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Kyousuke Kamada, Tomoki Todo, Takahiro Ota, Kenji Ino, Yoshitaka Masutani, Shigeki Aoki, Fumiya Takeuchi, Kensuke Kawai and Nobuhito Saito

Object

To validate the corticospinal tract (CST) illustrated by diffusion tensor imaging, the authors used tractography-integrated neuronavigation and direct fiber stimulation with monopolar electric currents.

Methods

Forty patients with brain lesions adjacent to the CST were studied. During the operation, the motor responses (motor evoked potential [MEP]) elicited at the hand by the cortical stimulation to the hand motor area were continuously monitored, maintaining the consistent stimulus intensity (mean 15.1 ± 2.21 mA). During lesion resection, direct fiber stimulation was applied to elicit MEP (referred to as fiber MEP) to identify the CST functionally. The threshold intensity for the fiber MEP was determined by searching for the best stimulus point and changing the stimulus intensity. The minimum distance between the resection border and illustrated CST was measured on postoperative isotropic images.

Results

Direct fiber stimulation demonstrated that tractography accurately reflected anatomical CST functioning. There were strong correlations between stimulus intensity for the fiber MEP and the distance between the CST and the stimulus points. The results indicate that the minimum stimulus intensity of 20, 15, 10, and 5 mA had stimulus points ~ 16, 13.2, 9.6, and 4.8 mm from the CST, respectively. The convergent calculation formulated 1.8 mA as the electrical threshold of the CST for the fiber MEP, which was much smaller than that of the hand motor area.

Conclusions

The investigators found that diffusion tensor imaging–based tractography is a reliable way to map the white matter connections in the entire brain in clinical and basic neuroscience applications. By combining these techniques, investigating the cortical-subcortical connections in the human CNS could contribute to elucidating the neural networks of the human brain and shed light on higher brain functions.

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Yuta Fukushima, Soichi Oya, Hirofumi Nakatomi, Junji Shibahara, Shunya Hanakita, Shota Tanaka, Masahiro Shin, Kensuke Kawai, Masashi Fukayama and Nobuhito Saito

Object

Meningiomas treated by subtotal or partial resection are associated with significantly shorter recurrence-free survival than those treated by gross-total resection. The Simpson grading system classifies incomplete resections into a single category, namely Simpson Grade IV, with wide variations in the volume and location of residual tumors, making it complicated to evaluate the achievement of surgical goals and predict the prognosis of these tumors. Authors of the present study investigated the factors related to necessity of retreatment and tried to identify any surgical nuances achievable with the aid of modern neurosurgical techniques for meningiomas treated using Simpson Grade IV resection.

Methods

This retrospective analysis included patients with WHO Grade I meningiomas treated using Simpson Grade IV resection as the initial therapy at the University of Tokyo Hospital between January 1995 and April 2010. Retreatment was defined as reresection or stereotactic radiosurgery due to postoperative tumor growth.

Results

A total of 38 patients were included in this study. Regrowth of residual tumor was observed in 22 patients with a mean follow-up period of 6.1 years. Retreatment was performed for 20 of these 22 tumors with regrowth. Risk factors related to significantly shorter retreatment-free survival were age younger than 50 years (p = 0.006), postresection tumor volume of 4 cm3 or more (p = 0.016), no dural detachment (p = 0.001), and skull base location (p = 0.016). Multivariate analysis revealed that no dural detachment (hazard ratio [HR] 6.42, 95% CI 1.41–45.0; p = 0.02) and skull base location (HR 11.6, 95% CI 2.18–218; p = 0.002) were independent risk factors for the necessity of early retreatment, whereas postresection tumor volume of 4 cm3 or more was not a statistically significant risk factor.

Conclusions

Compared with Simpson Grade I, II, and III resections, Simpson Grade IV resection includes highly heterogeneous tumors in terms of resection rate and location of the residual mass. Despite the difficulty in analyzing such diverse data, these results draw attention to the favorable effect of dural detachment (instead of maximizing the resection rate) on long-term tumor control. Surgical strategy with an emphasis on detaching the tumor from the affected dura might be another important option in resection of high-risk meningiomas not amenable to gross-total resection.

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Sunho Ko, Atsushi Nakazawa, Yusuke Kurose, Kanako Harada, Mamoru Mitsuishi, Shigeo Sora, Naoyuki Shono, Hirofumi Nakatomi, Nobuhito Saito and Akio Morita

OBJECTIVE

Advanced and intelligent robotic control is necessary for neurosurgical robots, which require great accuracy and precision. In this article, the authors propose methods for dynamically and automatically controlling the motion-scaling ratio of a master-slave neurosurgical robotic system to reduce the task completion time.

METHODS

Three dynamic motion-scaling modes were proposed and compared with the conventional fixed motion-scaling mode. These 3 modes were defined as follows: 1) the distance between a target point and the tip of the slave manipulator, 2) the distance between the tips of the slave manipulators, and 3) the velocity of the master manipulator. Five test subjects, 2 of whom were neurosurgeons, sutured 0.3-mm artificial blood vessels using the MM-3 neurosurgical robot in each mode.

RESULTS

The task time, total path length, and helpfulness score were evaluated. Although no statistically significant differences were observed, the mode using the distance between the tips of the slave manipulators improves the suturing performance.

CONCLUSIONS

Dynamic motion scaling has great potential for the intelligent and accurate control of neurosurgical robots.

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Gakushi Yoshikawa, Toshihiko Momiyama, Soichi Oya, Keisuke Takai, Jun-ichi Tanaka, Shigeki Higashiyama, Nobuhito Saito, Takaaki Kirino and Nobutaka Kawahara

Object

The capacity to replace lost neurons after insults is retained by several regions of adult mammalian brains. However, it is unknown how many neurons actually replace and mature into region-specific functional neurons to restore lost brain function. In this paper, the authors asked whether neuronal regeneration could be achieved efficaciously by growth factor treatment using a global ischemia model in rats, and they analyzed neuronal long-term maturation processes.

Methods

Rat global ischemia using a modified 4-vessel occlusion model was used to induce consistent ischemic neuronal injury in the dorsolateral striatum. To potentiate the proliferative response of neural progenitors, epidermal growth factor and fibroblast growth factor–2 were infused intraventricularly for 7 days from Day 2 after ischemia. Six weeks after ischemia, the number of neurons was counted in the defined dorsolateral striatum. To label the proliferating neural progenitors for tracing studies, 5-bromo-2′-deoxyuridine (BrdU; 150 mg/kg, twice a day) was injected intraperitoneally from Days 5 to 7, and immunohistochemical studies were conducted to explore the maturation of these progenitors. Migration of the progenitors was further studied by enhanced green fluorescent protein retrovirus injection. The effect of an antimitotic drug (cytosine arabinoside) on the neuronal count was also evaluated for contribution to regeneration. To see electrophysiological changes, treated rats were subjected to slice studies by whole-cell recordings. Finally, the effect of neural regeneration was assessed by motor performance by using the staircase test.

Results

Following epidermal growth factor and fibroblast growth factor–2 infusion into the lateral ventricles for 7 days beginning on Day 2, when severe neuronal loss in the adult striatum was confirmed (2.3% of normal controls), a significant increase of striatal neurons was observed at 6 weeks (~ 15% of normal controls) compared with vehicle controls (~ 5% of normal controls). Immunohistochemical studies by BrdU and enhanced green fluorescent protein retrovirus injection disclosed proliferation of neural progenitors in the subventricular zone and their migration to the ischemic striatum. By BrdU tracing study, NeuN- and BrdU-positive new neurons significantly increased at 6 and 12 weeks following the treatment. These accounted for 4.6 and 11.0% of the total neurons present, respectively. Antimitotic treatment demonstrated an approximately 66% reduction in neurons at 6 weeks. Further long-term studies showed dynamic changes of site-specific maturation among various neuronal subtypes even after 6 weeks. Electrophysiological properties of these newly appeared neurons underwent changes that conform to neonatal development. These regenerative changes were accompanied by a functional improvement of overall behavioral performance.

Conclusions

Treatment by growth factors significantly contributed to regeneration of mature striatal neurons after ischemia by endogenous neural progenitors, which was accompanied by electrophysiological maturation and improved motor performance. Recognition and improved understanding of these underlying dynamic processes will contribute to the development of novel and efficient regenerative therapies for brain injuries.

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Taichi Kin, Hirofumi Nakatomi, Masaaki Shojima, Minoru Tanaka, Kenji Ino, Harushi Mori, Akira Kunimatsu, Hiroshi Oyama and Nobuhito Saito

Object

In this study, the authors used preoperative simulation employing 3D computer graphics (interactive computer graphics) to fuse all imaging data for brainstem cavernous malformations. The authors evaluated whether interactive computer graphics or 2D imaging correlated better with the actual operative field, particularly in identifying a developmental venous anomaly (DVA).

Methods

The study population consisted of 10 patients scheduled for surgical treatment of brainstem cavernous malformations. Data from preoperative imaging (MRI, CT, and 3D rotational angiography) were automatically fused using a normalized mutual information method, and then reconstructed by a hybrid method combining surface rendering and volume rendering methods. With surface rendering, multimodality and multithreshold techniques for 1 tissue were applied. The completed interactive computer graphics were used for simulation of surgical approaches and assumed surgical fields. Preoperative diagnostic rates for a DVA associated with brainstem cavernous malformation were compared between conventional 2D imaging and interactive computer graphics employing receiver operating characteristic (ROC) analysis.

Results

The time required for reconstruction of 3D images was 3–6 hours for interactive computer graphics. Observation in interactive mode required approximately 15 minutes. Detailed anatomical information for operative procedures, from the craniotomy to microsurgical operations, could be visualized and simulated three-dimensionally as 1 computer graphic using interactive computer graphics. Virtual surgical views were consistent with actual operative views. This technique was very useful for examining various surgical approaches. Mean (± SEM) area under the ROC curve for rate of DVA diagnosis was significantly better for interactive computer graphics (1.000 ± 0.000) than for 2D imaging (0.766 ± 0.091; p < 0.001, Mann-Whitney U-test).

Conclusions

The authors report a new method for automatic registration of preoperative imaging data from CT, MRI, and 3D rotational angiography for reconstruction into 1 computer graphic. The diagnostic rate of DVA associated with brainstem cavernous malformation was significantly better using interactive computer graphics than with 2D images. Interactive computer graphics was also useful in helping to plan the surgical access corridor.

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Hirofumi Nakatomi, Jeffrey T. Jacob, Matthew L. Carlson, Shota Tanaka, Minoru Tanaka, Nobuhito Saito, Christine M. Lohse, Colin L. W. Driscoll and Michael J. Link

OBJECTIVE

The management of vestibular schwannoma (VS) remains controversial. One commonly cited advantage of microsurgery over other treatment modalities is that tumor removal provides the greatest chance of long-term cure. However, there are very few publications with long-term follow-up to support this assertion. The purpose of the current study is to report the very long-term risk of recurrence among a large historical cohort of patients who underwent microsurgical resection.

METHODS

The authors retrospectively reviewed the medical records of patients who had undergone primary microsurgical resection of unilateral VS via a retrosigmoid approach performed by a single neurosurgeon-neurotologist team between January 1980 and December 1999. Complete tumor removal was designated gross-total resection (GTR), and anything less than complete removal was designated subtotal resection (STR). The primary end point was radiological recurrence-free survival. Time-to-event analyses were performed to identify factors associated with recurrence.

RESULTS

Four hundred fourteen patients met the study inclusion criteria and were analyzed. Overall, 67 patients experienced recurrence at a median of 6.9 years following resection (IQR 3.9–12.1, range 1.2–22.5 years). Estimated recurrence-free survival rates at 5, 10, 15, and 20 years following resection were 93% (95% CI 91–96, 248 patients still at risk), 78% (72–85, 88), 68% (60–77, 47), and 51% (41–64, 22), respectively. The strongest predictor of recurrence was extent of resection, with patients who underwent STR having a nearly 11-fold greater risk of recurrence than the patients treated with GTR (HR 10.55, p < 0.001). Among the 18 patients treated with STR, 15 experienced recurrence at a median of 2.7 years following resection (IQR 1.9–8.9, range 1.2–18.7). Estimated recurrence-free survival rates at 5, 10, 15, and 20 years following GTR were 96% (95% CI 93–98, 241 patients still at risk), 82% (77–89, 86), 73% (65–81, 46), and 56% (45–70, 22), respectively. Estimated recurrence-free survival rates at 5, 10, and 15 years following STR were 47% (95% CI 28–78, 7 patients still at risk), 17% (5–55, 2), and 8% (1–52, 1), respectively.

CONCLUSIONS

Long-term surveillance is required following microsurgical resection of VS even after GTR. Subtotal resection alone should not be considered a definitive long-term cure. These data emphasize the importance of long-term follow-up when reporting tumor control outcomes for VS.

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Hua Zhong, Zhihong Zhou, Guo-Hua Lv, Jing Li and Ming-Xiang Zou

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Mitsunobu Nakamura, Hideaki Imai, Kenjiro Konno, Chisato Kubota, Koji Seki, Sandra Puentes, Ahmad Faried, Hideaki Yokoo, Hidekazu Hata, Yuhei Yoshimoto and Nobuhito Saito

Object

Encephalomyosynangiosis (EMS) is a surgical treatment for moyamoya disease that is widely used to provide increased intracranial blood flow via revascularization by arterial anastomosis from the external carotid artery. However, the angiogenic mechanism responsible for the revascularization induced by EMS has not been systematically evaluated. In this study the authors investigated the chronological angiogenic changes associated with EMS to clarify the favorable factors and identify revascularization mechanisms by using an experimental internal carotid artery occlusion (ICAO) model in the miniature pig.

Methods

Fourteen miniature pigs were used, 11 of which underwent ICAO before transcranial surgery for EMS was performed. Animals were allowed to recover for 1 week (4 pigs) or 4 weeks (7 pigs) after EMS. Control group animals were treated in the same way, but without occlusion (3 pigs). Magnetic resonance imaging, angiography, and histological investigation were performed.

Results

One week after EMS, on histological examination of both the ICAO and control groups it was found that the transplanted temporal muscle had adhered to the arachnoid via a granulation zone, which was enriched with immune cells such as macrophages associated with the angiogenic process. Four weeks after EMS, angiography and histological examination of the ICAO group showed patent anastomoses between the external carotid artery and the cortical arteries without any detectable boundary between the temporal muscle and the cerebral cortex. In contrast, histological examination of the control group found scar tissue between the cerebral cortex and temporal muscle.

Conclusions

The initial step for formation of anastomoses resembles the process of wound healing associated with repair processes such as active proliferation of macrophages and angiogenesis within the new connective tissue. Functional revascularization requires a suitable environment (such as tissue containing vascular beds) and stimulus (such as ischemia) to induce vascular expansion.

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Hideaki Imai, Kenjiro Konno, Mitsunobu Nakamura, Tatsuya Shimizu, Chisato Kubota, Koji Seki, Fumiaki Honda, Shinichiro Tomizawa, Yukitaka Tanaka, Hidekazu Hata and Nobuhito Saito

Object

The purpose of this set of studies is to design a minimally invasive, reproducible stroke model in the gyrencephalic brain. This paper provides information on both surgical technique and methods of quantification of ischemic damage to both gray and white matter in the miniature pig.

Methods

Sixteen male miniature pigs were randomly divided into three groups and underwent transcranial surgery involving a frontotemporal approach with orbital rim osteotomy for permanent middle cerebral artery occlusion (MCAO; five animals), permanent internal carotid artery occlusion (ICAO; six animals), and a sham operation (five animals). Histological mapping and magnetic resonance (MR) imaging were used to delineate the areas of ischemic damage. The volumes of infarction measured directly from MR images were 16.2 ± 1.1, 1.5 ± 0.5, and 0.0 ± 0.0 cm3 (mean ± standard deviation [SD], p < 0.001) in the MCAO, ICAO, and sham-operated groups, respectively. The areas of ischemia identified through histological analysis and MR imaging showed a good correlation (r2 = 0.86, p < 0.0001). Immunohistochemical staining with an amyloid precursor protein (APP) antibody was used to evaluate axonal damage and calculate a total APP score for axonal damage of 44.8 ± 2.9 in the MCAO, 13.2 ± 6.6 in the ICAO, and 0.0 ± 0.0 (mean ± SD, p < 0.002) in the sham-operated animals.

Conclusions

This new model of focal cerebral ischemia induces a reproducible amount of ischemic damage in both gray and white matter, and has significant utility for studies of the pathophysiology of ischemia in the gyrencephalic brain and for assessment of the therapeutic efficacy of drugs prior to the initiation of human clinical trials.

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Hirofumi Nakatomi, Hidemi Miyazaki, Minoru Tanaka, Taichi Kin, Masanori Yoshino, Hiroshi Oyama, Masaaki Usui, Hiroshi Moriyama, Hiromi Kojima, Kimitaka Kaga and Nobuhito Saito

OBJECT

Restoration of cranial nerve functions during acoustic neuroma (AN) surgery is crucial for good outcome. The effects of minimizing the injury period and maximizing the recuperation period were investigated in 89 patients who consecutively underwent retrosigmoid unilateral AN surgery.

METHODS

Cochlear nerve and facial nerve functions were evaluated during AN surgery by use of continuous auditory evoked dorsal cochlear nucleus action potential monitoring and facial nerve root exit zone–elicited compound muscle action potential monitoring, respectively. Factors affecting preservation of function at the same (preoperative) grade were analyzed.

RESULTS

A total of 23 patients underwent standard treatment and investigation of the monitoring threshold for preservation of function; another 66 patients underwent extended recuperation treatment and assessment of its effect on recovery of nerve function. Both types of final action potential monitoring response and extended recuperation treatment were associated with preservation of function at the same grade.

CONCLUSIONS

Preservation of function was significantly better for patients who received extended recuperation treatment.