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James L. Leach, Reem Awwad, Hansel M. Greiner, Jennifer J. Vannest, Lili Miles and Francesco T. Mangano

OBJECTIVE

Diagnostic criteria for hippocampal malrotation (HIMAL) on brain MRI typically include a rounded hippocampus, vertical collateral sulcus, and architectural blurring. Relationship to epileptogenesis remains speculative, and usefulness for surgical guidance is unknown. The study was performed to determine the prevalence of hippocampal rotational anomalies in a cohort of pediatric patients with intractable epilepsy undergoing evaluation for surgery and to determine the significance of this finding in the context of surgical planning.

METHODS

Forty-eight surgically treated children with intractable epilepsy were compared with matched healthy subjects; reviewers were blinded to surgical side. Each temporal lobe was evaluated for rounded hippocampus, blurring, vertical collateral sulcus, wide choroidal fissure, enlarged temporal horn, low fornix, hippocampal signal, and findings of hippocampal sclerosis. A mesial temporal lobe (MTL) score was calculated by summing the number of features, and the collateral sulcus angle (CSA) was measured in each temporal lobe. Surgical side, pathological diagnosis, and imaging findings elsewhere in the brain were tabulated. Presence of HIMAL, associated imaging features, and MTL score were compared between sides, between epilepsy and control groups, in relationship to side of surgery, and in relationship to postoperative outcome.

RESULTS

Only 3 epilepsy patients (6.2%) and no controls exhibited all 3 features of HIMAL (p = 0.12). Eight of 48 (16.7%) epilepsy versus 2 of 48 (4.6%) control subjects had both a rounded hippocampus and vertical collateral sulcus (suggesting HIMAL) (p = 0.045). In control and epilepsy subjects, most findings were more prevalent on the left, and the left CSA was more vertical (p < 0.0001). Epilepsy subjects had higher MTL scores (z = −2.95, p = 0.002) and more acute CSAs (p = 0.04) than controls. Only lateralizing raw MTL score had a significant association with surgical side (p = 0.03, OR 7.33); however, this was not significant when hippocampal sclerosis cases were excluded. HIMAL findings were more prevalent and MTL scores were higher in patients with resections involving the temporal lobes. On group analysis, HIMAL findings did not predict eventual surgical side and did not predict outcome, although the numbers are small. In 4 patients the abnormally rotated hippocampus was resected and showed hippocampal sclerosis and/or dysplastic changes on histopathology. All of these patients had a good outcome after surgery.

CONCLUSIONS

While increased in prevalence in children with intractable epilepsy, imaging findings of HIMAL did not have preoperative lateralizing utility in this group. Findings of HIMAL (including round hippocampus, architectural blurring, and vertical collateral sulcus) did not predict outcome after surgery, although the small number of patients with these findings limits evaluation. In the small number of patients in which the malrotated hippocampus was removed, outcome was good. Further research is needed to continue to define this association in children with intractable epilepsy, focusing on a temporal lobe cohort.

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Charles B. Stevenson, James L. Leach, Anita Gupta and Kerry R. Crone

Object

The operative indications and treatment algorithms for pediatric patients with Chiari Type I malformation (CM-I) vary widely. When an intradural approach and duraplasty are thought necessary at the time of surgery, neurosurgeons may elect to fulgurate or resect a portion of the cerebellar tonsils. Histological analyses of cerebellar tonsils resected during decompression in pediatric patients with CM-I have revealed multiple abnormal findings including extensive ischemic and degenerative changes. The authors describe an interesting phenomenon of cystic degeneration in the distal ends of the cerebellar tonsils in children undergoing operative treatment of CM-I.

Methods

The authors reviewed the clinical database of 440 pediatric patients who underwent surgical decompression for CM-I performed by a single surgeon. The clinical course, preoperative MR imaging and intraoperative ultrasound characteristics, and histological findings in 3 children found to have tonsillar cystic degeneration were analyzed and detailed.

Results

Cystic changes were subtle but uniformly evident on preoperative MR imaging and were more readily apparent on intraoperative ultrasonography. In each patient, the tonsillar cyst was resected. Histological examination revealed areas of cystic degenerative change characterized by distortion of the normal cerebellar architecture with absent Purkinje and internal granular cell layers. All children experienced improvement in their symptoms, without complication, postoperatively.

Conclusions

Cystic degeneration of the tonsils in pediatric patients with CM-I is an uncommon pathological process most likely resulting from long-standing and excessive compression. Based on their experience, the authors advocate expeditious surgical treatment, including intradural exploration and capacious duraplasty, for patients in whom there is evidence of this phenomenon on preoperative imaging.

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Ellen L. Air, James L. Leach, Ronald E. Warnick and Christopher M. McPherson

Object

Frameless stereotactic biopsy has been shown in multiple studies to be a safe and effective tool for the diagnosis of brain lesions. However, no study has directly evaluated its safety in lesions located in eloquent regions in comparison with noneloquent locations. In this study, the authors determine whether an increased risk of neurological decline is associated with biopsy of lesions in eloquent regions of the brain.

Methods

Medical records, including imaging studies, were reviewed for 284 cases in which frameless stereotactic biopsy procedures were performed by 19 neurosurgeons at 7 institutions between January 2000 and December 2006. Lesion location was classified as eloquent or noneloquent in each patient. The incidence of neurological decline was calculated for each group.

Results

During the study period, 160 of the 284 biopsies predominately involved eloquent regions of the brain. In evaluation of the complication rate with respect to biopsy site, neurological decline occurred in 9 (5.6%) of 160 biopsies in eloquent brain areas and 10 (8.1%) of 124 biopsies in noneloquent regions; this difference was not statistically significant (p = 0.416). A higher number of needle passes was associated with the presence of a postoperative hemorrhage at the biopsy site, although not with a change in the result of neurological examination.

Conclusions

Frameless stereotactic biopsy of lesions located in eloquent brain regions is as safe and effective as biopsy of lesions in noneloquent regions. Therefore, with careful planning, frameless stereotactic biopsy remains a valuable and safe tool for diagnosis of brain lesions, independent of lesion location.

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Ravindra Arya, Jeffrey R. Tenney, Paul S. Horn, Hansel M. Greiner, Katherine D. Holland, James L. Leach, Michael J. Gelfand, Leonid Rozhkov, Hisako Fujiwara, Douglas F. Rose, David N. Franz and Francesco T. Mangano

OBJECT

Tuberous sclerosis complex (TSC) with medically refractory epilepsy is characterized by multifocal brain abnormalities, traditionally indicating poor surgical candidacy. This single-center, retrospective study appraised seizurerelated, neuropsychological, and other outcomes of resective surgery in TSC patients with medically refractory epilepsy, and analyzed predictors for these outcomes.

METHODS

Patients with multilesional TSC who underwent epilepsy surgery between 2007 and 2012 were identified from an electronic database. All patients underwent multimodality noninvasive and subsequent invasive evaluation. Seizure outcomes were classified using the International League Against Epilepsy (ILAE) scale. The primary outcome measure was complete seizure remission (ILAE Class 1). Secondary outcome measures included 50% responder rate, change in full-scale IQ, electroencephalography improvement, and reduction in antiepileptic drug (AED) burden.

RESULTS

A total of 37 patients with TSC underwent resective surgery during the study period. After a mean follow-up of 5.68 ± 3.67 years, 56.8% achieved complete seizure freedom (ILAE Class 1) and 86.5% had ILAE Class 4 outcomes or better. The full-scale IQ on follow-up was significantly higher in patients with ILAE Class 1 outcome (66.70 ± 12.36) compared with those with ILAE Class 2 or worse outcomes (56.00 ± 1.41, p = 0.025). In 62.5% of the patients with ILAE Class 2 or worse outcomes, the number of AEDs were found to be significantly reduced (p = 0.004).

CONCLUSIONS

This study substantiates the evidence for efficacy of resective epilepsy surgery in patients with bilateral multilesional TSC. More than half of the patients were completely seizure free. Additionally, a high proportion achieved clinically meaningful reduction in seizure burden and the number of AEDs.

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James L. Leach, Lili Miles, David M. Henkel, Hansel M. Greiner, Marcia K. Kukreja, Katherine D. Holland, Douglas F. Rose, Bin Zhang and Francesco T. Mangano

Object

The authors conducted a study to correlate histopathological features, MRI findings, and postsurgical outcomes in children with cortical dysplasia (CD) by performing a novel resection site–specific evaluation.

Methods

The study cohort comprised 43 children with intractable epilepsy and CD. The MR image review was blinded to pathology but with knowledge of the resection location. An MRI score (range 0–7) was calculated for each resection region based on the number of imaging features of CD and was classified as “lesional” or “nonlesional” according to all imaging features. Outcome was determined using the International League Against Epilepsy (ILAE) scale. The determination of pathological CD type was based on the ILAE 2011 consensus classification system, and the cortical gliosis pattern was assessed on GFAP staining.

Results

There were 89 resection regions (50 ILAE Type I, 29 Type IIa, and 10 Type IIb). Eleven (25.6%) of 43 children had more than one type of CD. The authors observed MRI abnormalities in 63% of patients, characteristic enough to direct resection (lesional) in 42%. Most MRI features, MRI score ≥ 3, and lesional abnormalities were more common in patients with Type II CD. Increased cortical signal was more common in those with Type IIb (70%) rather than Type IIa (17.2%) CD (p = 0.004). A good outcome was demonstrated in 39% of children with Type I CD and 72% of those with Type II CD (61% in Type IIa and 100% in Type IIb) (p = 0.03). A lesional MRI abnormality and an MRI score greater than 3 correlated with good outcome in 78% and 90% of patients, respectively (p < 0.03). Diffuse cortical gliosis was more prevalent in Type II CD and in resection regions exhibiting MRI abnormalities. Complete surgical exclusion of the MRI abnormality was associated with a better postoperative outcome.

Conclusions

This study provides a detailed correlation of MRI findings, neuropathological features, and outcomes in children with intractable epilepsy by using a novel resection site–specific evaluation. Because 25% of the patients had multiple CD subtypes, a regional analysis approach was mandated. Those children with lesional MRI abnormalities, Type II CD, and surgical exclusion of the MRI abnormality had better outcomes. Type II CD is more detectable by MRI than other types, partly because of the greater extent of associated gliosis in Type II. Although MRI findings were correlated with the pathological CD type and outcome in this study, the majority of patients (58%) did not have MRI findings that could direct surgical therapy, underscoring the need for improved MRI techniques for detection and for the continued use of multimodal evaluation methods in patient selection.

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Alan M. Chen, Kunal B. Karani, J. Michael Taylor, Bin Zhang, Andrew Furthmiller, Gabriel De Vela, James L. Leach, Sudhakar Vadivelu and Todd A. Abruzzo

OBJECTIVE

Although intracranial arterial aneurysms (IAAs) of childhood are usually idiopathic, it is possible that underlying arteriopathy escapes detection when using conventional diagnostic tools. Quantitative arterial tortuosity (QAT) has been studied as a biomarker of arteriopathy. The authors analyzed cervicocerebral QAT in children with idiopathic IAAs to assess the possibility of arteriopathy.

METHODS

Cases were identified by text-string searches of imaging reports spanning the period January 1993 through June 2017. QAT of cervicocerebral arterial segments was measured from cross-sectional studies using image-processing software. Other imaging and clinical data were confirmed by retrospective electronic record review. Children with idiopathic IAAs and positive case controls, with congenital arteriopathy differentiated according to aneurysm status (with and without an aneurysm), were compared to each other and to healthy controls without vascular risk factors.

RESULTS

Cervicocerebral QAT was measured in 314 children: 24 with idiopathic IAAs, 163 with congenital arteriopathy (including 14 arteriopathic IAAs), and 127 healthy controls. QAT of all vertebrobasilar segments was larger in children with IAAs (idiopathic and arteriopathic forms) (p < 0.05). In children with congenital arteriopathy without an aneurysm, QAT was decreased for the distal cervical vertebral arteries and increased for the supraspinal vertebral artery relative to healthy children. QAT of specific cervicocerebral segments correlated with IAA size and rupture status.

CONCLUSIONS

Cervicocerebral QAT is a biomarker of arteriopathy in children with IAA, even in the absence of other disease markers. Additional findings suggest a correlation of cervicocerebral QAT with IAA size and rupture status and with the presence of IAA in children with congenital arteriopathy.

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Ravindra Arya, Francesco T. Mangano, Paul S. Horn, Sabrina K. Kaul, Serena K. Kaul, Celie Roth, James L. Leach, Michele Turner, Katherine D. Holland and Hansel M. Greiner

OBJECTIVE

There is emerging data that adults with temporal lobe epilepsy (TLE) without a discrete lesion on brain MRI have surgical outcomes comparable to those with hippocampal sclerosis (HS). However, pediatric TLE is different from its adult counterpart. In this study, the authors investigated if the presence of a potentially epileptogenic lesion on presurgical brain MRI influences the long-term seizure outcomes after pediatric temporal lobectomy.

METHODS

Children who underwent temporal lobectomy between 2007 and 2015 and had at least 1 year of seizure outcomes data were identified. These were classified into lesional and MRI-negative groups based on whether an epilepsy-protocol brain MRI showed a lesion sufficiently specific to guide surgical decisions. These patients were also categorized into pure TLE and temporal plus epilepsies based on the neurophysiological localization of the seizure-onset zone. Seizure outcomes at each follow-up visit were incorporated into a repeated-measures generalized linear mixed model (GLMM) with MRI status as a grouping variable. Clinical variables were incorporated into GLMM as covariates.

RESULTS

One hundred nine patients (44 females) were included, aged 5 to 21 years, and were classified as lesional (73%), MRI negative (27%), pure TLE (56%), and temporal plus (44%). After a mean follow-up of 3.2 years (range 1.2–8.8 years), 66% of the patients were seizure free for ≥ 1 year at last follow-up. GLMM analysis revealed that lesional patients were more likely to be seizure free over the long term compared to MRI-negative patients for the overall cohort (OR 2.58, p < 0.0001) and for temporal plus epilepsies (OR 1.85, p = 0.0052). The effect of MRI lesion was not significant for pure TLE (OR 2.64, p = 0.0635). Concordance of ictal electroencephalography (OR 3.46, p < 0.0001), magnetoencephalography (OR 4.26, p < 0.0001), and later age of seizure onset (OR 1.05, p = 0.0091) were associated with a higher likelihood of seizure freedom. The most common histological findings included cortical dysplasia types 1B and 2A, HS (40% with dual pathology), and tuberous sclerosis.

CONCLUSIONS

A lesion on presurgical brain MRI is an important determinant of long-term seizure freedom after pediatric temporal lobectomy. Pediatric TLE is heterogeneous regarding etiologies and organization of seizure-onset zones with many patients qualifying for temporal plus nosology. The presence of an MRI lesion determined seizure outcomes in patients with temporal plus epilepsies. However, pure TLE had comparable surgical seizure outcomes for lesional and MRI-negative groups.