repeat surgery, while 1 (1.1%) site was found to be positive. Of the 22 sites that were initially positive, 13 (59.1%) remained positive at repeat surgery, while 9 (40.9%) had become negative for function. Overall, 6 (33.3%) of 18 patients exhibited loss of function at 1 or more motor or language sites between surgeries. Loss of function at these sites was not associated with neurological impairment at the time of repeat surgery, suggesting that neurological function was preserved through neural circuit reorganization or activation of latent functional pathways.

CONCLUSIONS

The adult central nervous system reorganizes motor and language areas in patients with glioma. Ultimately, adult neural plasticity may help to preserve motor and language function in the presence of evolving structural lesions. The insight gained from this subset of patients has implications for our understanding of brain plasticity in clinical settings.

In Journal of Neurosurgery Volume 124 (2016): Issue 5 (May 2016)

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Intraoperative perception and estimates on extent of resection during awake glioma surgery: overcoming the learning curve

Darryl Lau, Shawn L. Hervey-Jumper, Seunggu J. Han, and Mitchel S. Berger

OBJECTIVE

There is ample evidence that extent of resection (EOR) is associated with improved outcomes for glioma surgery. However, it is often difficult to accurately estimate EOR intraoperatively, and surgeon accuracy has yet to be reviewed. In this study, the authors quantitatively assessed the accuracy of intraoperative perception of EOR during awake craniotomy for tumor resection.

METHODS

A single-surgeon experience of performing awake craniotomies for tumor resection over a 17-year period was examined. Retrospective review of operative reports for quantitative estimation of EOR was recorded. Definitive EOR was based on postoperative MRI. Analysis of accuracy of EOR estimation was examined both as a general outcome (gross-total resection [GTR] or subtotal resection [STR]), and quantitatively (5% within EOR on postoperative MRI). Patient demographics, tumor characteristics, and surgeon experience were examined. The effects of accuracy on motor and language outcomes were assessed.

RESULTS

A total of 451 patients were included in the study. Overall accuracy of intraoperative perception of whether GTR or STR was achieved was 79.6%, and overall accuracy of quantitative perception of resection (within 5% of postoperative MRI) was 81.4%. There was a significant difference (p = 0.049) in accuracy for gross perception over the 17-year period, with improvement over the later years: 1997–2000 (72.6%), 2001–2004 (78.5%), 2005–2008 (80.7%), and 2009–2013 (84.4%). Similarly, there was a significant improvement (p = 0.015) in accuracy of quantitative perception of EOR over the 17-year period: 1997–2000 (72.2%), 2001–2004 (69.8%), 2005–2008 (84.8%), and 2009–2013 (93.4%). This improvement in accuracy is demonstrated by the significantly higher odds of correctly estimating quantitative EOR in the later years of the series on multivariate logistic regression. Insular tumors were associated with the highest accuracy of gross perception (89.3%; p = 0.034), but lowest accuracy of quantitative perception (61.1% correct; p < 0.001) compared with tumors in other locations. Even after adjusting for surgeon experience, this particular trend for insular tumors remained true. The absence of 1p19q co-deletion was associated with higher quantitative perception accuracy (96.9% vs 81.5%; p = 0.051). Tumor grade, recurrence, diagnosis, and isocitrate dehydrogenase-1 (IDH-1) status were not associated with accurate perception of EOR. Overall, new neurological deficits occurred in 8.4% of cases, and 42.1% of those new neurological deficits persisted after the 3-month follow-up. Correct quantitative perception was associated with lower postoperative motor deficits (2.4%) compared with incorrect perceptions (8.0%; p = 0.029). There were no detectable differences in language outcomes based on perception of EOR.

CONCLUSIONS

The findings from this study suggest that there is a learning curve associated with the ability to accurately assess intraoperative EOR during glioma surgery, and it may take more than a decade to be truly proficient. Understanding the factors associated with this ability to accurately assess EOR will provide safer surgeries while maximizing tumor resection.

In Journal of Neurosurgery Volume 128: Issue 5 (May 2018)

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Cerebrospinal fluid leak with recurrent meningitis following tonsillectomy

Case report

Shawn L. Hervey-Jumper, Ahmer K. Ghori, Douglas J. Quint, Lawrence J. Marentette, and Cormac O. Maher

The authors report an unusual case of bilateral large petrous apex cephaloceles in a 14-year-old boy with a history of recurrent meningitis. Although these lesions are rare and usually asymptomatic, surgical correction is recommended if they are associated with a persistent CSF leak. In this patient, the extensive bilateral cranial defects were not adequately treated by an intracranial approach alone. Repair of a defect in the posterior pharyngeal wall, the site of a prior tonsillectomy, ultimately resulted in repair of the CSF fistula.

In Journal of Neurosurgery: Pediatrics Volume 5: Issue 3 (Mar 2010)

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Macrovascular decompression of the median nerve for posttraumatic neuralgic limb pain

Case report

Aqueel Pabaney, Shawn L. Hervey-Jumper, Joseph Domino, Cormac O. Maher, and Lynda J. S. Yang

Neuropathic pain is rare in children, and few reports provide adequate guidelines for treatment. The authors describe the successful treatment of tardy neuropathic pain via macrovascular decompression in a 15-year-old boy who presented with progressive pain 11 years following trauma to the upper extremity that had required surgical repair of the brachial artery. Examination revealed mild chronic median and ulnar motor neuropathy as well as recent progressive lancinating pain and a Tinel sign at the prior scar. A soft tissue mass in the neurovascular bundle at the site of previous injury was noted on MRI. Surgical exploration demonstrated an altered anatomical relationship of the previously repaired brachial artery and the median nerve, resulting in pulsatile compression of the median nerve by the brachial artery. Neurolysis and decompression of the median nerve with physical separation from the brachial artery resulted in immediate pain relief.

This is the first report of macrovascular decompression of a major peripheral nerve with complete symptom resolution. Noninvasive imaging together with a thorough history and physical examination can support identification of this potential etiology of peripheral neuralgic pain. Recognition and treatment of this uncommon problem may yield improved outcomes for children with neuropathic pain.

In Journal of Neurosurgery: Pediatrics Volume 12 (2013): Issue 3 (Sep 2013)

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Frontal-to-temporal horn shunt as treatment for temporal horn entrapment

Technical note

Shawn L. Hervey-Jumper, John E. Ziewacz, Jason A. Heth, and Stephen E. Sullivan

In cases of temporal horn entrapment caused by primary malignant central nervous system tumors, the goal is to restore physiological flow of cerebrospinal fluid (CSF) while preventing the spread of malignant tumor cells to distant sites. This goal is usually accomplished by placement of a traditional ventriculoperitoneal, ventriculopleural, or ventriculoatrial shunt. In this study, the authors describe a novel treatment approach using placement of a frontal-to-temporal horn shunt as an alternative to distal CSF diversion. Stereotactic surgery was used for placement of frontal-to-temporal horn shunts in 3 patients who presented with focal compressive symptoms caused by temporal horn dilation. Serial imaging studies confirmed temporal horn decompression with symptom resolution after a maximum of 20 months of follow-up (minimum 2 months in 1 patient who died of tumor progression). The authors believe this simple technique may be considered for use in all patients with neurological symptoms resulting from temporal horn dilation caused by malignant central nervous system neoplasms in which seeding of distant sites by CSF diversion is a concern.

In Journal of Neurosurgery Volume 112 (2010): Issue 2 (Feb 2010)

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Surgical assessment of the insula. Part 1: surgical anatomy and morphometric analysis of the transsylvian and transcortical approaches to the insula

Arnau Benet, Shawn L. Hervey-Jumper, Jose Juan González Sánchez, Michael T. Lawton, and Mitchel S. Berger

OBJECT

Transcortical and transsylvian corridors have been previously described as the main surgical approaches to the insula, but there is insufficient evidence to support one approach versus the other. The authors performed a cadaveric comparative study regarding insular exposure, surgical window and freedom, between the transcortical and transsylvian approaches (with and without cutting superficial sylvian bridging veins). Surgical anatomy and skull surface reference points to the different insular regions are also described.

METHODS

Sixteen cadaveric specimens were embalmed with a customized formula to enhance neurosurgical simulation. Two different blocks were defined in the study: first, transsylvian without (TS) and with the superficial sylvian bridging veins cut (TSVC) and transcortical (TC) approaches to the insula were simulated in all (16) specimens. Insular surface exposure, surgical window and surgical freedom were calculated for each procedure and related to the Berger-Sanai insular glioma classification (Zones I–IV) in 10 specimens. Second, the venous drainage pattern and anatomical landmarks considered critical for surgical planning were studied in all specimens.

RESULTS

In the insular Zone I (anterior-superior), the TC approach provided the best insular exposure compared with both TS and TSVC. The surgical window obtained with the TC approach was also larger than that obtained with the TS. The TC approach provided 137% more surgical freedom than the TS approach. Only the TC corridor provided complete insular exposure. In Zone II (posterior-superior), results depended on the degree of opercular resection. Without resection of the precentral gyrus in the operculum, insula exposure, surgical windows and surgical freedom were equivalent. If the opercular cortex was resected, the insula exposure and surgical freedom obtained through the TC approach was greater to that of the other groups. In Zone III (posterior-inferior), the TC approach provided better surgical exposure than the TS, yet similar to the TSVC. The TC approach provided the best insular exposure, surgical window, and surgical freedom if components of Heschl’s gyrus were resected. In Zone IV (anterior-inferior), the TC corridor provided better exposure than both the TS and the TSVC. The surgical window was equivalent. Surgical freedom provided by the TC was greater than the TS approach. This zone was completely exposed only with the TC approach. A dominant anterior venous drainage was found in 87% of the specimens. In this group, 50% of the specimens had good alternative venous drainage. The sylvian fissure corresponded to the superior segment of the squamosal suture in 14 of 16 specimens. The foramen of Monro was 1.9 cm anterior and 4.42 cm superior to the external acoustic meatus. The M2 branch over the central sulcus of the insula became the precentral M4 (rolandic) artery in all specimens.

CONCLUSIONS

Overall, the TC approach to the insula provided better insula exposure and surgical freedom compared with the TS and the TSVC. Cortical and subcortical mapping is critical during the TC approach to the posterior zones (II and III), as the facial motor and somatosensory functions (Zone II) and language areas (Zone III) may be involved. The evidence provided in this study may help the neurosurgeon when approaching insular gliomas to achieve a greater extent of tumor resection via an optimal exposure.

In Journal of Neurosurgery Volume 124 (2016): Issue 2 (Feb 2016)

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Surgical assessment of the insula. Part 2: validation of the Berger-Sanai zone classification system for predicting extent of glioma resection

Shawn L. Hervey-Jumper, Jing Li, Joseph A. Osorio, Darryl Lau, Annette M. Molinaro, Arnau Benet, and Mitchel S. Berger

OBJECT

Though challenging, maximal safe resection of insular gliomas enhances overall and progression-free survival and deters malignant transformation. Previously published reports have shown that surgery can be performed with low morbidity. The authors previously described a Berger-Sanai zone classification system for insular gliomas. Using a subsequent dataset, they undertook this study to validate this zone classification system for predictability of extent of resection (EOR) in patients with insular gliomas.

METHODS

The study population included adults who had undergone resection of WHO Grade II, III, or IV insular gliomas. In accordance with our prior published report, tumor location was classified according to the Berger-Sanai quadrant-style classification system into Zones I through IV. Interobserver variability was analyzed using a cohort of newly diagnosed insular gliomas and independent classification scores given by 3 neurosurgeons at various career stages. Glioma volumes were analyzed using FLAIR and T1-weighted contrast-enhanced MR images.

RESULTS

One hundred twenty-nine procedures involving 114 consecutive patients were identified. The study population from the authors’ previously published experience included 115 procedures involving 104 patients. Thus, the total experience included 244 procedures involving 218 patients with insular gliomas treated at the authors’ institution. The most common presenting symptoms were seizure (68.2%) and asymptomatic recurrence (17.8%). WHO Grade II glioma histology was the most common (54.3%), followed by Grades III (34.1%) and IV (11.6%). The median tumor volume was 48.5 cm3. The majority of insular gliomas were located in the anterior portion of the insula with 31.0% in Zone I, 10.9% in Zone IV, and 16.3% in Zones I+IV. The Berger-Sanai zone classification system was highly reliable, with a kappa coefficient of 0.857. The median EOR for all zones was 85%. Comparison of EOR between the current and prior series showed no change and Zone I gliomas continue to have the highest median EOR. Short- and long-term neurological complications remain low, and zone classification correlated with short-term complications, which were highest in Zone I and in Giant insular gliomas.

CONCLUSIONS

The previously proposed Berger-Sanai classification system is highly reliable and predictive of insular glioma EOR and morbidity.

In Journal of Neurosurgery Volume 124 (2016): Issue 2 (Feb 2016)

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Awake craniotomy to maximize glioma resection: methods and technical nuances over a 27-year period

Shawn L. Hervey-Jumper, Jing Li, Darryl Lau, Annette M. Molinaro, David W. Perry, Lingzhong Meng, and Mitchel S. Berger

OBJECT

Awake craniotomy is currently a useful surgical approach to help identify and preserve functional areas during cortical and subcortical tumor resections. Methodologies have evolved over time to maximize patient safety and minimize morbidity using this technique. The goal of this study is to analyze a single surgeon's experience and the evolving methodology of awake language and sensorimotor mapping for glioma surgery.

METHODS

The authors retrospectively studied patients undergoing awake brain tumor surgery between 1986 and 2014. Operations for the initial 248 patients (1986–1997) were completed at the University of Washington, and the subsequent surgeries in 611 patients (1997–2014) were completed at the University of California, San Francisco. Perioperative risk factors and complications were assessed using the latter 611 cases.

RESULTS

The median patient age was 42 years (range 13–84 years). Sixty percent of patients had Karnofsky Performance Status (KPS) scores of 90–100, and 40% had KPS scores less than 80. Fifty-five percent of patients underwent surgery for high-grade gliomas, 42% for low-grade gliomas, 1% for metastatic lesions, and 2% for other lesions (cortical dysplasia, encephalitis, necrosis, abscess, and hemangioma). The majority of patients were in American Society of Anesthesiologists (ASA) Class 1 or 2 (mild systemic disease); however, patients with severe systemic disease were not excluded from awake brain tumor surgery and represented 15% of study participants. Laryngeal mask airway was used in 8 patients (1%) and was most commonly used for large vascular tumors with more than 2 cm of mass effect. The most common sedation regimen was propofol plus remifentanil (54%); however, 42% of patients required an adjustment to the initial sedation regimen before skin incision due to patient intolerance. Mannitol was used in 54% of cases. Twelve percent of patients were active smokers at the time of surgery, which did not impact completion of the intraoperative mapping procedure. Stimulation-induced seizures occurred in 3% of patients and were rapidly terminated with ice-cold Ringer's solution. Preoperative seizure history and tumor location were associated with an increased incidence of stimulation-induced seizures. Mapping was aborted in 3 cases (0.5%) due to intraoperative seizures (2 cases) and patient emotional intolerance (1 case). The overall perioperative complication rate was 10%.

CONCLUSIONS

Based on the current best practice described here and developed from multiple regimens used over a 27-year period, it is concluded that awake brain tumor surgery can be safely performed with extremely low complication and failure rates regardless of ASA classification; body mass index; smoking status; psychiatric or emotional history; seizure frequency and duration; and tumor site, size, and pathology.

In Journal of Neurosurgery Volume 123 (2015): Issue 2 (Aug 2015): Pages 297-A541

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Management of intractable chronic cough during awake craniotomy: illustrative case

Yena Kang, Robbi A. Kupfer, Elizabeth Ford-Baldner, Karen J. Kluin, Shawn L. Hervey-Jumper, and Robert J. Morrison

BACKGROUND

Chronic cough is a common but challenging clinical condition that can adversely affect the safety of awake surgical endeavors such as awake craniotomy (AC). This case lesson highlighted a patient with severe refractory chronic cough undergoing AC for resection of a recurrent left frontal, insula, anterior temporal anaplastic ependymoma of the eloquent cortex.

OBSERVATIONS

The patient was successfully managed using a multifaceted medical treatment regimen combined with preoperative and intraoperative cough suppression therapy with a speech-language pathologist. The patient coughed only once intraoperatively and had a positive outcome.

LESSONS

Chronic cough is often multifactorial and requires a multifaceted treatment approach. Despite this challenge, select patients can successfully be navigated through AC with appropriate treatment for their condition. A review of neurogenic cough and modern treatments, which were used in this patient and would be helpful to neurologists or neurosurgeons, are also discussed.

In Journal of Neurosurgery: Case Lessons Volume 2 (2021): Issue 25 (Dec 2021)