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Gilbert Cadena, Huy T. Duong, Jonathan J. Liu and Kee D. Kim

OBJECTIVE

C1–2 is a highly mobile complex that presents unique surgical challenges to achieving biomechanical rigidity and fusion. Posterior wiring methods have been largely replaced with segmental constructs using the C1 lateral mass, C1 pedicle, C2 pars, and C2 pedicle. Modifications to reduce surgical morbidity led to the development of C2 laminar screws. The C1 posterior arch has been utilized mostly as a salvage technique, but recent data indicate that this method provides significant rigidity in flexion-extension and axial rotation. The authors performed biomechanical testing of a C1 posterior arch screw (PAS)/C2 pars screw construct, collected morphometric data from a population of 150 CT scans, and performed a feasibility study of a freehand C1 PAS technique in 45 cadaveric specimens.

METHODS

Cervical spine CT scans from 150 patients were analyzed to determine the average C1 posterior tubercle thickness and size of C1 posterior arches. Eight cadavers were used to compare biomechanical stability of intact specimens, C1 lateral mass/C2 pars screw, and C1 PAS/C2 pars screw constructs. Paired comparisons were made using repeated-measures ANOVA and Holm-Sidak tests. Forty-five cadaveric specimens were used to demonstrate the feasibility and safety of the C1 PAS freehand technique.

RESULTS

Morphometric data showed the average craniocaudal thickness of the C1 posterior tubercle was 12.3 ± 1.94 mm. Eight percent (12/150) of cases showed thin posterior tubercles or midline defects. Average posterior arch thickness was 6.1 ± 1.1 mm and right and left average posterior arch length was 28.7 mm ± 2.53 mm and 28.9 ± 2.29 mm, respectively. Biomechanical testing demonstrated C1 lateral mass/C2 pars and C1 PAS/C2 pars constructs significantly reduced motion in flexion-extension and axial rotation compared with intact specimens (p < 0.05). The C1 lateral mass/C2 pars screw construct provided significant rigidity in lateral bending (p < 0.05). There was no statistically significant difference between the two constructs in flexion-extension, lateral bending, or axial rotation. Of the C1 posterior arches, 91.3% were successfully cannulated using a freehand technique with a low incidence of cortical breach (4.4%).

CONCLUSIONS

This biomechanical analysis indicates equivalent stability of the C1 PAS/C2 pars screw construct compared with a traditional C1 lateral mass/C2 pars screw construct. Both provide significant rigidity in flexion-extension and axial rotation. Feasibility testing in 45 cadaveric specimens indicates a high degree of accuracy with low incidence of cortical breach. These findings are supported by a separate radiographic morphometric analysis.

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Matthew J. Zdilla

OBJECTIVE

The presence of a caroticoclinoid foramen may increase the likelihood of adverse neurosurgical events. Despite the clinical importance of the caroticoclinoid foramen, its study has been mostly limited to adult populations. Therefore, the object of this study was to describe the prevalence, morphology, and development of the caroticoclinoid foramen among varied sexes and races in early life.

METHODS

The study analyzed caroticoclinoid foramina in dry orbitosphenoid, presphenoid, and sphenoid bones from a population of 101 fetal and infantile crania of varied sex and race.

RESULTS

A caroticoclinoid foramen, whether complete, near complete, or partial, was found in 36 of 199 sides (18.1%). Of the 98 crania with bilaterally intact sides, 21 (21.4%) had the presence of at least one caroticoclinoid foramen. Caroticoclinoid foramina were found unilaterally and bilaterally, in both female and male crania (9/41, 22.0%; 12/57, 21.1%, respectively) and, likewise, in crania of both black and white races (9/54, 16.7%; 12/44, 27.3%, respectively). Caroticoclinoid foramina were formed from cornuate bony projections from the anterior clinoid process, middle clinoid process, or both anterior and middle clinoid processes. Caroticoclinoid foramina were also found in isolated orbitosphenoid bones from individuals as young as 4 months’ fetal age.

CONCLUSIONS

The caroticoclinoid foramen occurs in approximately one of every 5 sides and in one in every 5 individuals of perinatal age and should, therefore, be considered a common finding in both fetuses and infants. It is common in both females and males as well as in both black and white races, alike. Furthermore, the caroticoclinoid foramen can be found in individuals as young as 4 months of fetal age. Failure to anticipate the presence of a caroticoclinoid foramen will place important neurovascular structures, including the internal carotid artery, at risk of injury. Neurosurgeons should, therefore, anticipate the caroticoclinoid foramen even in their youngest patients.

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Jennifer Muller, Mahdi Alizadeh, Feroze B. Mohamed, Jonathan Riley, John J. Pearce, Benjamin Trieu, Tsao-Wei Liang, Victor Romo, Ashwini Sharan and Chengyuan Wu

OBJECTIVE

Deep brain stimulation (DBS) is an effective procedure in improving motor symptoms for patients with advanced Parkinson’s disease (PD) through the use of high-frequency stimulation. Although one of the most commonly used target sites for DBS, sensorimotor regions of the globus pallidus interna (GPi) have yet to be thoroughly described with advanced neuroimaging analysis in vivo for human subjects. Furthermore, many imaging studies to date have been performed in a research setting and bring into question the feasibility of their applications in a clinical setting, such as for surgical planning. This study compares two different tractography methods applied to clinically feasible acquisition sequences in identifying sensorimotor regions of the GPi and the subthalamic nucleus (STN) in patients with advanced PD selected to undergo DBS.

METHODS

Seven patients with refractory PD selected for DBS were examined by MRI. Diffusion images were acquired with an average acquisition time of 15 minutes. Probabilistic and deterministic tractography methods were applied to each diffusion-weighted data set using FSL and MRtrix, respectively. Fiber assignment was performed using combined sensorimotor areas as initiation seeds and the STN and GPi, separately, as inclusion masks. Corticospinal tracts were excluded by setting the cerebral peduncles as exclusion masks. Variability between proposed techniques was shown using center of gravity (CoG) coordinates.

RESULTS

Deterministic and probabilistic corticopallidal and corticosubthalamic pathways were successfully reconstructed for all subjects across all target sites (bilaterally). Both techniques displayed large connections between the sensorimotor cortex with the posterolateral aspect of the ipsilateral GPi and the posterosuperolateral aspect of the ipsilateral STN. The average variability was 2.67 mm, with the probabilistic method identifying the CoG consistently more posterior and more lateral than the deterministic method.

CONCLUSIONS

Successful delineation of the sensorimotor regions in both the GPi and STN is achievable within a clinically reasonable timeframe. The techniques described in this paper may enhance presurgical planning with increased accuracy and improvement of patient outcomes in patients undergoing DBS. The variability found between tracking techniques warrants the use of the probabilistic tractography method over the deterministic method for presurgical planning. Probabilistic tractography was found to have an advantage over deterministic tractography in its sensitivity, in accurately describing previously described tracts, and in its ability to detect a larger number of fibers.

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Eric S. Sussman, Venkatesh Madhugiri, Mario Teo, Troels H. Nielsen, Sunil V. Furtado, Arjun V. Pendharkar, Allen L. Ho, Rogelio Esparza, Tej D. Azad, Michael Zhang and Gary K. Steinberg

OBJECTIVE

Revascularization surgery is a safe and effective surgical treatment for symptomatic moyamoya disease (MMD) and has been shown to reduce the frequency of future ischemic events and improve quality of life in affected patients. The authors sought to investigate the occurrence of acute perioperative occlusion of the contralateral internal carotid artery (ICA) with contralateral stroke following revascularization surgery, a rare complication that has not been previously reported.

METHODS

This study is a retrospective review of a prospective database of a single surgeon’s series of revascularization operations in patients with MMD. From 1991 to 2016, 1446 bypasses were performed in 905 patients, 89.6% of which involved direct anastomosis of the superficial temporal artery (STA) to a distal branch of the middle cerebral artery (MCA). Demographic, surgical, and radiographic data were collected prospectively in all treated patients.

RESULTS

Symptomatic contralateral hemispheric infarcts occurred during the postoperative period in 34 cases (2.4%). Digital subtraction angiography (DSA) was performed in each of these patients. In 8 cases (0.6%), DSA during the immediate postoperative period revealed associated new occlusion of the contralateral ICA. In each of these cases, revascularization surgery involved direct anastomosis of the STA to an M4 branch of the MCA. Preoperative DSA revealed moderate (n = 1) or severe (n = 3) stenosis or occlusion (n = 4) of the ipsilateral ICA and mild (n = 2), moderate (n = 4), or severe (n = 2) stenosis of the contralateral ICA. The baseline Suzuki stage was 4 (n = 7) or 5 (n = 1). The collateral supply originated exclusively from the intracranial circulation in 4/8 patients (50%), and from both the intracranial and extracranial circulation in the remaining 50% of patients. Seven (88%) of 8 patients improved symptomatically during the acute postoperative period with induced hypertension. The modified Rankin Scale (mRS) score at discharge was worse than baseline in 7/8 patients (88%), whereas 1 patient had only minor deficits that did not affect the mRS score. At the 3-year follow-up, 3/8 patients (38%) were at their baseline mRS score or better, 1 patient had significant disability compared with preoperatively, 2 patients had died, and 1 patient was lost to follow-up. Three-year follow-up is not yet available in 1 patient.

CONCLUSIONS

Acute occlusion of the ICA on the contralateral side from an STA-MCA bypass is a rare, but potentially serious, complication of revascularization surgery for MMD. It highlights the importance of the hemodynamic interrelationships that exist between the two hemispheres, a concept that has been previously underappreciated. Induced hypertension during the acute period may provide adequate cerebral blood flow via developing collateral vessels, and good outcomes may be achieved with aggressive supportive management and expedited contralateral revascularization.

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James D. Lin, Chao Wei, Jamal N. Shillingford, Eduardo C. Beauchamp, Lee A. Tan, Yongjung J. Kim, Ronald A. Lehman Jr. and Lawrence G. Lenke

OBJECTIVE

To demonstrate that a more ventral starting point for thoracic pedicle screw insertion, produced by aggressively removing the dorsal transverse process bone down to the superior articular facet (SAF), results in a larger margin for error and more medial screw angulation compared to the traditional dorsal starting point (DSP). The margin for error will be quantified by the maximal insertional arc (MIA).

METHODS

The study population included 10 consecutive operative patients with adult idiopathic scoliosis who underwent primary surgery. All measurements were performed using 3D visualization software by an attending spine surgeon. The screw starting points were 2 mm lateral to the midline of the SAF in the mediolateral direction and in the center of the pedicle in the cephalocaudal direction. The DSP was on the dorsal cortex. The ventral starting point (VSP) was at the depth of the SAF. Measurements included distance to the pedicle isthmus, MIA, and screw trajectories.

RESULTS

Ten patients and 110 vertebral levels (T1–11) were measured. The patients’ average age was 41.4 years (range 18–64 years). The pedicle isthmus was largest at T1 (4.04 ± 1.09 mm), and smallest at T5 (1.05 ± 0.93 mm). The distance to the pedicle isthmus was 7.47 mm for the VSP and 11.92 mm for the DSP (p < 0.001). The MIA was 15.3° for the VSP and 10.1° for the DSP (p < 0.001). Screw angulation was 21.7° for the VSP and 16.8° for the DSP (p < 0.001).

CONCLUSIONS

A more ventral starting point for thoracic pedicle screws results in increased MIA and more medial screw angulation. The increased MIA represents an increased tolerance for error that should improve the safety of pedicle screw placement. More medial screw angulation allows improved triangulation of pedicle screws.

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Naoki Tani, Takahide Yaegaki, Akio Nishino, Kenta Fujimoto, Hiroyuki Hashimoto, Kaoru Horiuchi, Mitsuhisa Nishiguchi and Haruhiko Kishima

OBJECTIVE

The neurocognitive course of patients who have undergone cerebral revascularization has been the subject of many studies, and the reported effects of carotid artery stenting (CAS) on cognitive function have varied from study to study. The authors hypothesized that cognitive amelioration after CAS is associated with alteration of the default mode network (DMN) connectivity, and they investigated the correlation between functional connectivity (FC) of the DMN and post-CAS changes in cognitive function in order to find a clinical marker that can be used to predict the effect of cerebral revascularization on patients’ cognitive function in this preliminary exploratory study.

METHODS

The authors examined post-CAS changes in cognitive function in relation to FC in patients treated for unilateral carotid artery stenosis. Resting-state functional MRI (rs-fMRI) was performed with a 3-T scanner before and 6 months after CAS in 8 patients. Neuropsychological tests (Wechsler Adult Intelligence Scale III and Wechsler Memory Scale–Revised) were administered to each patient before and 6 months after CAS. The DMN was mapped for each patient through independent component analysis of the rs-fMR images, and the correlation between FC of the DMN and post-CAS change in cognitive function was analyzed on a voxel level. Multivariable regression analysis was performed to identify preoperative factors associated with a post-CAS change in cognitive function.

RESULTS

Post-CAS cognitive function varied between patients and between categories of neuropsychological tests. Although there was no significant overall improvement in Working Memory scores after CAS, post-CAS Working Memory scores changed in negative correlation with changes in FC between the DMN and the precentral/superior frontal gyrus and between the DMN and the middle frontal gyrus. In addition, the preoperative FC between those areas correlated positively with the post-CAS improvement in working memory.

CONCLUSIONS

FC between the DMN and working memory–related areas is closely associated with improvement in working memory after CAS. Preoperative analysis of FC of the DMN may be useful for predicting postoperative improvement in the working memory of patients being treated for unilateral stenosis of the extracranial internal carotid artery.

Clinical trial registration no.: UMIN000020045 (www.umin.ac.jp/ctr/index.htm)

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Wataru Yanagihara, Kohei Chida, Masakazu Kobayashi, Yoshitaka Kubo, Kenji Yoshida, Kazunori Terasaki and Kuniaki Ogasawara

OBJECTIVE

Some adult patients with moyamoya disease (MMD) undergoing revascularization surgery show an improvement or decline in cognition postoperatively. Revascularization surgery for ischemic MMD augments cerebral blood flow (CBF) and improves cerebral oxygen metabolism. However, cerebral hyperperfusion, which is a short-term, major increase in ipsilateral CBF that is much greater than the metabolic needs of the brain, sometimes occurs as a complication. Cerebral hyperperfusion produces widespread, minimal injury to the ipsilateral white matter and cortical regions. The aim of the present prospective study was to determine how changes in CBF due to arterial bypass surgery affect cognitive function in adult patients with symptomatic ischemic MMD and misery perfusion.

METHODS

Thirty-two patients with cerebral misery perfusion, as determined on the basis of 15O gas positron emission tomography, underwent single superficial temporal artery–middle cerebral artery (M4 in the precentral region) anastomosis. Brain perfusion single-photon emission computed tomography (SPECT) studies were performed preoperatively, on the 1st postoperative day, and 2 months after surgery. Neuropsychological tests were also performed preoperatively and 2 months after surgery.

RESULTS

Postoperative neuropsychological assessments demonstrated cognitive improvement in 10 cases (31%), no change in 8 cases (25%), and decline in 14 cases (44%). Based on brain perfusion SPECT and symptoms, 10 patients were considered to have cerebral hyperperfusion syndrome, and all of these patients exhibited a postoperative decline in cognition. Relative precentral CBF on the 1st postoperative day was significantly greater in patients with postoperative cognitive decline (167.3% ± 15.3%) than in those with improved (105.3% ± 18.2%; p < 0.0001) or unchanged (131.4% ± 32.1%; p = 0.0029) cognition. The difference between relative precentral CBF 2 months after surgery and that before surgery was significantly greater in patients with postoperative cognitive improvement (17.2% ± 3.8%) than in those with no postoperative change (10.1% ± 2.4%; p = 0.0003) or with postoperative decline (11.5% ± 3.2%; p = 0.0009) in cognition.

CONCLUSIONS

Cerebral hyperperfusion in the acute stage after arterial bypass surgery impairs cognitive function. An increase in CBF in the chronic stage without acute-stage cerebral hyperperfusion improves cognitive function in adult patients with symptomatic ischemic MMD and misery perfusion.

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Joseph R. Linzey, James F. Burke, Jeffrey L. Nadel, Craig A. Williamson, Luis E. Savastano, D. Andrew Wilkinson and Aditya S. Pandey

OBJECTIVE

It is unknown what proportion of patients who undergo emergent neurosurgical procedures initiate comfort care (CC) measures shortly after the operation. The purpose of the present study was to analyze the proportion and predictive factors of patients who initiated CC measures within the same hospital admission after undergoing emergent neurosurgery.

METHODS

This retrospective cohort study included all adult patients who underwent emergent neurosurgical and endovascular procedures at a single center between 2009 and 2014. Primary and secondary outcomes were initiation of CC measures during the initial hospitalization and determination of predictive factors, respectively.

RESULTS

Of the 1295 operations, comfort care was initiated in 111 (8.6%) during the initial admission. On average, CC was initiated 9.3 ± 10.0 days postoperatively. One-third of the patients switched to CC within 3 days. In multivariate analysis, patients > 70 years of age were significantly more likely to undergo CC than those < 50 years (70–79 years, p = 0.004; > 80 years, p = 0.0001). Two-thirds of CC patients had been admitted with a cerebrovascular pathology (p < 0.001). Admission diagnosis of cerebrovascular pathology was a significant predictor of initiating CC (p < 0.0001). A high Hunt and Hess grade of IV or V in patients with subarachnoid hemorrhage was significantly associated with initiation of CC compared to a low grade (27.1% vs 2.9%, p < 0.001). Surgery starting between 15:01 and 06:59 hours had a 1.70 times greater odds of initiating CC compared to surgery between 07:00 and 15:00.

CONCLUSIONS

Initiation of CC after emergent neurosurgical and endovascular procedures is relatively common, particularly when an elderly patient presents with a cerebrovascular pathology after typical operating hours.

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Steve S. Cho, Jun Jeon, Love Buch, Shayoni Nag, MacLean Nasrallah, Philip S. Low, M. Sean Grady, Sunil Singhal and John Y. K. Lee

OBJECTIVE

Intraoperative molecular imaging with tumor-targeted fluorescent dyes can enhance resection rates. In contrast to visible-light fluorophores (e.g., 5-aminolevulinic-acid), near-infrared (NIR) fluorophores have increased photon tissue penetration and less contamination from tissue autofluorescence. The second-window ICG (SWIG) technique relies on passive accumulation of indocyanine green (ICG) in neoplastic tissues. OTL38, conversely, targets folate receptor overexpression in nonfunctioning pituitary adenomas. In this study, we compare the properties of these 2 modalities for NIR imaging of pituitary adenomas to better understand the potential for NIR imaging in neurosurgery.

METHODS

A total of 39 patients with pituitary adenomas were enrolled between June 2015 and January 2018 in 2, sequential, IRB-approved studies. Sixteen patients received systemic ICG infusions 24 hours prior to surgery, and another 23 patients received OTL38 infusions 2–3 hours prior to surgery. NIR fluorescence signal-to-background ratio (SBR) was recorded during and after resection. Immunohistochemistry was performed on the 23 adenomas resected from patients who received OTL38 to assess expression of folate receptor–alpha (FRα).

RESULTS

All 16 adenomas operated on after ICG administration demonstrated strong NIR fluorescence (mean SBR 4.1 ± 0.69 [SD]). There was no statistically significant difference between the 9 functioning and 7 nonfunctioning adenomas (p = 0.9). After administration of OTL38, the mean SBR was 1.7 ± 0.47 for functioning adenomas, 2.6 ± 0.91 for all nonfunctioning adenomas, and 3.2 ± 0.53 for the subset of FRα-overexpressing adenomas. Tissue identification with white light alone for all adenomas demonstrated 88% sensitivity and 90% specificity. SWIG demonstrated 100% sensitivity but only 29% specificity for both functioning and nonfunctioning adenomas. OTL38 was 75% sensitive and 100% specific for all nonfunctioning adenomas, but when assessment was limited to the 9 FRα-overexpressing adenomas, the sensitivity and specificity of OTL38 were both 100%.

CONCLUSIONS

Intraoperative imaging with NIR fluorophores demonstrates highly sensitive detection of pituitary adenomas. OTL38, a folate-receptor–targeted fluorophore, is highly specific for nonfunctioning adenomas but has no utility in functioning adenomas. SWIG, which relies on passive diffusion into neoplastic tissue, is applicable to both functioning and nonfunctioning pituitary adenomas, but it is less specific than targeted fluorophores. Thus, targeted and nontargeted NIR fluorophores play important, yet distinct, roles in intraoperative imaging. Selectively and intelligently using either agent has the potential to greatly improve resection rates and outcomes for patients with intracranial tumors.

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Byron Bailey, Cristian Vera and Fraser Henderson Jr.