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Thomas Guiho, Christine Azevedo-Coste, David Guiraud, Claire Delleci, Grégoire Capon, Natalia Delgado-Piccoli, Luc Bauchet and Jean-Rodolphe Vignes

OBJECTIVE

Spinal cord injuries (SCIs) result in loss of movement and sensory feedback, but also organ dysfunction. Nearly all patients with complete SCI lose bladder control and are prone to kidney failure if intermittent catheterization is not performed. Electrical stimulation of sacral spinal roots was initially considered to be a promising approach for restoring continence and micturition control, but many patients are discouraged by the need for surgical deafferentation as it could lead to a loss of sensory functions and reflexes. Nevertheless, recent research findings highlight the renewed interest in spinal cord stimulation (SCS). It is thought that synergic recruitment of spinal fibers could be achieved by stimulating the spinal neural networks involved in regulating physiological processes. Paradoxically, most of these recent studies focused on locomotor issues, while few addressed visceral dysfunction. This could at least partially be attributed to the lack of methodological tools. In this study, the authors aim to fill this gap by presenting a comprehensive method for investigating the potential of SCS to restore visceral functions in domestic pigs, a large-animal model considered to be a close approximation to humans.

METHODS

This methodology was tested in 7 female pigs (Landrace pig breed, 45–60 kg, 4 months old) during acute experiments. A combination of morphine and propofol was used for anesthesia when transurethral catheterization and lumbosacral laminectomy (L4–S4) were performed. At the end of the operation, spinal root stimulation (L6–S5) and urodynamic recordings were performed to compare the evoked responses with those observed intraoperatively in humans.

RESULTS

Nervous excitability was preserved despite long-term anesthesia (mean 8.43 ± 1.5 hours). Transurethral catheterization and conventional laminectomy were possible while motor responses (gluteus muscle monitoring) were unaffected throughout the procedure. Consistent detrusor (approximately 25 cm H2O) and sphincter responses were obtained, whereas spinal root stimulation elicited detrusor and external urethral sphincter co-contractions similar to those observed intraoperatively in humans.

CONCLUSIONS

Pigs represent an ideal model for SCS studies aimed at visceral function investigation and restoration because of the close similarities between female domestic pigs and humans, both in terms of anatomical structure and experimental techniques implemented. This article provides methodological keys for conducting experiments with equipment routinely used in clinical practice.

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Jennifer L. Quon, Lily H. Kim, Robert M. Lober, Maryam Maleki, Gary K. Steinberg and Kristen W. Yeom

OBJECTIVE

Moyamoya disease is a dynamic cerebrovascular condition that often requires vascular surveillance. Arterial spin labeling (ASL) is an MR perfusion method that is increasingly used for stroke and other various neurovascular pathologies. Unlike perfusion-weighted MRI, ASL uses endogenous water molecules for signal and therefore obviates gadolinium use; and provides direct, not relative, quantitative cerebral blood flow (CBF) measures. Presently, the potential role of ASL for evaluating postoperative pediatric moyamoya patients is relatively unexplored. This study investigated the role for ASL in evaluating cerebral hemodynamic changes in children who underwent revascularization surgery.

METHODS

This retrospective study examined 15 consecutive pediatric patients with moyamoya disease (n = 7) or moyamoya syndrome (n = 8) presenting between 2010 and 2014 who underwent revascularization and in whom 3T ASL was performed pre- and postoperatively. Postoperative MRI at least 3 months after revascularization procedure was used for analysis. Quantitative CBF in various vascular territories was interrogated: anterior, middle, and posterior cerebral arteries, and basal ganglia supplied by the lenticulostriate collaterals, resulting in evaluation of 20 brain regions.

RESULTS

After revascularization, CBF in the high middle cerebral artery territory significantly increased (p = 0.0059), accompanied by a decrease in CBF to the ipsilateral lenticulostriate-supplied basal ganglia (p = 0.0053). No perfusion changes occurred in the remaining cerebral vascular territories after surgery.

CONCLUSIONS

ASL-based quantitative CBF showed improved cerebral perfusion to the middle cerebral artery territory after revascularization in children with both moyamoya syndrome and disease. Reduced perfusion to the basal ganglia might reflect pruning of the lenticulostriate collaterals, potentially from effects of revascularization. ASL can quantitatively evaluate hemodynamic changes in children with moyamoya after revascularization, and it may be a useful adjunct to routine clinical MRI surveillance.

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Taylor A. Wilson, Rebekah G. Langston, Ka Hin Wong and Analiz Rodriguez

OBJECTIVE

The American Association of Neurological Surgeons (AANS) Neurosurgery Research and Education Foundation (NREF) provides ongoing competitive research fellowships for residents and young investigators. The authors sought to determine the characteristics and career tracks of award recipients.

METHODS

The authors analyzed characteristics and academic productivity parameters of NREF resident and young investigator awardees in the United States and Canada from 1983 to 2017. Data were extracted from the NREF database and online resources (Web of Science, NIH reporter).

RESULTS

In total, 224 research grants were awarded to 31 women (14%) and 193 men (86%) from 1983 to 2017. Neuro-oncology (36%) was the most common research category. Sixty percent of awardees were in training and most resident award winners were in postgraduate year 5 (37%). Forty-nine percent of all awardees had an additional postgraduate degree (PhD 39%, Master’s 10%) with a significantly higher number of PhD recipients being from Canada in comparison to any US region (p = 0.024). The Northeastern and Southeastern United States were the regions with the highest and lowest numbers of award recipients, respectively. More than one-third (40%) of awardees came from institutions that have a National Institute of Neurological Disorders and Stroke Research Education Grant (NINDS R25) for neurosurgical training. Awardees from NINDS R25–funded programs were significantly more likely to go on to receive funding from the National Institutes of Health (NIH) (40.4% vs 26.1%; p = 0.024). The majority of recipients (72%) who were no longer in training pursued fellowships, with a significant likelihood that fellowship subspecialty correlated with NREF research category (p < 0.001). Seventy-nine percent of winners entered academic neurosurgery practice, with 18% obtaining the position of chair. The median h-index among NREF winners was 11. NIH funding was obtained by 71 awardees (32%) with 36 (18%) being a principal investigator on an R01 grant from the NIH Research Project Grant Program.

CONCLUSIONS

The majority of AANS/NREF research award recipients enter academics as fellowship-trained neurosurgeons, with approximately one-third obtaining NIH funding. Analysis of this unique cohort allows for identification of characteristics of academic success.

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A. Scott Emmert, Shawn M. Vuong, Crystal Shula, Diana Lindquist, Weihong Yuan, Yueh-Chiang Hu, Francesco T. Mangano and June Goto

OBJECTIVE

Emergence of CRISPR/Cas9 genome editing provides a robust method for gene targeting in a variety of cell types, including fertilized rat embryos. The authors used this method to generate a transgenic rat L1cam knockout model of X-linked hydrocephalus (XLH) with human genetic etiology. The object of this study was to use diffusion tensor imaging (DTI) in studying perivascular white matter tract injury in the rat model and to characterize its pathological definition in histology.

METHODS

Two guide RNAs designed to disrupt exon 4 of the L1cam gene on the X chromosome were injected into Sprague-Dawley rat embryos. Following embryo transfer into pseudopregnant females, rats were born and their DNA was sequenced for evidence of L1cam mutation. The mutant and control wild-type rats were monitored for growth and hydrocephalus phenotypes. Their macro- and microbrain structures were studied with T2-weighted MRI, DTI, immunohistochemistry, and transmission electron microscopy (TEM).

RESULTS

The authors successfully obtained 2 independent L1cam knockout alleles and 1 missense mutant allele. Hemizygous male mutants from all 3 alleles developed hydrocephalus and delayed development. Significant reductions in fractional anisotropy and axial diffusivity were observed in the corpus callosum, external capsule, and internal capsule at 3 months of age. The mutant rats did not show reactive gliosis by then but exhibited hypomyelination and increased extracellular fluid in the corpus callosum.

CONCLUSIONS

The CRISPR/Cas9-mediated genome editing system can be harnessed to efficiently disrupt the L1cam gene in rats for creation of a larger XLH animal model than previously available. This study provides evidence that the early pathology of the periventricular white matter tracts in hydrocephalus can be detected in DTI. Furthermore, TEM-based morphometric analysis of the corpus callosum elucidates the underlying cytopathological changes accompanying hydrocephalus-derived variations in DTI. The CRISPR/Cas9 system offers opportunities to explore novel surgical and imaging techniques on larger mammalian models.

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Anders Behrens, Eva Elgh, Göran Leijon, Bo Kristensen, Anders Eklund and Jan Malm

OBJECTIVE

The Computerized General Neuropsychological INPH Test (CoGNIT) provides the clinician and the researcher with standardized and accessible cognitive assessments in patients with idiopathic normal pressure hydrocephalus (INPH). CoGNIT includes tests of memory, executive functions, attention, manual dexterity, and psychomotor speed. Investigations of the validity and reliability of CoGNIT have been published previously. The aim of this study was to evaluate CoGNIT’s sensitivity to cognitive change after shunt surgery in patients with INPH.

METHODS

Forty-one patients with INPH (median Mini-Mental State Examination score 26) were given CoGNIT preoperatively and at a postoperative follow-up 4 months after shunt surgery. Scores were compared to those of 44 healthy elderly control volunteers. CoGNIT was administered by either a nurse or an occupational therapist.

RESULTS

Improvement after shunt surgery was seen in all cognitive domains: memory (10-word list test, p < 0.01); executive functions (Stroop incongruent color and word test, p < 0.01); attention (2-choice reaction test, p < 0.01); psychomotor speed (Stroop congruent color and word test, p < 0.01); and manual dexterity (4-finger tapping, p < 0.01). No improvement was seen in the Mini-Mental State Examination score. Preoperative INPH test scores were significantly impaired compared to healthy control subjects (p < 0.001 for all tests).

CONCLUSIONS

In this study the feasibility for CoGNIT to detect a preoperative impairment and postoperative improvement in INPH was demonstrated. CoGNIT has the potential to become a valuable tool in clinical and research work.

Clinical trial registration no.: NCT01618500 (clinicaltrials.gov)

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Michael Glantz and Nicholas Brandmeir

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Takeshi Funaki, Jun C. Takahashi, Kiyohiro Houkin, Satoshi Kuroda, Miki Fujimura, Yasutake Tomata and Susumu Miyamoto

OBJECTIVE

Following hemorrhagic stroke in moyamoya disease, de novo intracranial hemorrhage can occur in the previously unaffected nonhemorrhagic hemisphere. In the present analysis the authors intended to determine whether the presence in the nonhemorrhagic hemisphere of choroidal collateral vessels, which have been the focus of attention as a source of bleeding, affects the risk of de novo hemorrhage.

METHODS

The subject of focus of the present cohort study was the nonhemorrhagic hemispheres of adult patients with hemorrhagic moyamoya disease enrolled in the Japan Adult Moyamoya Trial and allocated to the nonsurgical arm. The variable of interest was the presence of choroidal collaterals (also termed choroidal anastomoses), identified with baseline angiography and represented by a connection (anastomosis) between the anterior or posterior choroidal arteries and the medullary arteries. The outcome measure was de novo hemorrhage during the 5-year follow-up period, assessed in all nonhemorrhagic hemispheres. The incidence of de novo hemorrhage in the collateral-positive and -negative groups was compared.

RESULTS

Choroidal collaterals were present in 15 of 36 (41.7%) nonhemorrhagic hemispheres analyzed. The overall annual risk of de novo hemorrhage was 2.0%. Three de novo hemorrhages occurred in the collateral-positive group, whereas no hemorrhage occurred in the collateral-negative group. The annual risk of de novo hemorrhage was significantly higher in the collateral-positive group than in the collateral-negative group (5.8% per year vs 0% per year; p = 0.017). All hemorrhage sites corresponded to the distribution of choroidal collaterals.

CONCLUSIONS

The present preliminary results suggest that the presence of choroidal collaterals affects the risk of de novo hemorrhage in the nonhemorrhagic hemisphere, subject to verification in larger studies. Further studies are needed to determine the optimal treatment strategy for nonhemorrhagic hemispheres and asymptomatic patients.

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Aaron P. Kamer, Jose M. Bonnin, Robert J. Spinner and Aaron A. Cohen-Gadol

Intracranial extension of temporomandibular joint (TMJ) ganglion cysts is very rare. Two previously reported cases presented clinically due to effects on cranial nerves and had obvious association with the TMJ on imaging. To the authors’ knowledge, intracranial extension of a TMJ ganglion cyst presenting with seizures and mimicking a primary brain tumor has not been previously reported. The patient underwent resection of a presumptive primary cystic temporal lobe tumor, but the lesion had histopathological features of a nonneoplastic cyst with a myxoid content. He was followed with serial imaging for 5 years before regrowth of the lesion caused new episodes of seizures requiring a repeat operation, during which the transdural defect was repaired after the adjacent segment of the TMJ was curetted. A thorough review of all imaging studies and the histopathological findings from the repeat operation led to the correct diagnosis of a TMJ ganglion cyst. This case highlights an unusual presentation of this rare lesion, as well as its potential for recurrence. TMJ ganglion cysts should be included in the differential diagnosis of cystic tumors involving the anterior temporal lobe, presenting with or without seizures. Focused imaging evaluation of the TMJ can be helpful to rule out the possible role of associated TMJ lesions.

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Philip L. Perez, Sarah S. Wang, Susan Heath, Jennifer Henderson-Sabes, Danielle Mizuiri, Leighton B. Hinkley, Srikantan S. Nagarajan, Paul S. Larson and Steven W. Cheung

OBJECTIVE

The object of this study was to define caudate nucleus locations responsive to intraoperative direct electrical stimulation for tinnitus loudness modulation and relate those locations to functional connectivity maps between caudate nucleus subdivisions and auditory cortex.

METHODS

Six awake study participants who underwent bilateral deep brain stimulation (DBS) electrode placement in the caudate nucleus as part of a phase I clinical trial were analyzed for tinnitus modulation in response to acute stimulation at 20 locations. Resting-state 3-T functional MRI (fMRI) was used to compare connectivity strength between centroids of tinnitus loudness-reducing or loudness-nonreducing caudate locations and the auditory cortex in the 6 DBS phase I trial participants and 14 other neuroimaging participants with a Tinnitus Functional Index > 50.

RESULTS

Acute tinnitus loudness reduction was observed at 5 caudate locations, 4 positioned at the body and 1 at the head of the caudate nucleus in normalized Montreal Neurological Institute space. The remaining 15 electrical stimulation interrogations of the caudate head failed to reduce tinnitus loudness. Compared to the caudate head, the body subdivision had stronger functional connectivity to the auditory cortex on fMRI (p < 0.05).

CONCLUSIONS

Acute tinnitus loudness reduction was more readily achieved by electrical stimulation of the caudate nucleus body. Compared to the caudate head, the caudate body has stronger functional connectivity to the auditory cortex. These first-in-human findings provide insight into the functional anatomy of caudate nucleus subdivisions and may inform future target selection in a basal ganglia–centric neuromodulation approach to treat medically refractory tinnitus.

Clinical trial registration no.: NCT01988688 (clinicaltrials.gov)

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Hiroki Ushirozako, Go Yoshida, Sho Kobayashi, Tomohiko Hasegawa, Yu Yamato, Tatsuya Yasuda, Tomohiro Banno, Hideyuki Arima, Shin Oe, Yuki Mihara, Daisuke Togawa and Yukihiro Matsuyama

OBJECTIVE

Intraoperative neuromonitoring may be valuable for predicting postoperative neurological complications, and transcranial motor evoked potentials (TcMEPs) are the most reliable monitoring modality with high sensitivity. One of the most frequent problems of TcMEP monitoring is the high rate of false-positive alerts, also called “anesthetic fade.” The purpose of this study was to clarify the risk factors for false-positive TcMEP alerts and to find ways to reduce false-positive rates.

METHODS

The authors analyzed 703 patients who underwent TcMEP monitoring under total intravenous anesthesia during spinal surgery within a 7-year interval. They defined an alert point as final TcMEP amplitudes ≤ 30% of the baseline. Variations in body temperature (maximum − minimum body temperature during surgery) were measured. Patients with false-positive alerts were classified into 2 groups: a global group with alerts observed in 2 or more muscles of the upper and lower extremities, and a focal group with alerts observed in 1 muscle.

RESULTS

False-positive alerts occurred in 100 cases (14%), comprising 60 cases with global and 40 cases with focal alerts. Compared with the 545 true-negative cases, in the false-positive cases the patients had received a significantly higher total propofol dose (1915 mg vs 1380 mg; p < 0.001). In the false-positive cases with global alerts, the patients had also received a higher mean propofol dose than those with focal alerts (4.5 mg/kg/hr vs 4.2 mg/kg/hr; p = 0.087). The cutoff value of the total propofol dose for predicting false-positive alerts, with the best sensitivity and specificity, was 1550 mg. Multivariate logistic analysis revealed that a total propofol dose > 1550 mg (OR 4.583; 95% CI 2.785–7.539; p < 0.001), variation in body temperature (1°C difference; OR 1.691; 95% CI 1.060–2.465; p < 0.01), and estimated blood loss (500-ml difference; OR 1.309; 95% CI 1.155–1.484; p < 0.001) were independently associated with false-positive alerts.

CONCLUSIONS

Intraoperative total propofol dose > 1550 mg, larger variation in body temperature, and greater blood loss are independently associated with false-positive alerts during spinal surgery. The authors believe that these factors may contribute to the false-positive global alerts that characterize anesthetic fade. As it is necessary to consider multiple confounding factors to distinguish false-positive alerts from true-positive alerts, including variation in body temperature or ischemic condition, the authors argue the importance of a team approach that includes surgeons, anesthesiologists, and medical engineers.