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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.

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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.

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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.

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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.

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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.

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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.

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Ramin A. Morshed, Jacob S. Young, Seunggu J. Han, Shawn L. Hervey-Jumper and Mitchel S. Berger

OBJECTIVE

Greater extent of resection (EOR) improves overall survival and progression-free survival for patients with low- and high-grade glioma. While resection for newly diagnosed insular gliomas can be performed with minimal morbidity, perioperative morbidity is not clearly defined for patients undergoing a repeat resection for recurrent insular gliomas. In this study the authors report on tumor characteristics, tumor EOR, and functional outcomes in patients undergoing reoperation for recurrent insular glioma.

METHODS

Adult patients with insular gliomas (WHO grades II–IV) who underwent index resection followed by reoperation were identified through the University of California San Francisco Brain Tumor Center. Treatment history and functional outcomes were collected retrospectively from the electronic medical record. Pre- and postoperative tumor volumes were quantified using software with region-of-interest analysis based on FLAIR and T1-weighted postgadolinium sequences from pre- and postoperative MRI.

RESULTS

Forty-four patients (63.6% male, 36.4% female) undergoing 49 reoperations for recurrent insular tumors were identified with a median follow-up of 741 days. Left- and right-sided tumors comprised 52.3% and 47.7% of the cohort, respectively. WHO grade II, III, and IV gliomas comprised 46.9%, 28.6%, and 24.5% of the cohort, respectively. Ninety-five percent (95.9%) of cases involved language and/or motor mapping. Median EOR of the insular component of grade II, III, and IV tumors were 82.1%, 75.0%, and 94.6%, respectively. EOR during reoperation was not impacted by Berger-Sanai insular zone or tumor side. At the time of reoperation, 44.9% of tumors demonstrated malignant transformation to a higher WHO grade. Ninety-day postoperative assessment confirmed that 91.5% of patients had no new postoperative deficit attributable to surgery. Of those with new deficits, 3 (6.4%) had a visual field cut and 1 (2.1%) had hemiparesis (strength grade 1–2/5). The presence of a new postoperative deficit did not vary with EOR.

CONCLUSIONS

Recurrent insular gliomas, regardless of insular zone and pathology, may be reoperated on with an overall acceptable degree of resection and safety despite their anatomical and functional complexities. The use of intraoperative mapping utilizing asleep or awake methods may reduce morbidity to acceptable rates despite prior surgery.

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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.

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Shawn L. Hervey-Jumper, Gail M. Annich, Andrea R. Yancon, Hugh J. L. Garton, Karin M. Muraszko and Cormac O. Maher

Object

Extracorporeal membrane oxygenation (ECMO) is a potentially life-saving treatment for patients in refractory cardiorespiratory failure. Neurological complications that result from ECMO treatment are known to significantly impact patient survival and quality of life. The purpose of this study was to review the incidence of neurological complications of ECMO in the pediatric population and the role of neurosurgery in the treatment of these patients.

Methods

Data were obtained from the national Extracorporeal Life Support Organization (ELSO) Registry for the years 1990 to 2009. The neurological complications recorded by the registry include CNS hemorrhage, CNS infarction, and seizure. The ECMO Registry at the authors' institution was then searched, and 3 pediatric patients who had undergone craniotomy during ECMO treatment were identified.

Results

Children in the ELSO Registry who were treated with ECMO survived to hospital discharge in 65% of cases. Intracranial hemorrhage occurred in 7.4% of the ECMO-treated patients, with 36% of those surviving to hospital discharge. Hemorrhage was more likely in patients younger than 30 days old and in those requiring ECMO for cardiac indications. Cerebral infarction occurred in 5.7% of all ECMO-treated patients. Clinically diagnosed seizures occurred in 8.4% of all ECMO-treated patients. The ECMO Registry at the authors' institution revealed that 1898 patients were treated there. Intracranial hemorrhage was diagnosed in 81 patients (5.8%), and 3 of these patients were treated with craniotomy. Two of the patients were alive with minimal neurological impairment and normal school performance at 10 and 16 years of follow-up.

Conclusions

Intracranial hemorrhage is a serious complication of ECMO treatment. While the surgical risk is substantial, there may be a role for surgical evacuation of hemorrhage in well-selected patients.

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Darryl Lau, Shawn L. Hervey-Jumper, Susan Chang, Annette M. Molinaro, Michael W. McDermott, Joanna J. Phillips and Mitchel S. Berger

OBJECT

There is evidence that 5-aminolevulinic acid (ALA) facilitates greater extent of resection and improves 6-month progression-free survival in patients with high-grade gliomas. But there remains a paucity of studies that have examined whether the intensity of ALA fluorescence correlates with tumor cellularity. Therefore, a Phase II clinical trial was undertaken to examine the correlation of intensity of ALA fluorescence with the degree of tumor cellularity.

METHODS

A single-center, prospective, single-arm, open-label Phase II clinical trial of ALA fluorescence-guided resection of high-grade gliomas (Grade III and IV) was held over a 43-month period (August 2010 to February 2014). ALA was administered at a dose of 20 mg/kg body weight. Intraoperative biopsies from resection cavities were collected. The biopsies were graded on a 4-point scale (0 to 3) based on ALA fluorescence intensity by the surgeon and independently based on tumor cellularity by a neuropathologist. The primary outcome of interest was the correlation of ALA fluorescence intensity to tumor cellularity. The secondary outcome of interest was ALA adverse events. Sensitivities, specificities, positive predictive values (PPVs), negative predictive values (NPVs), and Spearman correlation coefficients were calculated.

RESULTS

A total of 211 biopsies from 59 patients were included. Mean age was 53.3 years and 59.5% were male. The majority of biopsies were glioblastoma (GBM) (79.7%). Slightly more than half (52.5%) of all tumors were recurrent. ALA intensity of 3 correlated with presence of tumor 97.4% (PPV) of the time. However, absence of ALA fluorescence (intensity 0) correlated with the absence of tumor only 37.7% (NPV) of the time. For all tumor types, GBM, Grade III gliomas, and recurrent tumors, ALA intensity 3 correlated strongly with cellularity Grade 3; Spearman correlation coefficients (r) were 0.65, 0.66, 0.65, and 0.62, respectively. The specificity and PPV of ALA intensity 3 correlating with cellularity Grade 3 ranged from 95% to 100% and 86% to 100%, respectively. In biopsies without tumor (cellularity Grade 0), 35.4% still demonstrated ALA fluorescence. Of those biopsies, 90.9% contained abnormal brain tissue, characterized by reactive astrocytes, scattered atypical cells, or inflammation, and 8.1% had normal brain. In nonfluorescent (ALA intensity 0) biopsies, 62.3% had tumor cells present. The ALA-associated complication rate among the study cohort was 3.4%.

CONCLUSIONS

The PPV of utilizing the most robust ALA fluorescence intensity (lava-like orange) as a predictor of tumor presence is high. However, the NPV of utilizing the absence of fluorescence as an indicator of no tumor is poor. ALA intensity is a strong predictor for degree of tumor cellularity for the most fluorescent areas but less so for lower ALA intensities. Even in the absence of tumor cells, reactive changes may lead to ALA fluorescence.