Diffusion tensor imaging and ventricle volume quantification in patients with chronic shunt-treated hydrocephalus

J Neurosurg 129:1611–1622, 2018

The object of this study was to use diffusion tensor imaging (DTI) and tract-based spatial statistics (TBSS) to characterize the long-term effects of hydrocephalus and shunting on white matter integrity and to investigate the relationship of ventricular size and alterations in white matter integrity with headache and quality-of-life outcome measures.

METHODS Patients with shunt-treated hydrocephalus and age- and sex-matched healthy controls were recruited into the study and underwent anatomical and DTI imaging on a 3-T MRI scanner. All patients were clinically stable, had undergone CSF shunt placement before 2 years of age, and had a documented history of complaints of headaches. Outcome was scored based on the Headache Disability Inventory and the Hydrocephalus Outcome Questionnaire. Fractional anisotropy (FA) and other DTI-based measures (axial, radial, and mean diffusivity; AD, RD, and MD, respectively) were extracted in the corpus callosum and internal capsule with manual region-of-interest delineation and in other regions with TBSS. Paired t-tests, corrected with a 5% false discovery rate, were used to identify regions with significant differences between patients and controls. Within the patient group, linear regression models were used to investigate the relationship between FA or ventricular volume and outcome, as well as the effect of shunt-related covariates.

RESULTS Twenty-one hydrocephalus patients and 21 matched controls completed the study, and their data were used in the final analysis. The authors found significantly lower FA for patients than for controls in 20 of the 48 regions, mostly posterior white matter structures, in periventricular as well as more distal tracts. Of these 20 regions, 17 demonstrated increased RD, while only 5 showed increased MD and 3 showed decreased AD. No areas of increased FA were observed. Higher FA in specific periventricular white matter tracts, tending toward FA in controls, was associated with increased ventricular size, as well as improved clinical outcome.

CONCLUSIONS The study shows that TBSS-based DTI is a sensitive technique for elucidating changes in white matter structures due to hydrocephalus and chronic CSF shunting and provides preliminary evidence that DTI may be a valuable tool for tailoring shunt procedures to monitor ventricular size following shunting and achieve optimal outcome, as well as for guiding the development of alternate therapies for hydrocephalus.

 

Value of whole-body low-dose computed tomography in patients with ventriculoperitoneal shunts: a retrospective study

J Neurosurg 129:1598–1603, 2018

The gold standard for evaluation of ventriculoperitoneal (VP) shunt position, dislocation, or disconnection is conventional radiography. Yet, assessment with this modality can be challenging because of low image quality and can result in repetitive radiation exposure with high fluctuation in the radiation dose. Recently, CT-based radiation doses have been significantly reduced by using low-dose protocols. Thus, whole-body low-dose CT (LDCT) has become applicable for routine use in VP shunt evaluation. The authors here compared image quality and approximate radiation dose between radiography and LDCT in patients with implanted VP shunt systems.

METHODS Ventriculoperitoneal shunt systems have been investigated with LDCT scanning at the authors’ department since 2015. A consecutive series of 57 patients (70 investigations) treated between 2015 and 2016 was retrospectively assessed. A historical patient cohort that had been evaluated with radiography was compared with the LDCT patients in terms of radiation dose and image quality. Three independent observers evaluated projection of the valve pressure level and correct intraperitoneal position, as well as complete shunt projection, using a Likert-type scale of 1–5, where 1 indicated “not assessable” and 5 meant “assessable with high accuracy.” Descriptive statistics and the Mann-Whitney U-test were used for analysis.

RESULTS Twenty-seven radiographs (38.6%) and 43 LDCT scans (61.4%) were analyzed. The median dose-length product (DLP) of the LDCT scans was 100 mGy·cm (range 59.9–183 mGy·cm). The median total dose-area product (DAP) of the radiographic images was 3177 mGy·cm2 (range 641–13,833 mGy·cm2). The estimated effective dose (EED) was significantly lower with the LDCT scan (p < 0.001). The median EED was 4.93 and 1.90 mSv for radiographs and LDCT, respectively. Significantly better identification of the abdominal position of the distal shunt catheter was achieved with LDCT (p < 0.001). Simultaneously, significantly improved visualization of the entire shunt system was realized with this technique (p < 0.001). On the contrary, identification of the valve settings was significantly worse with LDCT (p < 0.001).

CONCLUSIONS Whole-body LDCT scanning allows good visualization of the distal catheter after VP shunt placement. Despite the fact that only a rough estimation of effective doses is possible in a direct comparison of LDCT and radiography, the data showed that shunt assessment via LDCT does not lead to greater radiation exposure. Thus, especially in difficult anatomical conditions, as in patients who have undergone multiple intraabdominal surgeries, have a high BMI, or are immobile, the use of LDCT shunt evaluation has high clinical value. Further data are needed to determine the value of LDCT for the evaluation of complications or radiation dose in pediatric patients.

 

Evaluation of a novel noninvasive ICP monitoring device in patients undergoing invasive ICP monitoring: preliminary results

J Neurosurg 128:1653–1660, 2018

There is no established method of noninvasive intracranial pressure (NI-ICP) monitoring that can serve as an alternative to the gold standards of invasive monitoring with external ventricular drainage or intraparenchymal monitoring. In this study a new method of NI-ICP monitoring performed using algorithms to determine ICP based on acoustic properties of the brain was applied in patients undergoing invasive ICP (I-ICP) monitoring, and the results were analyzed.

METHODS In patients with traumatic brain injury and subarachnoid hemorrhage who were undergoing treatment in a neurocritical intensive care unit, the authors recorded ICP using the gold standard method of invasive external ventricular drainage or intraparenchymal monitoring. In addition, the authors simultaneously measured the ICP noninvasively with a device (the HS-1000) that uses advanced signal analysis algorithms for acoustic signals propagating through the cranium. To assess the accuracy of the NI-ICP method, data obtained using both I-ICP and NI-ICP monitoring methods were analyzed with MATLAB to determine the statistical significance of the differences between the ICP measurements obtained using NI-ICP and I-ICP monitoring.

RESULTS Data were collected in 14 patients, yielding 2543 data points of continuous parallel ICP values in recordings obtained from I-ICP and NI-ICP. Each of the 2 methods yielded the same number of data points. For measurements at the ≥ 17–mm Hg cutoff, which was arbitrarily chosen for this preliminary analysis, the sensitivity and specificity for the NI-ICP monitoring were found to be 0.7541 and 0.8887, respectively. Linear regression analysis indicated that there was a strong positive relationship between the measurements. Differential pressure between NI-ICP and I-ICP was within ± 3 mm Hg in 63% of data-paired readings and within ± 5 mm Hg in 85% of data-paired readings. The receiver operating characteristic–area under the curve analysis revealed that the area under the curve was 0.895, corresponding to the overall performance of NI-ICP monitoring in comparison with I-ICP monitoring.

CONCLUSIONS This study provides the first clinical data on the accuracy of the HS-1000 NI-ICP monitor, which uses advanced signal analysis algorithms to evaluate properties of acoustic signals traveling through the brain in patients undergoing I-ICP monitoring. The findings of this study highlight the capability of this NI-ICP device to accurately measure ICP noninvasively. Further studies should focus on clinical validation for elevated ICP values.

Risk assessment of motor function using nTMS-based tractography

J Neurosurg 128:800–810, 2018

Navigated transcranial magnetic stimulation (nTMS) and diffusion tensor imaging fiber tracking (DTI FT) based on nTMS data are increasingly used for preoperative planning and resection guidance in patients suffering from motor-eloquent brain tumors. The present study explores whether nTMS-based DTI FT can also be used for individual preoperative risk assessment regarding surgery-related motor impairment.

METHODS Data derived from preoperative nTMS motor mapping and subsequent nTMS-based tractography in 86 patients were analyzed. All patients suffered from high-grade glioma (HGG), low-grade glioma (LGG), or intracranial metastasis (MET). In this context, nTMS-based DTI FT of the corticospinal tract (CST) was performed at a range of fractional anisotropy (FA) levels based on an individualized FA threshold ([FAT]; tracking with 50%, 75%, and 100% FAT), which was defined as the highest FA value allowing for visualization of fibers (100% FAT). Minimum lesion-to-CST distances were measured, and fiber numbers of the reconstructed CST were assessed. These data were then correlated with the preoperative, postoperative, and follow-up status of motor function and the resting motor threshold (rMT).

RESULTS At certain FA levels, a statistically significant difference in lesion-to-CST distances was observed between patients with HGG who had no impairment and those who developed surgery-related transient or permanent motor deficits (75% FAT: p = 0.0149; 100% FAT: p = 0.0233). In this context, no patient with a lesion-to-CST distance ≥ 12 mm suffered from any new surgery-related permanent paresis (50% FAT and 75% FAT). Furthermore, comparatively strong negative correlations were observed between the rMT and lesion-to-CST distances of patients with surgery-related transient paresis (Spearman correlation coefficient [rs]; 50% FAT: rs = –0.8660; 75% FAT: rs = –0.8660) or surgery-related permanent paresis (50% FAT: rs = –0.7656; 75% FAT: rs = –0.6763).

CONCLUSIONS This is one of the first studies to show a direct correlation between imaging, clinical status, and neurophysiological markers for the integrity of the motor system in patients with brain tumors. The findings suggest that nTMSbased DTI FT might be suitable for individual risk assessment in patients with HGG, in addition to being a surgery-planning tool. Importantly, necessary data for risk assessment were obtained without significant additional efforts, making this approach potentially valuable for direct clinical use.

Symmetry of the arcuate fasciculus and its impact on language performance of patients with brain tumors in the language-dominant hemisphere

J Neurosurg 127:1407–1416, 2017

Cerebral damage in frontal, parietal, and temporal brain areas and, probably more importantly, their interconnections can lead to deficits in language. However, neural plasticity and repair allow the brain to partly compensate for neural injury, mediated by both functional and structural changes. In this study, the authors sought to systematically investigate the relationship between language performance in brain tumor patients and structural perisylvian pathways (i.e., the arcuate fasciculus [AF]) using probabilistic fiber tracking on diffusion tensor imaging. The authors used a previously proposed model in which the AF is divided into anterior, long, and posterior segments. The authors hypothesized that right-handed patients with gliomas in the language-dominant (left) hemisphere would benefit from a more symmetrical or right-lateralized language pathway in terms of better preservation of language abilities. Furthermore, they investigated to what extent specific tumor characteristics, including proximity to the AF, affect language outcome in such patients.

METHODS Twenty-seven right-handed patients (12 males and 15 females; mean age 52 ± 16 years) with 11 low-grade and 16 high-grade gliomas of the left hemisphere underwent 3-T diffusion-weighted MRI (30 directions) and language assessment as part of presurgical planning. For a systematic quantitative evaluation of the AF, probabilistic fiber tracking with a 2 regions of interest approach was carried out. Volumes of the 3 segments of both hemispheric AFs were evaluated by quantifying normalized and thresholded pathways. Resulting values served to generate the laterality index of the AFs.

RESULTS Patients without language deficits tended to have an AF that was symmetric or lateralized to the right, whereas patients with deficits in language significantly more often demonstrated a left-lateralized posterior segment of the AF. Patients with high-grade gliomas had more severe language deficits than those with low-grade gliomas. Backward logistic regression revealed the laterality index of the posterior AF segment and tumor grade as the only independent statistically significant predictors for language deficits in this cohort.

CONCLUSIONS In addition to the well-known fact that tumor entity influences behavioral outcome, the authors’ findings suggest that the right homologs of structural language-associated pathways could be supportive for language function and facilitate compensation mechanisms after brain damage in functionally eloquent areas. This further indicates that knowledge about preoperative functional redistribution (identified by neurofunctional imaging) increases the chance for total or near-total resections of tumors in eloquent areas. In the future, longitudinal studies with larger groups are mandatory to overcome the methodological limitations of this cross-sectional study and to map neuroplastic changes associated with language performance and rehabilitation in brain tumor patients.

 

Navigated transcranial magnetic stimulation for glioma removal- prognostic value in motor function recovery from postsurgical neurological deficits

J Neurosurg 127:877–891, 2017

The aim of the present study was to evaluate the usefulness of navigated transcranial magnetic stimulation (nTMS) as a prognostic predictor for upper-extremity motor functional recovery from postsurgical neurological deficits.

METHODS Preoperative and postoperative nTMS studies were prospectively applied in 14 patients (mean age 39 ± 12 years) who had intraparenchymal brain neoplasms located within or adjacent to the motor eloquent area in the cerebral hemisphere. Mapping by nTMS was done 3 times, i.e., before surgery, and 1 week and 3 weeks after surgery. To assess the response induced by nTMS, motor evoked potential (nTMS-MEP) was recorded using a surface electromyography electrode attached to the abductor pollicis brevis (APB). The cortical locations that elicited the largest electromyography response by nTMS were defined as hotspots. Hotspots for APB were confirmed as positive responsive sites by direct electrical stimulation (DES) during awake craniotomy. The distances between hotspots and lesions (DHS-L) were measured. Postoperative neurological deficits were assessed by manual muscle test and dynamometer. To validate the prognostic value of nTMS in recovery from upper-extremity paresis, the following were investigated: 1) the correlation between DHS-L and the serial grip strength change, and 2) the correlation between positive nTMS-MEP at 1 week after surgery and the serial grip strength change.

RESULTS From the presurgical nTMS study, MEPs from targeted muscles were identified in 13 cases from affected hemispheres. In one case, MEP was not evoked due to a huge tumor. Among 9 cases from which intraoperative DES mapping for hand motor area was available, hotspots for APB identified by nTMS were concordant with DES-positive sites. Compared with the adjacent group (DHS-L < 10 mm, n = 6), the nonadjacent group (DHS-L ≥ 10 mm, n = 7) showed significantly better recovery of grip strength at 3 months after surgery (p < 0.01). There were correlations between DHS-L and recovery of grip strength at 1 week, 3 weeks, and 3 months after surgery (r = 0.74, 0.68, and 0.65, respectively). Postsurgical nTMS was accomplished in 13 patients. In 9 of 13 cases, nTMS-MEP from APB muscle was positive at 1 week after surgery. Excluding the case in which nTMS-MEP was negative from the presurgical nTMS study, recoveries in grip strength were compared between 2 groups, in which nTMS-MEP at 1 week after surgery was positive (n = 9) or negative (n = 3). Significant differences were observed between the 2 groups at 1 week, 3 weeks, and 3 months after surgery (p < 0.01). Positive nTMS-MEP at 1 week after surgery correlated well with the motor recovery at 1 week, 3 weeks, and 3 months after surgery (r = 0.87, 0.88, and 0.77, respectively).

CONCLUSIONS Navigated TMS is a useful tool for identifying motor eloquent areas. The results of the present study have demonstrated the predictive value of nTMS in upper-extremity motor function recovery from postsurgical neurological deficits. The longer DHS-L and positive nTMS-MEP at 1 week after surgery have prognostic values of better recovery from postsurgical neurological deficits.

 

Ventriculostomy-associated hemorrhage: a risk assessment by radiographic simulation

J Neurosurg 127:532–536, 2017

Ventriculostomy entry sites are commonly selected by freehand estimation of Kocher’s point or approximations from skull landmarks and a trajectory toward the ipsilateral frontal horn of the lateral ventricles. A recognized ventriculostomy complication is intracranial hemorrhage from cortical vessel damage; reported rates range from 1% to 41%. In this report, the authors assess hemorrhagic risk by simulating traditional ventriculostomy trajectories and using CT angiography (CTA) with venography (CTV) data to identify potential complications, specifically from cortical draining veins.

METHODS Radiographic analysis was completed on 50 consecutive dynamic CTA/CTV studies obtained at a tertiarycare academic neurosurgery department. Image sections were 0.5 mm thick, and analysis was performed on a venous phase that demonstrated high-quality opacification of the cortical veins and sagittal sinus. Virtual ventriculostomy trajectories were determined for right and left sides using medical diagnostic imaging software. Entry points were measured along the skull surface, 10 cm posteriorly from the nasion, and 3 cm laterally for both left and right sides. Cannulation was simulated perpendicular to the skull surface. Distances between the software-traced cortical vessels and the virtual catheter were measured. To approximate vessel injury by twist drill and ventricular catheter placement, veins within a 3-mm radius were considered a hemorrhage risk.

RESULTS In 100 virtual lines through Kocher’s point toward the ipsilateral ventricle, 19% were predicted to cause cortical vein injury and suspected hemorrhage (radius ≤ 3 mm). Little difference existed between cerebral hemispheres (right 18%, left 20%). The average (± SD) distance from the trajectory line and a cortical vein was 7.23 ± 4.52 mm. In all 19 images that predicted vessel injury, a site of entry for an avascular zone near Kocher’s point could be achieved by moving the trajectory less than 1.0 cm laterally and less than 1.0 cm along the anterior/posterior axis, suggesting that empirical measures are suboptimal, and that patient-specific coordinates based on preprocedural CTA/CVA imaging may optimize ventriculostomy in the future.

CONCLUSIONS In this institutional radiographic imaging analysis, traditional methods of ventriculostomy site selection predicted significant rates of cortical vein injury, matching described rates in the literature. CTA/CTV imaging potentiates identification of patient-specific cannulation sites and custom trajectories that avoid cortical vessels, which may lessen the risk of intracranial hemorrhage during ventriculostomy placement. Further development of this software is underway to facilitate stereotactic ventriculostomy and improve outcomes.

Endoscopic endonasal transclival resection of a ventral pontine cavernous malformation

J Neurosurg 127:553–558, 2017

Brainstem cavernous malformations are challenging due to the critical anatomy and potential surgical risks. Anterolateral, lateral, and dorsal surgical approaches provide limited ventral exposure of the brainstem.

The authors present a case of a midline ventral pontine cavernous malformation resected through an endoscopic endonasal transclival approach based on minimal brainstem transection, negligible cranial nerve manipulation, and a straightforward trajectory.

Technical and reconstruction technique advances in endoscopic endonasal skull base surgery provide a direct, safe, and effective corridor to the brainstem.