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Alexandre Boutet, Ileana Hancu, Utpal Saha, Adrian Crawley, David S. Xu, Manish Ranjan, Eugen Hlasny, Robert Chen, Warren Foltz, Francesco Sammartino, Ailish Coblentz, Walter Kucharczyk and Andres M. Lozano

OBJECTIVE

Physicians are more frequently encountering patients who are treated with deep brain stimulation (DBS), yet many MRI centers do not routinely perform MRI in this population. This warrants a safety assessment to improve DBS patients’ accessibility to MRI, thereby improving their care while simultaneously providing a new tool for neuromodulation research.

METHODS

A phantom simulating a patient with a DBS neuromodulation device (DBS lead model 3387 and IPG Activa PC model 37601) was constructed and used. Temperature changes at the most ventral DBS electrode contacts, implantable pulse generator (IPG) voltages, specific absorption rate (SAR), and B1+rms were recorded during 3-T MRI scanning. Safety data were acquired with a transmit body multi-array receive and quadrature transmit-receive head coil during various pulse sequences, using numerous DBS configurations from “the worst” to “the most common.”

In addition, 3-T MRI scanning (T1 and fMRI) was performed on 41 patients with fully internalized and active DBS using a quadrature transmit-receive head coil. MR images, neurological examination findings, and stability of the IPG impedances were assessed.

RESULTS

In the phantom study, temperature rises at the DBS electrodes were less than 2°C for both coils during 3D SPGR, EPI, DTI, and SWI. Sequences with intense radiofrequency pulses such as T2-weighted sequences may cause higher heating (due to their higher SAR). The IPG did not power off and kept a constant firing rate, and its average voltage output was unchanged. The 41 DBS patients underwent 3-T MRI with no adverse event.

CONCLUSIONS

Under the experimental conditions used in this study, 3-T MRI scanning of DBS patients with selected pulse sequences appears to be safe. Generally, T2-weighted sequences (using routine protocols) should be avoided in DBS patients. Complementary 3-T MRI phantom safety data suggest that imaging conditions that are less restrictive than those used in the patients in this study, such as using transmit body multi-array receive coils, may also be safe. Given the interplay between the implanted DBS neuromodulation device and the MRI system, these findings are specific to the experimental conditions in this study.

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Corey T. Walker, S. Harrison Farber, Tyler S. Cole, David S. Xu, Jakub Godzik, Alexander C. Whiting, Cory Hartman, Randall W. Porter, Jay D. Turner and Juan Uribe

OBJECTIVE

Minimally invasive anterolateral retroperitoneal approaches for lumbar interbody arthrodesis have distinct advantages attractive to spine surgeons. Prepsoas or transpsoas trajectories can be employed with differing complication profiles because of the inherent anatomical differences encountered in each approach. The evidence comparing them remains limited because of poor quality data. Here, the authors sought to systematically review the available literature and perform a meta-analysis comparing the two techniques.

METHODS

A systematic review and meta-analysis was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. A database search was used to identify eligible studies. Prepsoas and transpsoas studies were compiled, and each study was assessed for inclusion criteria. Complication rates were recorded and compared between approach groups. Studies incorporating an analysis of postoperative subsidence and pseudarthrosis rates were also assessed and compared.

RESULTS

For the prepsoas studies, 20 studies for the complications analysis and 8 studies for the pseudarthrosis outcomes analysis were included. For the transpsoas studies, 39 studies for the complications analysis and 19 studies for the pseudarthrosis outcomes analysis were included. For the complications analysis, 1874 patients treated via the prepsoas approach and 4607 treated with the transpsoas approach were included. In the transpsoas group, there was a higher rate of transient sensory symptoms (21.7% vs 8.7%, p = 0.002), transient hip flexor weakness (19.7% vs 5.7%, p < 0.001), and permanent neurological weakness (2.8% vs 1.0%, p = 0.005). A higher rate of sympathetic nerve injury was seen in the prepsoas group (5.4% vs 0.0%, p = 0.03). Of the nonneurological complications, major vascular injury was significantly higher in the prepsoas approach (1.8% vs 0.4%, p = 0.01). There was no difference in urological or peritoneal/bowel injury, postoperative ileus, or hematomas (all p > 0.05). A higher infection rate was noted for the transpsoas group (3.1% vs 1.1%, p = 0.01). With regard to postoperative fusion outcomes, similar rates of subsidence (12.2% prepsoas vs 13.8% transpsoas, p = 0.78) and pseudarthrosis (9.9% vs 7.5%, respectively, p = 0.57) were seen between the groups at the last follow-up.

CONCLUSIONS

Complication rates vary for the prepsoas and transpsoas approaches owing to the variable retroperitoneal anatomy encountered during surgical dissection. While the risks of a lasting motor deficit and transient sensory disturbances are higher for the transpsoas approach, there is a reciprocal reduction in the risks of major vascular injury and sympathetic nerve injury. These results can facilitate informed decision-making and tailored surgical planning regarding the choice of minimally invasive anterolateral access to the spine.

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The comprehensive anatomical spinal osteotomy and anterior column realignment classification

Presented at the 2018 AANS/CNS Joint Section on Disorders of the Spine and Peripheral Nerves

Juan S. Uribe, Frank Schwab, Gregory M. Mundis Jr., David S. Xu, Jacob Januszewski, Adam S. Kanter, David O. Okonkwo, Serena S. Hu, Deviren Vedat, Robert Eastlack, Pedro Berjano and Praveen V. Mummaneni

OBJECTIVE

Spinal osteotomies and anterior column realignment (ACR) are procedures that allow preservation or restoration of spine lordosis. Variations of these techniques enable different degrees of segmental, regional, and global sagittal realignment. The authors propose a comprehensive anatomical classification system for ACR and its variants based on the level of technical complexity and invasiveness. This serves as a common language and platform to standardize clinical and radiographic outcomes for the utilization of ACR.

METHODS

The proposed classification is based on 6 anatomical grades of ACR, including anterior longitudinal ligament (ALL) release, with varying degrees of posterior column release or osteotomies. Additionally, a surgical approach (anterior, lateral, or posterior) was added. Reliability of the classification was evaluated by an analysis of 16 clinical cases, rated twice by 14 different spine surgeons, and calculation of Fleiss kappa coefficients.

RESULTS

The 6 grades of ACR are as follows: grade A, ALL release with hyperlordotic cage, intact posterior elements; grade 1 (ACR + Schwab grade 1), additional resection of the inferior facet and joint capsule; grade 2 (ACR + Schwab grade 2), additional resection of both superior and inferior facets, interspinous ligament, ligamentum flavum, lamina, and spinous process; grade 3 (ACR + Schwab grade 3), additional adjacent-level 3-column osteotomy including pedicle subtraction osteotomy; grade 4 (ACR + Schwab grade 4), 2-level distal 3-column osteotomy including pedicle subtraction osteotomy and disc space resection; and grade 5 (ACR + Schwab grade 5), complete or partial removal of a vertebral body and both adjacent discs with or without posterior element resection. Intraobserver and interobserver reliability were 97% and 98%, respectively, across the 14-reviewer cohort.

CONCLUSIONS

The proposed anatomical realignment classification provides a consistent description of the various posterior and anterior column release/osteotomies. This reliability study confirmed that the classification is consistent and reproducible across a diverse group of spine surgeons.

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Christopher S. Lozano, Manish Ranjan, Alexandre Boutet, David S. Xu, Walter Kucharczyk, Alfonso Fasano and Andres M. Lozano

OBJECTIVE

The clinical results of deep brain stimulation (DBS) of the subthalamic nucleus (STN) are highly dependent on accurate targeting and target implantation. Several targeting tactics are in current use, including image-only and/or electrophysiologically guided approaches using microelectrode recordings (MERs). The purpose of the present study was to make an appraisal of imaging only–based versus imaging with the addition of intraoperative MER-guided STN electrode targeting.

METHODS

The authors evaluated 100 consecutive patients undergoing STN DBS. The position of the STN target was estimated from preoperative MR images (direct target) or in relation to the position of the anterior and posterior commissures (indirect target). MERs were obtained for each trajectory. The authors tracked which targets were adjusted intraoperatively as a consequence of MER data. The final placement of 182 total STN electrodes was validated by intraoperative macrostimulation through the implanted DBS electrodes. The authors compared the image-based direct, indirect, MER-guided target adjustments and the final coordinates of the electrodes as seen on postoperative MRI.

RESULTS

In approximately 80% of the trajectories, there was a good correspondence between the imaging-based and the MER-guided localization of the STN target. In approximately 20% of image-based targeting trajectories, however, the electrophysiological data revealed that the trajectory was suboptimal, missing the important anatomical structures to a significant extent. The greatest mismatch was in the superior-inferior axis, but this had little impact because it could be corrected without changing trajectories. Of more concern were mismatches of 2 mm or more in the mediolateral (x) or anteroposterior (y) planes, discrepancies that necessitated a new targeting trajectory to correct for the mis-targeting. The incidence of mis-targetting requiring a second MER trajectory on the first and second sides was similar (18% and 22%).

CONCLUSIONS

According to the present analysis, approximately 80% of electrodes were appropriately targeted using imaging alone. In the other 20%, imaging alone led to suboptimal targeting that could be corrected by a trajectory course correction guided by the acquired MER data. The authors’ results suggest that preoperative imaging is insufficient to obtain optimal results in all patients undergoing STN DBS.

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David S. Xu and Francisco A. Ponce

OBJECTIVE

The aim of this article is to review the authors’ and published experience with deep brain stimulation (DBS) therapy for the treatment of patients with Alzheimer’s disease (AD) and Parkinson’s disease dementia (PDD).

METHODS

Two targets are current topics of investigation in the treatment of AD and PDD, the fornix and the nucleus basalis of Meynert. The authors reviewed the current published clinical experience with attention to patient selection, biological rationale of therapy, anatomical targeting, and clinical results and adverse events.

RESULTS

A total of 7 clinical studies treating 57 AD patients and 7 PDD patients have been reported. Serious adverse events were reported in 6 (9%) patients; none resulted in death or disability. Most studies were case reports or Phase 1/2 investigations and were not designed to assess treatment efficacy. Isolated patient experiences demonstrating improved clinical response after DBS have been reported, but no significant or consistent cognitive benefits associated with DBS treatment could be identified across larger patient populations.

CONCLUSIONS

PDD and AD are complex clinical entities, with investigation of DBS intervention still in an early phase. Recently published studies demonstrate acceptable surgical safety. For future studies to have adequate power to detect meaningful clinical changes, further refinement is needed in patient selection, metrics of clinical response, and optimal stimulation parameters.

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David S. Xu, Al-Wala Awad, Chad Mehalechko, Jeffrey R. Wilson, Lynn S. Ashby, Stephen W. Coons and Nader Sanai

OBJECTIVE

Seizures are the most common presenting symptom of newly diagnosed WHO Grade II gliomas (low-grade glioma [LGG]) and significantly impair quality of life. Although gross-total resection of LGG is associated with better seizure control, it remains unclear whether an extent of resection (EOR) “threshold” exists for long-term seizure control. Specifically, what proportion of FLAIR-positive tissue in patients with newly diagnosed LGG must be removed to achieve Engel Class I seizure freedom? To clarify the EOR threshold for long-term seizure control, the authors analyzed data from a consecutive series of patients with newly diagnosed LGG who presented with seizures and subsequently underwent microsurgical resection.

METHODS

The authors identified consecutive patients with newly diagnosed LGG who presented with seizures and were treated at the Barrow Neurological Institute between 2002 and 2012. Patients were dichotomized into those who were seizure free postoperatively and those who were not. The EOR was calculated by quantitative comparison of pre- and postoperative MRI. Univariate analysis of these 2 groups included the chi-square test and the Mann-Whitney U-test, and a multivariate logistic regression was constructed to predict the impact of multiple independent variables on the likelihood of postoperative seizure freedom. To determine a threshold of EOR that optimizes seizure freedom, a receiver operating characteristic curve was plotted and the optimal point of discrimination was determined.

RESULTS

Data from 128 patients were analyzed (male/female ratio 1.37:1; mean age 40.8 years). All 128 patients presented with seizures, usually generalized (n = 57, 44.5%) or simple partial (n = 57, 44.5%). The median EOR was 90.0%. Of 128 patients, 46 (35.9%) had 100% volumetric tumor resection, 64 (50.0%) had 90%–99% volumetric tumor resection, and 11 (8.6%) had 80%–89% volumetric tumor resection. Postoperatively, 105 (82%) patients were seizure free (Engel Class I); 23 (18%) were not (Engel Classes II–IV). The proportion of seizure-free patients increased in proportion to the EOR. Predictive variables included in the regression model were preoperative Karnofsky Performance Scale score, seizure type, time from diagnosis to surgery, preoperative number of antiepileptic drugs, and EOR. Only EOR significantly affected the likelihood of postoperative Engel Class I status (OR 11.5, 95% CI 2.4–55.6; p = 0.002). The receiver operating characteristic curve generated based on Engel Class I status showed a sensitivity of 0.65 and 1 – specificity of 0.175, corresponding to an EOR of 80%.

CONCLUSIONS

For adult patients with LGG who suffer seizures, the results suggest that seizure freedom can be attained when EOR > 80% is achieved. Improvements in both the proportion of seizure-free patients and the durability of seizure freedom were observed beyond this 80% threshold. Interestingly, this putative EOR seizure-freedom threshold closely approximates that reported for the overall survival benefit in newly diagnosed hemispheric LGGs, suggesting that a minimum level of residual tumor burden is necessary for both disease and symptomatic progression.

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David S. Xu, Konrad Bach and Juan S. Uribe

OBJECTIVE

Minimally invasive anterior and lateral approaches to the lumbar spine are increasingly used to treat and reduce grade I spondylolisthesis, but concerns still exist for their usage in the management of higher-grade lesions. The authors report their experience with this strategy for grade II spondylolisthesis in a single-surgeon case series and provide early clinical and radiographic outcomes.

METHODS

A retrospective review of a single surgeon’s cases between 2012 and 2016 identified all patients with a Meyerding grade II lumbar spondylolisthesis who underwent minimally invasive lateral lumbar interbody fusion (LLIF) or anterior lumbar interbody fusion (ALIF) targeting the slipped level. Demographic, clinical, and radiographic data were collected and analyzed. Changes in radiographic measurements, Oswestry Disability Index (ODI), and visual analog scale (VAS) scores were compared using the paired t-test and Wilcoxon signed rank test for continuous and ordinal variables, respectively.

RESULTS

The average operative time was 199.1 minutes (with 60.6 ml of estimated blood loss) for LLIFs and 282.1 minutes (with 106.3 ml of estimated blood loss), for ALIFs. Three LLIF patients had transient unilateral anterior thigh numbness during the 1st week after surgery, and 1 ALIF patient had transient dorsiflexion weakness, which was resolved at postoperative week 1. The mean follow-up time was 17.6 months (SD 12.5 months) for LLIF patients and 10 months (SD 3.1 months) for ALIF patients. Complete reduction of the spondylolisthesis was achieved in 12 LLIF patients (75.0%) and 7 ALIF patients (87.5%). Across both procedures, there was an increase in both the segmental lordosis (LLIF 5.6°, p = 0.002; ALIF 15.0°, p = 0.002) and overall lumbar lordosis (LLIF 2.9°, p = 0.151; ALIF 5.1°, p = 0.006) after surgery. Statistically significant decreases in the mean VAS and the mean ODI measurements were seen in both treatment groups. The VAS and ODI scores fell by a mean value of 3.9 (p = 0.002) and 19.8 (p = 0.001), respectively, for LLIF patients and 3.8 (p = 0.02) and 21.0 (p = 0.03), respectively, for ALIF patients at last follow-up.

CONCLUSIONS

Early clinical and radiographic results from using minimally invasive LLIF and ALIF approaches to treat grade II spondylolisthesis appear to be good, with low operative blood loss and no neurological deficits. Complete reduction of the spondylolisthesis is frequently possible with a statistically significant reduction in pain scores.

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David S. Xu, Michael R. Levitt, M. Yashar S. Kalani, Leonardo Rangel-Castilla, Celene B. Mulholland, Isaac J. Abecassis, Ryan P. Morton, John D. Nerva, Adnan H. Siddiqui, Elad I. Levy, Robert F. Spetzler, Felipe C. Albuquerque and Cameron G. McDougall

OBJECTIVE

Fusiform dolichoectatic vertebrobasilar aneurysms are rare, challenging lesions. The natural history of these lesions and medium- and long-term patient outcomes are poorly understood. The authors sought to evaluate patient prognosis after diagnosis of fusiform dolichoectatic vertebrobasilar aneurysms and to identify clinical and radiographic predictors of neurological deterioration.

METHODS

The authors reviewed multiple, prospectively maintained, single-provider databases at 3 large-volume cerebrovascular centers to obtain data on patients with unruptured, fusiform, basilar artery dolichoectatic aneurysms diagnosed between January 1, 2000, and January 1, 2015.

RESULTS

A total of 50 patients (33 men, 17 women) were identified; mean clinical follow-up was 50.1 months and mean radiographic follow-up was 32.4 months. At last follow-up, 42% (n = 21) of aneurysms had progressed and 44% (n = 22) of patients had deterioration of their modified Rankin Scale scores. When patients were dichotomized into 2 groups— those who worsened and those who did not—univariate analysis showed 5 variables to be statistically significantly different: sex (p = 0.007), radiographic brainstem compression (p = 0.03), clinical posterior fossa compression (p < 0.001), aneurysmal growth on subsequent imaging (p = 0.001), and surgical therapy (p = 0.006). A binary logistic regression was then created to evaluate these variables. The only variable found to be a statistically significant predictor of clinical worsening was clinical symptoms of posterior fossa compression at presentation (p = 0.01).

CONCLUSIONS

Fusiform dolichoectatic vertebrobasilar aneurysms carry a poor prognosis, with approximately one-half of the patients deteriorating or experiencing progression of their aneurysm within 5 years. Despite being high risk, intervention—when carefully timed (before neurological decline)—may be beneficial in select patients.

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Isaac Josh Abecassis, David S. Xu, H. Hunt Batjer and Bernard R. Bendok

Object

The authors aimed to systematically review the literature to clarify the natural history of brain arteriovenous malformations (BAVMs).

Methods

The authors searched PubMed for one or more of the following terms: natural history, brain arteriovenous malformations, cerebral arteriovenous malformations, and risk of rupture. They included studies that reported annual rates of hemorrhage and that included either 100 patients or 5 years of treatment-free follow-up.

Results

The incidence of BAVMs is 1.12–1.42 cases per 100,000 person-years; 38%–68% of new cases are first-ever hemorrhage. The overall annual rates of hemorrhage for patients with untreated BAVMs range from 2.10% to 4.12%. Consistently implicated in subsequent hemorrhage are initial hemorrhagic presentation, exclusively deep venous drainage, and deep and infrantentorial brain location. The risk for rupture seems to be increased by large nidus size and concurrent arterial aneurysms, although these factors have not been studied as thoroughly. Venous stenosis has not been implicated in increased risk for rupture.

Conclusions

For patients with BAVMs, although the overall risk for hemorrhage seems to be 2.10%–4.12% per year, calculating an accurate risk profile for decision making involves clinical attention and accounting for specific features of the malformation.

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Zhengping Zhuang, Meng Qi, Jie Li, Hiroaki Okamoto, David S. Xu, Rajiv R. Iyer, Jie Lu, Chunzhang Yang, Robert J. Weil, Alexander Vortmeyer and Russell R. Lonser

Object

Astrocytomas and oligodendrogliomas are primary CNS tumors that remain a challenge to differentiate histologically because of their morphological variability and because there is a lack of reliable differential diagnostic markers. To identify proteins that are differentially expressed between astrocytomas and oligodendrogliomas, the authors analyzed the proteomic expression patterns and identified uniquely expressed proteins in these neoplasms.

Methods

Proteomes of astrocytomas and oligodendrogliomas were analyzed using 2D gel electrophoresis and subsequent computerized gel analysis to detect differentially expressed proteins. The proteins were identified using high-performance liquid chromatography accompanied by tandem mass spectrometry. To determine the role of the differentially expressed proteins in astrocytes, undifferentiated glial cell cultures were treated with dibutyryl–cyclic adenosine monophosphate (cAMP).

Results

Two-dimensional gel electrophoresis revealed that glutamine synthetase was differentially expressed in astrocytomas and oligodendrogliomas. Western blot and immunohistochemical analyses confirmed the increased expression of glutamine synthetase in astrocytomas compared with oligodendrogliomas. Whereas glutamine synthetase expression was demonstrated across all grades of astrocytomas (Grade II–IV [15 tumors]) and oligoastrocytomas (4 tumors), it was expressed in only 1 oligodendroglioma (6% [16 tumors]). Treatment of undifferentiated glial cell cultures with dibutyryl-cAMP resulted in astrocyte differentiation that was associated with increased levels of glial fibrillary acidic protein and glutamine synthetase.

Conclusions

These data indicate that glutamine synthetase expression can be used to distinguish astrocytic from oligodendroglial tumors and may play a role in the pathogenesis of astrocytomas.