Combined noninvasive language mapping by navigated transcranial magnetic stimulation and functional MRI and its comparison with direct cortical stimulation

Combined noninvasive language mapping by navigated transcranial magnetic stimulation and functional MRI and its comparison with direct cortical stimulation

 

J Neurosurg 123:212–225, 2015

Repetitive navigated transcranial magnetic stimulation (rTMS) is now increasingly used for preoperative language mapping in patients with lesions in language-related areas of the brain. Yet its correlation with intraoperative direct cortical stimulation (DCS) has to be improved. To increase rTMS’s specificity and positive predictive value, the authors aim to provide thresholds for rTMS’s positive language areas. Moreover, they propose a protocol for combining rTMS with functional MRI (fMRI) to combine the strength of both methods.

Methods The authors performed multimodal language mapping in 35 patients with left-sided perisylvian lesions by using rTMS, fMRI, and DCS. The rTMS mappings were conducted with a picture-to-trigger interval (PTI, time between stimulus presentation and stimulation onset) of either 0 or 300 msec. The error rates (ERs; that is, the number of errors per number of stimulations) were calculated for each region of the cortical parcellation system (CPS). Subsequently, the rTMS mappings were analyzed through different error rate thresholds (ERT; that is, the ER at which a CPS region was defined as language positive in terms of rTMS), and the 2-out-of-3 rule (a stimulation site was defined as language positive in terms of rTMS if at least 2 out of 3 stimulations caused an error). As a second step, the authors combined the results of fMRI and rTMS in a predefined protocol of combined noninvasive mapping. To validate this noninvasive protocol, they correlated its results to DCS during awake surgery.

Results The analysis by different rTMS ERTs obtained the highest correlation regarding sensitivity and a low rate of false positives for the ERTs of 15%, 20%, 25%, and the 2-out-of-3 rule. However, when comparing the combined fMRI and rTMS results with DCS, the authors observed an overall specificity of 83%, a positive predictive value of 51%, a sensitivity of 98%, and a negative predictive value of 95%.

Conclusions In comparison with fMRI, rTMS is a more sensitive but less specific tool for preoperative language mapping than DCS. Moreover, rTMS is most reliable when using ERTs of 15%, 20%, 25%, or the 2-out-of-3 rule and a PTI of 0 msec. Furthermore, the combination of fMRI and rTMS leads to a higher correlation to DCS than both techniques alone, and the presented protocols for combined noninvasive language mapping might play a supportive role in the language-mapping assessment prior to the gold-standard intraoperative DCS.

Clinical factors associated with venous thromboembolism risk in patients undergoing craniotomy

Awake craniotomy for gliomas in a high-field intraoperative magnetic resonance imaging suite

J Neurosurg 122:1004–1011, 2015

Patients undergoing craniotomy are at risk for developing venous thromboembolism (VTE). The safety of anticoagulation in these patients is not clear. The authors sought to identify risk factors predictive of VTE in patients undergoing craniotomy.

METHODS The authors reviewed a national surgical quality database, the American College of Surgeons National Surgical Quality Improvement Program. Craniotomy patients were identified by current procedural terminology code. Clinical factors were analyzed to identify associations with VTE.

RESULTS Four thousand eight hundred forty-four adult patients who underwent craniotomy were identified. The rate of VTE in the cohort was 3.5%, including pulmonary embolism in 1.4% and deep venous thrombosis in 2.6%. A number of factors were found to be statistically significant in multivariate binary logistic regression analysis, including craniotomy for tumor, transfer from acute care hospital, age ≥ 60 years, dependent functional status, tumor involving the CNS, sepsis, emergency surgery, surgery time ≥ 4 hours, postoperative urinary tract infection, postoperative pneumonia, on ventilator ≥ 48 hours postoperatively, and return to the operating room. Patients were assigned a score based on how many of these factors they had (minimum score 0, maximum score 12). Increasing score was predictive of increased VTE incidence, as well as risk of mortality, and time from surgery to discharge.

CONCLUSIONS Patients undergoing craniotomy are at low risk of developing VTE, but this risk is increased by preoperative medical comorbidities and postoperative complications. The presence of more of these clinical factors is associated with progressively increased VTE risk; patients possessing a VTE Risk Score of ≥ 5 had a greater than 20-fold increased risk of VTE compared with patients with a VTE score of 0.

Comparison of language cortex reorganization patterns between cerebral arteriovenous malformations and gliomas: a functional MRI study

Comparison of language cortex reorganization patterns between cerebral arteriovenous malformations and gliomas- a functional MRI study

J Neurosurg 122:996–1003, 2015

Cerebral arteriovenous malformations (AVMs) are congenital malformations that may grow in the language cortex but usually do not lead to aphasia. In contrast, language dysfunction is a common presentation for patients with a glioma that involves language areas. The authors attempted to demonstrate the difference in patterns of language cortex reorganization between cerebral AVMs and gliomas by blood oxygen level–dependent (BOLD) functional MRI (fMRI) evaluation.

Methods The authors retrospectively reviewed clinical and imaging data of 63 patients with an unruptured cerebral AVM (AVM group) and 38 patients with a glioma (glioma group) who underwent fMRI. All the patients were right handed, and all their lesions were located in the left cerebral hemisphere. Patients were further categorized into 1 of the 2 following subgroups according to their lesion location: the BA subgroup (overlying or adjacent to the inferior frontal or the middle frontal gyri [the Broca area]) and the WA subgroup (overlying or adjacent to the supramarginal, angular, or superior temporal gyri [the Wernicke area]). Lateralization indices of BOLD signal activations were calculated separately for the Broca and Wernicke areas. Statistical analysis was performed to identify the difference in patterns of language cortex reorganization between the 2 groups.

Results In the AVM group, right-sided lateralization of BOLD signal activations was observed in 23 patients (36.5%), including 6 with right-sided lateralization in the Broca area alone, 12 in the Wernicke area alone, and 5 in both areas. More specifically, in the 34 patients in the AVM-BA subgroup, right-sided lateralization of the Broca area was detected in 9 patients (26.5%), and right-sided lateralization of the Wernicke area was detected in 4 (11.8%); in the 29 patients in the AVM-WA subgroup, 2 (6.9%) had right-sided lateralization of the Broca area, and 13 (44.8%) had right-sided lateralization of the Wernicke area. In the glioma group, 6 patients (15.8%) showed right-sided lateralization of the Wernicke area, including 2 patients in the glioma-BA subgroup and 4 patients in the glioma-WA subgroup. No patient showed right-sided lateralization of the Broca area. Moreover, although the incidence of right-sided lateralization was higher in cases of low-grade gliomas (5 in 26 [19.2%]) than in high-grade gliomas (1 in 12 [8.3%]), no significant difference was detected between them (p = 0.643). Compared with the AVM group, the incidence of aphasia was significantly higher (p < 0.001), and right-sided lateralization of language areas was significantly rarer (p = 0.026) in the glioma group.

Conclusions Right-sided lateralization of BOLD signal activations was observed in patients with a cerebral AVM and in those with a glioma, suggesting that language cortex reorganization may occur with both diseases. However, the potential of reorganization in patients with gliomas seems to be insufficient compared with patients AVMs, which is suggested by clinical manifestations and the fMRI findings. Moreover, this study seems to indicate that in patients with an AVM, a nidus near the Broca area mainly leads to right-sided lateralization of the Broca area, and a nidus near the Wernicke area mainly leads to right-sided lateralization of the Wernicke area.

Endoscopic endonasal treatment of 103 craniopharyngiomas

Endoscopic endonasal treatment of 103 craniopharyngiomas

J Neurosurg 121:100–113, 2014

Despite their benign histological appearance, craniopharyngiomas can be considered a challenge for the neurosurgeon and a possible source of poor prognosis for the patient. With the widespread use of the endoscope in endonasal surgery, this route has been proposed over the past decade as an alternative technique for the removal of craniopharyngiomas.

Methods. The authors retrospectively analyzed data from a series of 103 patients who underwent the endoscopic endonasal approach at two institutions (Division of Neurosurgery of the Università degli Studi di Napoli Federico II, Naples, Italy, and Division of Neurosurgery of the Bellaria Hospital, Bologna, Italy), between January 1997 and December 2012, for the removal of infra- and/or supradiaphragmatic craniopharyngiomas. Twenty-nine patients (28.2%) had previously been surgically treated.

Results. The authors achieved overall gross-total removal in 68.9% of the cases: 78.9% in purely infradiaphragmatic lesions and 66.3% in lesions involving the supradiaphragmatic space. Among lesions previously treated surgically, the gross-total removal rate was 62.1%. The overall improvement rate in visual disturbances was 74.7%, whereas worsening occurred in 2.5%. No new postoperative defect was noted. Worsening of the anterior pituitary function was reported in 46.2% of patients overall, and there were 38 new cases (48.1% of 79) of postoperative diabetes insipidus. The most common complication was postoperative CSF leakage; the overall rate was 14.6%, and it diminished to 4% in the last 25 procedures, thanks to improvement in reconstruction techniques. The mortality rate was 1.9%, with a mean follow-up duration of 48 months (range 3–246 months).

Conclusions. The endoscopic endonasal approach has become a valid surgical technique for the management of craniopharyngiomas. It provides an excellent corridor to infra- and supradiaphragmatic midline craniopharyngiomas, including the management of lesions extending into the third ventricle chamber. Even though indications for this approach are rigorously lesion based, the data in this study confirm its effectiveness in a large patient series.

Minimally invasive treatment of intracerebral hemorrhage with magnetic resonance–guided focused ultrasound

Sonothrombolysis in ICH

J Neurosurg 118:1035–1045, 2013

Intracerebral hemorrhage (ICH) is a major cause of death and disability throughout the world. Surgical techniques are limited by their invasive nature and the associated disability caused during clot removal. Preliminary data have shown promise for the feasibility of transcranial MR-guided focused ultrasound (MRgFUS) sonothrombolysis in liquefying the clotted blood in ICH and thereby facilitating minimally invasive evacuation of the clot via a twist-drill craniostomy and aspiration tube.

Methods and Results. In an in vitro model, the following optimum transcranial sonothrombolysis parameters were determined: transducer center frequency 230 kHz, power 3950 W, pulse repetition rate 1 kHz, duty cycle 10%, and sonication duration 30 seconds. Safety studies were performed in swine (n = 20). In a swine model of ICH, MRgFUS sonothrombolysis of 4 ml ICH was performed. Magnetic resonance imaging and histological examination demonstrated complete lysis of the ICH without additional brain injury, blood-brain barrier breakdown, or thermal necrosis due to sonothrombolysis. A novel cadaveric model of ICH was developed with 40-ml clots implanted into fresh cadaveric brains (n = 10). Intracerebral hemorrhages were successfully liquefied (> 95%) with transcranial MRgFUS in a highly accurate fashion, permitting minimally invasive aspiration of the lysate under MRI guidance.

Conclusions. The feasibility of transcranial MRgFUS sonothrombolysis was demonstrated in in vitro and cadaveric models of ICH. Initial in vivo safety data in a swine model of ICH suggest the process to be safe. Minimally invasive treatment of ICH with MRgFUS warrants evaluation in the setting of a clinical trial.

Awake mapping for resection of cavernous angioma and surrounding gliosis in the left dominant hemisphere

Awake mapping for resection of cavernous angioma and surrounding gliosis in the left dominant hemisphere

J Neurosurg 117:1076–1081, 2012

Maximal resection of symptomatic cavernous angioma (CA), including its surrounding gliosis if possible, has been recommended to minimize the risk of seizures or (re)bleeding. However, despite recent neurosurgical advances, such extensive CA removal is still a challenge in eloquent areas. The authors report a consecutive series of patients who underwent awake surgery for CA within the left dominant hemisphere in which intraoperative cortical– subcortical electrical stimulation was used.

Methods. Nine patients harboring a CA that was revealed by seizures in 6 cases and bleeding in 3 cases underwent resection. All CAs were located in the left dominant hemisphere: 3 temporal, 2 insular, 2 parietal, and 2 in the parietotemporal region. Awake mapping was performed in all cases by using intraoperative cortical–subcortical electrical stimulation and ultrasonography (except in 1 insular CA in which a neuronavigation system was used).

Results. Total removal of the CA was achieved in all patients, with identification and preservation of language and sensory-motor structures. In addition, the pericavernomatous gliosis was removed in 7 cases, according to the functional boundaries provided by intraoperative subcortical stimulation. In 2 cases, subcortical mapping revealed eloquent areas within the surrounding gliosis, which was voluntarily avoided. There was no postsurgical permanent deficit, no rebleeding, and no epilepsy in 7 cases (2 patients had rare seizures in the 1st year or two after surgery, and then complete arrest), with a mean follow-up of 28.5 months (range 3–64 months).

Conclusions. These results suggest that intraoperative cortical–subcortical stimulation in awake patients represents a valuable adjunct to image-guided surgery with the aim of selecting the safer surgical approach for CAs involving eloquent areas. Moreover, such online mapping can be helpful when removing the pericavernomatous gliosis while preserving functional structures, which can persist within the hemosiderin rim. Thus, the authors propose that awake surgery be routinely considered, both to optimize the resection and to improve the quality of life through seizure control and avoidance of (re)bleeding for CAs located in the left dominant hemisphere.

Interhemispheric approach for tuberculum sellae meningiomas

J Neurosurg 117:1013–1021, 2012

The objective of this study was to evaluate the ophthalmological outcome, nonvisual morbidity, and surgical complications after tuberculum sellae meningioma (TSM) removal using a superior interhemispheric approach.

Methods. In the last decade, 20 consecutive patients with TSM underwent operations using the superior interhemispheric approach. Visual acuity, visual field, and ocular fundus examination were assessed both preoperatively and 6-months postoperatively. Nonvisual morbidity was determined at an early postoperative period and at 6 months based on assessment of the Karnofsky Performance Scale score, leakage of CSF, endocrinological status, and olfactory function, which was assessed using a visual analog scale (VAS). The potential brain injury related to the approach was assessed by MRI at 6 months. Magnetic resonance imaging was then performed yearly to detect a recurrence.
The mean follow up was 56.3 ± 34 months.

Results. The primary presenting symptom for diagnosis of TSM in 20 patients (female:male ratio of 6.6:1, mean age 59.1 ± 11.1 years) was visual disturbance in 12 patients (60%), headache in 4 (20%), cognitive alteration in 1 (5%), epilepsy in 2 (10%), and accidental in 1 (5%). In a total of 40 eyes, 17 eyes in 11 patients presented with preoperative deterioration of visual acuity. Postoperatively, the visual acuity improved in 13 eyes in 8 patients (72.8%), remained unchanged in 3 eyes in 2 patients (18.2%) and deteriorated in 1 patient (9%). The nonvisual morbidity included olfactory deterioration in 7 patients (35%), and panhypopituitarism in 1 patient (5%). No patients experienced a CSF leak. The impact of olfactory deterioration on the quality of life, as estimated by a VAS score (range 0–10), was a mean of 5.7 ± 2.2 (95% CI 4.1–7.3). On the follow-up MRI, no additional lesions or recurrences were observed on the medial aspect of the frontal lobe along the surgical corridor.

Conclusions. The superior interhemispheric approach appears to be effective in resolving the problem of visual deterioration due to a TSM, without inducing surgical injury on the brain surface along the surgical corridor. Olfactory deterioration remained the challenging predominant nonvisual morbidity using this approach.

Frameless robotically targeted stereotactic brain biopsy

J Neurosurg 116:1002–1006, 2012. (http://thejns.org/doi/abs/10.3171/2012.1.JNS111746)

Frameless stereotactic brain biopsy has become an established procedure in many neurosurgical centers worldwide. Robotic modifications of image-guided frameless stereotaxy hold promise for making these procedures safer, more effective, and more efficient. The authors hypothesized that robotic brain biopsy is a safe, accurate procedure, with a high diagnostic yield and a safety profile comparable to other stereotactic biopsy methods.

Methods. This retrospective study included 41 patients undergoing frameless stereotactic brain biopsy of lesions (mean size 2.9 cm) for diagnostic purposes. All patients underwent image-guided, robotic biopsy in which the Surgi-Scope system was used in conjunction with scalp fiducial markers and a preoperatively selected target and trajectory. Forty-five procedures, with 50 supratentorial targets selected, were performed.

Results. The mean operative time was 44.6 minutes for the robotic biopsy procedures. This decreased over the second half of the study by 37%, from 54.7 to 34.5 minutes (p < 0.025). The diagnostic yield was 97.8% per procedure, with a second procedure being diagnostic in the single nondiagnostic case. Complications included one transient worsening of a preexisting deficit (2%) and another deficit that was permanent (2%). There were no infections.

Conclusions. Robotic biopsy involving a preselected target and trajectory is safe, accurate, efficient, and comparable to other procedures employing either frame-based stereotaxy or frameless, nonrobotic stereotaxy. It permits biopsy in all patients, including those with small target lesions. Robotic biopsy planning facilitates careful preoperative study and optimization of needle trajectory to avoid sulcal vessels, bridging veins, and ventricular penetration.

Optimal trajectory of endoscopic third ventriculostomy

J Neurosurg 116:1153–1157, 2012. http://thejns.org/doi/abs/10.3171/2012.2.JNS111287

An optimal entry point for endoscopic third ventriculostomy (ETV) helps protect critical structures from undue manipulation. A commonly accepted ideal entry point is 3 cm from the midline and 1 cm anterior to the coronal suture. The authors of this study reexamine this ideal entry point.

Methods. Trajectory views from MR images or CT scans used for cranial image guidance in 53 patients (age range 3–85 years) who had undergone ETV were retrospectively evaluated. The trajectory from the tuber cinereum back through the center of the foramen of Monro was projected to the surface of the head. The relation of the entry point to the midline and the coronal suture was established.

Results. The mean perpendicular distance from the ideal entry point to the midline was 30.1 ± 7 mm (median 31.9 mm, range 12.5–42.2 mm). The mean perpendicular distance to the coronal suture was 8.9 ± 14.1 mm posterior (median 10.4 mm), ranging from 30.6 mm anterior to 35.8 mm posterior. The entry point tended to be located more posteriorly in women and adults: 5.8 ± 15.4 mm posterior in males versus 13.1 ± 13.2 mm posterior in females (p = 0.08) and 9.1 ± 14.8 mm posterior in adults versus 8.2 ± 11.7 mm posterior in children (p = 0.84).

Conclusions. While the entry point may need to be modified from the ideal trajectory for other anatomical reasons, such as a trajectory through the motor cortex, in general, the authors found that the optimal entry point for ETV was more posterior than previously published and highly variable. Using image guidance or a customized trajectory based on analysis of a patient’s own imaging is highly preferable to using an empirical ideal trajectory.

Supracerebellar transtentorial approach—resection of the tentorium instead of an opening—to provide broad exposure of the mediobasal temporal lobe: anatomical aspects and surgical applications

J Neurosurg 116:764–772, 2012.  http://thejns.org/doi/abs/10.3171/2011.12.JNS111256

The aim of this study was to describe the surgical anatomy of the mediobasal aspect of the temporal lobe and the supracerebellar transtentorial (SCTT) approach performed not with an opening, but with the resection of the tentorium, as an alternative route for the neurosurgical management of vascular and tumoral lesions arising from this region.

Methods. Cadaveric specimens were used to illustrate the surgical anatomy of the mediobasal region of the temporal lobe. Demographic aspects, characteristics of lesions, clinical presentation, surgical results, follow-up findings, and outcomes were retrospectively reviewed for patients referred to receive the SCTT approach with tentorial resection.

Results. Ten patients (83%) were female and 2 (17%) were male. Their ages ranged from 6 to 59 years (mean 34.5 ± 15.8 years). All lesions (3 posterior cerebral artery aneurysms, 3 arteriovenous malformations, 3 cavernous malformations, and 3 tumors) were completely excluded or resected. After a mean follow-up period of 143 months (range 10–240 months), the mean postoperative Glasgow Outcome Scale score was 4.9.

Conclusions. Knowledge of the surgical anatomy provides improvement for microsurgical approaches. The evolution from a small opening to a resection of the tentorium absolutely changed the exposure of the mediobasal aspect of the temporal lobe. The SCTT approach with tentorial resection is an excellent alternative route to the posterior part of mediobasal aspect of the temporal lobe, and it was enough to achieve the best neurosurgical management of tumoral and vascular lesions located in this area.

Preoperative identification of the facial nerve in patients with large cerebellopontine angle tumors using high-density diffusion tensor imaging


 

J Neurosurg 116:697–702, 2012. http://thejns.org/doi/abs/10.3171/2011.12.JNS111404

Facial nerve paresis can be a devastating complication following resection of large (> 2.5 cm) cerebellopontine angle (CPA) tumors. The authors have developed and used a new high-density diffusion tensor imaging (HD-DT imaging) method, aimed at preoperatively identifying the location and course of the facial nerve in relation to large CPA tumors. Their study objective was to preoperatively identify the facial nerve in patients with large CPA tumors and compare their HD-DT imaging method with a traditional standard DT imaging method and correlate with intraoperative findings.

Methods. The authors prospectively studied 5 patients with large (> 2.5 cm) CPA tumors. All patients underwent preoperative traditional standard- and HD-DT imaging. Imaging results were correlated with intraoperative findings.

Results. Utilizing their HD-DT imaging method, the authors positively identified the location and course of the facial nerve in all patients. In contrast, using a standard DT imaging method, the authors were unable to identify the facial nerve in 4 of the 5 patients.

Conclusions. The HD-DT imaging method that the authors describe and use has proven to be a powerful, accurate, and rapid method for preoperatively identifying the facial nerve in relation to large CPA tumors. Routine integration of HD-DT imaging in preoperative planning for CPA tumor resection could lead to improved facial nerve preservation.

The paramedian supracerebellar-transtentorial approach to the entire length of the mediobasal temporal region

J Neurosurg 116:773–791, 2012. http://thejns.org/doi/abs/10.3171/2011.12.JNS11791

The exploration of lesions in the mediobasal temporal region (MTR) has challenged generations of neurosurgeons to achieve an appropriate approach. To address this challenge, the extensive use of the paramedian supracerebellar-transtentorial (PST) approach to expose the entire length of the MTR, as well as the fusiform gyrus, was investigated.

Methods. The authors studied the microsurgical aspects of the PST approach in 20 cadaver brains and 5 cadaver heads under the operating microscope. They evaluated the features, advantages, difficulties, and limitations of the PST approach and refined the surgical technique. They then used the PST approach in 15 patients with large intrinsic MTR tumors (6 patients), tumor in the posterior fusiform gyrus with mediobasal temporal epilepsy (MTE) (1 patient), cavernous malformations in the posterior MTR including the fusiform gyrus (2 patients), or intractable MTE with hippocampal sclerosis (6 patients) from December 2007 to May 2010. Patients ranged in age from 11 to 63 years (mean 35.2 years), and in 9 patients (60%) the lesion was located on the left side.

Results. In all patients with neuroepithelial tumors or cavernous malformations, the lesions were completely and safely resected. In all patients with intractable MTE with hippocampal sclerosis, the anterior two-thirds of the parahippocampal gyrus and hippocampus, as well as the amygdala, were removed selectively through the PST approach. There was no surgical morbidity or mortality in this series. Three patients (20%) with high-grade neuroepithelial tumors underwent postoperative radiotherapy and chemotherapy but needed a second surgery for recurrence during the follow-up period. In all patients with MTE, antiepileptic medication could be decreased to a single drug at lower doses, and no seizure activity has occurred until this point.

Conclusions. The PST approach provides the surgeon precise anatomical orientation when exposing the entire length of the MTR, as well as the fusiform gyrus, for removing any lesion. This is a novel technique especially for removing tumors involving the entire MTR in a single session without damaging neighboring neural or vascular structures. This approach can also be a viable alternative for selective removal of the parahippocampal gyrus, hippocampus, and amygdala in patients with MTE due to hippocampal sclerosis.