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Haruhiko Kishima, Keiji Shimizu, Yasuyoshi Miyao, Eiichiro Mabuchi and Toru Hayakawa

✓ A primary intracranial germ cell tumor in a 16-year-old boy secreted both a-fetoprotein (AFP) and human chorionic gonadotropin (HCG). The tumor, located in the right thalamus, contained germinomatous, trophoblastic, and endodermal sinus components. To identify AFP- and HCG-secreting cells, germ cells from the surgical specimen were cultured in vitro. These cultured cells secreted AFP and HCG for 10 weeks, and immunohistochemical studies showed that some of the cells secreted both AFP and HCG. These findings suggest that multipotential germ cells migrate to the encephalic region and may become germ cell tumors containing various types of tissue.

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Ryuichi Hirayama, Manabu Kinoshita, Hideyuki Arita, Naoki Kagawa, Haruhiko Kishima, Naoya Hashimoto, Yasunori Fujimoto and Toshiki Yoshimine

OBJECTIVE

In the present study the authors aimed to determine preferred locations of meningiomas by avoiding descriptive analysis and instead using voxel-based lesion mapping and 3D image-rendering techniques.

METHODS

Magnetic resonance images obtained in 248 treatment-naïve meningioma patients with 260 lesions were retrospectively and consecutively collected. All images were registered to a 1-mm isotropic, high-resolution, T1-weighted brain atlas provided by the Montreal Neurological Institute (the MNI152), and a lesion frequency map was created, followed by 3D volume rendering to visualize the preferred locations of meningiomas in 3D.

RESULTS

The 3D lesion frequency map clearly showed that skull base structures such as parasellar, sphenoid wing, and petroclival regions were commonly affected by the tumor. The middle one-third of the superior sagittal sinus was most commonly affected in parasagittal tumors. Substantial lesion accumulation was observed around the leptomeninges covering the central sulcus and the sylvian fissure, with very few lesions observed at the frontal, parietal, and occipital convexities.

CONCLUSIONS

Using an objective visualization method, meningiomas were shown to be located around the middle third of the superior sagittal sinus, the perisylvian convexity, and the skull base. These observations, which are in line with previous descriptive analyses, justify further use of voxel-based lesion mapping techniques to help understand the biological nature of this disease.

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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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Takufumi Yanagisawa, Masayuki Hirata, Youichi Saitoh, Tetsu Goto, Haruhiko Kishima, Ryohei Fukuma, Hiroshi Yokoi, Yukiyasu Kamitani and Toshiki Yoshimine

Object

A brain-machine interface (BMI) offers patients with severe motor disabilities greater independence by controlling external devices such as prosthetic arms. Among the available signal sources for the BMI, electrocorticography (ECoG) provides a clinically feasible signal with long-term stability and low clinical risk. Although ECoG signals have been used to infer arm movements, no study has examined its use to control a prosthetic arm in real time. The authors present an integrated BMI system for the control of a prosthetic hand using ECoG signals in a patient who had suffered a stroke. This system used the power modulations of the ECoG signal that are characteristic during movements of the patient's hand and enabled control of the prosthetic hand with movements that mimicked the patient's hand movements.

Methods

A poststroke patient with subdural electrodes placed over his sensorimotor cortex performed 3 types of simple hand movements following a sound cue (calibration period). Time-frequency analysis was performed with the ECoG signals to select 3 frequency bands (1–8, 25–40, and 80–150 Hz) that revealed characteristic power modulation during the movements. Using these selected features, 2 classifiers (decoders) were trained to predict the movement state—that is, whether the patient was moving his hand or not—and the movement type based on a linear support vector machine. The decoding accuracy was compared among the 3 frequency bands to identify the most informative features. With the trained decoders, novel ECoG signals were decoded online while the patient performed the same task without cues (free-run period). According to the results of the real-time decoding, the prosthetic hand mimicked the patient's hand movements.

Results

Offline cross-validation analysis of the ECoG data measured during the calibration period revealed that the state and movement type of the patient's hand were predicted with an accuracy of 79.6% (chance 50%) and 68.3% (chance 33.3%), respectively. Using the trained decoders, the onset of the hand movement was detected within 0.37 ± 0.29 seconds of the actual movement. At the detected onset timing, the type of movement was inferred with an accuracy of 69.2%. In the free-run period, the patient's hand movements were faithfully mimicked by the prosthetic hand in real time.

Conclusions

The present integrated BMI system successfully decoded the hand movements of a poststroke patient and controlled a prosthetic hand in real time. This success paves the way for the restoration of the patient's motor function using a prosthetic arm controlled by a BMI using ECoG signals.

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Masanori Aoki, Haruhiko Kishima, Kazuhiro Yoshimura, Masahiro Ishihara, Masaki Ueno, Katsuhiko Hata, Toshihide Yamashita, Koichi Iwatsuki and Toshiki Yoshimine

Object

The olfactory mucosa (OM) consists of 2 layers, the epithelium and the lamina propria. Attempts have been made to restore motor function in rat models of spinal cord injury (SCI) by transplanting olfactory ensheathing cells from the lamina propria, but there has been no attempt to transplant the OM in animal models. To investigate the potential of the OM to restore motor function, the authors developed a rat model of SCI and delayed transplantation of syngenic OM.

Methods

Two weeks after complete transection of the spinal cord at the T-10 level in Wistar rats, pieces of syngenic whole-layer OM were transplanted into the lesion. Rats that underwent respiratory mucosa transplantation were used as controls. The authors evaluated the locomotor activity according to the Basso-Beattie-Bresnahan scale for 8 weeks after transplantation. Obtained spinal cords were analyzed histologically.

Results

The OM transplantation rats showed significantly greater hindlimb locomotor recovery than the respiratory mucosa–transplanted rats. However, the recovery was limited according to the Basso-Beattie-Bresnahan scale. In the histological examination, the serotonergic raphespinal tract was regenerated. The pseudocyst cavity volume in the vicinity of the SCI lesion correlated negatively with the functional recovery.

Conclusions

Transplantation of whole-layer OM in rats contributes to functional recovery from SCI, but the effect is limited. In addition to OM transplantation, other means would be necessary for better outcomes in clinical situations.

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Youichi Saitoh, Azuma Hirayama, Haruhiko Kishima, Toshio Shimokawa, Satoru Oshino, Masayuki Hirata, Naoki Tani, Amami Kato and Toshiki Yoshimine

Object

The authors previously reported that navigation-guided repetitive transcranial magnetic stimulation (rTMS) of the precentral gyrus relieves deafferentation pain. Stimulation parameters were 10 trains of 10-second 5-Hz TMS pulses at 50-second intervals. In the present study, they used various stimulation frequencies and compared efficacies between two types of lesions.

Methods

Patients were divided into two groups: those with a cerebral lesion and those with a noncerebral lesion. The rTMS was applied to all the patients at frequencies of 1, 5, and 10 Hz and as a sham procedure in random order. The effect of rTMS on pain was rated by patients using a visual analog scale.

Results

The rTMS at frequencies of 5 and 10 Hz, compared with sham stimulation, significantly reduced pain, and the pain reduction continued for 180 minutes. A stimulation frequency of 10 Hz may be more effective than 5 Hz, and at 1 Hz was ineffective. The effect of rTMS at frequencies of 5 and 10 Hz was greater in patients with a noncerebral lesion than those with a cerebral lesion.

Conclusions

High-frequency (5- or 10-Hz) rTMS of the precentral gyrus can reduce intractable deafferentation pain, but low-frequency stimulation (at 1 Hz) cannot. Patients with a noncerebral lesion are more suitable candidates for high-frequency rTMS of the precentral gyrus.

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Youichi Saitoh, Shun-ichiro Hirano, Amami Kato, Haruhiko Kishima, Masayuki Hirata, Kazumi Yamamoto and Toshiki Yoshimine

Object

The authors tested a modified motor cortex stimulation (MCS) protocol for the treatment of deafferentation pain in 15 patients: eight patients with poststroke pain, four with brachial plexus injury, two with phantom limb pain, and one with spinal cord injury.

Methods

Preoperative pharmacological tests were performed with phentolamine, lidocaine, ketamine, thiopental, morphine, and a placebo. In 12 patients we placed a 20– or 40–grid electrode in the subdural space to determine the best stimulation point for pain relief over a few weeks and therefore the optimum position for a permanent internal device. In four patients, the MCS devices were implanted in the interhemispheric fissure to reduce lower-extremity pain. In one patient, the MCS device was placed within the central sulcus, and a 20-grid electrode was placed on the brain surface. In two patients with pain extending from the upper extremity to the hyperbody, dual-electrode devices were implanted to drive two electrodes. In 10 of the 15 patients MCS-induced pain reduction was achieved (four with excellent, two with good, and four with fair alleviation of pain). The result of pharmacological testing indicated that patients with ketamine sensitivity seem to be good candidates for MCS.

Conclusions

Test stimulation with a subdural multigrid electrode was helpful in locating the best stimulation point for pain relief.

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Haruhiko Kishima, Youichi Saitoh, Yasuhiro Osaki, Hiroshi Nishimura, Amami Kato, Jun Hatazawa and Toshiki Yoshimine

Object

The mechanisms underlying deafferentation pain are not well understood. Motor cortex stimulation (MCS) is useful in the treatment of this kind of chronic pain, but the detailed mechanisms underlying its effects are unknown.

Methods

Six patients with intractable deafferentation pain in the left hand were included in this study. All were right-handed and had a subdural electrode placed over the right precentral gyrus. The pain was associated with brainstem injury in one patient, cervical spine injury in one patient, thalamic hemorrhage in one patient, and brachial plexus avulsion in three patients. Treatment with MCS reduced pain; visual analog scale (VAS) values for pain were 82 ± 20 before MCS and 39 ± 20 after MCS (mean ± standard error). Regional cerebral blood flow (rCBF) was measured by positron emission tomography with H2 15O before and after MCS. The obtained images were analyzed with statistical parametric mapping software (SPM99).

Results

Significant rCBF increases were identified after MCS in the left posterior thalamus and left insula. In the early post-MCS phase, the left posterior insula and right orbitofrontal cortex showed significant rCBF increases, and the right precentral gyrus showed an rCBF decrease. In the late post-MCS phase, a significant rCBF increase was detected in the left caudal part of the anterior cingulate cortex (ACC).

Conclusions

These results suggest that MCS modulates the pathways from the posterior insula and orbitofrontal cortex to the posterior thalamus to upregulate the pain threshold and pathways from the posterior insula to the caudal ACC to control emotional perception. This modulation results in decreased VAS scores for deafferentation pain.

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Manabu Kinoshita, Hideyuki Arita, Yoshiko Okita, Naoki Kagawa, Haruhiko Kishima, Naoya Hashimoto, Hisashi Tanaka, Yoshiyuki Watanabe, Eku Shimosegawa, Jun Hatazawa, Yasunori Fujimoto and Toshiki Yoshimine

OBJECTIVE

Diffusion MRI is attracting increasing interest for tissue characterization of gliomas, especially after the introduction of antiangiogenic therapy to treat malignant gliomas. The goal of the current study is to elucidate the actual magnitude of the correlation between diffusion MRI and cell density within the tissue. The obtained results were further extended and compared with metabolic imaging with 11C-methionine (MET) PET.

METHODS

Ninety-eight tissue samples from 37 patients were stereotactically obtained via an intraoperative neuronavigation system. Diffusion tensor imaging (DTI) and MET PET were performed as routine presurgical imaging studies for these patients. DTI was converted into fractional anisotropy (FA) and apparent diffusion coefficient (ADC) maps, and MET PET images were registered to Gd-administered T1-weighted images that were used for navigation. Metrics of FA, ADC, and tumor-to-normal tissue ratio of MET PET along with relative values of FA (rFA) and ADC (rADC) compared with normal-appearing white matter were correlated with cell density of the stereotactically obtained tissues.

RESULTS

rADC was significantly lower in lesions obtained from Gd-enhancing lesions than from nonenhancing lesions. Although rADC showed a moderate but statistically significant negative correlation with cell density (p = 0.010), MET PET showed a superb positive correlation with cell density (p < 0.0001). On the other hand, rFA showed little correlation with cell density.

CONCLUSIONS

The presented data validated the use of rADC for estimating the treatment response of gliomas but also caution against overestimating its limited accuracy compared with MET PET.

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Naoya Hashimoto, Carter S. Rabo, Yoshiko Okita, Manabu Kinoshita, Naoki Kagawa, Yasunori Fujimoto, Eiichi Morii, Haruhiko Kishima, Motohiko Maruno, Amami Kato and Toshiki Yoshimine

Object

The precise natural history of incidentally discovered meningiomas (IDMs) remains unknown. It has been reported that for symptomatic meningiomas, tumor location can be used to predict growth. As to whether the same is true for IDMs has not been reported. This study aims to answer this question and provide biological evidence for this assumption by extending the study to involve symptomatic cases.

Methods

A total of 113 IDMs were analyzed by fine volumetry. A comparison of growth rates and patterns between skull base and non–skull base IDMs was made. Subsequently, materials obtained from 210 patients with symptomatic meningiomas who were treated in the authors' hospital during the same period were included for a biological comparison between skull base and non–skull base tumors using the MIB-1 index.

Results

The 110 patients with IDMs included 93 females and 17 males, with a mean follow-up period of 46.9 months. There were 38 skull base (34%) and 75 non–skull base (66%) meningiomas. Forty-two (37%) did not exhibit growth of more than 15% of the volume, whereas 71 (63%) showed growth. Only 15 (39.5%) of 38 skull base meningiomas showed growth, whereas 56 (74.7%) of 75 non–skull base meningiomas showed growth (p = 0.0004). In the 71 IDMs (15 skull base and 56 non–skull base), there was no statistical difference between the 2 groups in terms of mean age, sex, follow-up period, or initial tumor volume. However, the percentage of growth (p = 0.002) was significantly lower and the doubling time (p = 0.008) was significantly higher in the skull base than in the non–skull base tumor group. In subsequently analyzed materials from 94 skull base and 116 non–skull base symptomatic meningiomas, the mean MIB-1 index for skull base tumors was markedly low (2.09%), compared with that for non–skull base tumors (2.74%; p = 0.013).

Conclusions

Skull base IDMs tend not to grow, which is different from non–skull base tumors. Even when IDMs grow, the rate of growth is significantly lower than that of non–skull base tumors. The same conclusion with regard to biological behavior was confirmed in symptomatic cases based on MIB-1 index analyses. The authors' findings may impact the understanding of the natural history of IDMs, as well as strategies for management and treatment of IDMs and symptomatic meningiomas.