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Kiyohiro Houkin and Satoshi Kuroda

✓ The authors examine the quality of intraoperative photography in which digital recording technology, including a microdigital camera and digital video paired with an operating microscope, is used during neurosurgery. A microdigital camera developed for this purpose (1.4 million pixels) was attached to an operating microscope and used during surgery. The same surgical views with precisely the same optical conditions were taken through the microscope by using both a conventional 35-mm camera and the microdigital camera, and the quality of the final output was compared. In addition, the quality of the digital camera photographs was compared with the still photograph clipped from the digital video recording.

The quality of the photographs taken with a microdigital camera was superior to the quality of those obtained with the conventional 35-mm camera. The success rate of recording (what you see is what you get) was almost 100%. The quality of the still photographs clipped from the digital video was nearly equal to those taken with the digital camera. The microdigital camera system is superior to the conventional 35-mm camera in neurosurgery in terms of its success rate and the quality of the photography. It is also a space-saving system for storing the huge amount of data generated in the recording of surgical procedures, and the cost/performance ratio is superior to that of the conventional method. Digital technology including digital cameras and videos is very useful for clear recording of microsurgical procedures.

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Mitsunori Matsumae, Akihiro Hirayama, Hideki Atsumi, Satoshi Yatsushiro and Kagayaki Kuroda

Object

New approaches for understanding CSF motion in healthy individuals and patients with hydrocephalus and Chiari malformation are presented. The velocity and the pressure gradient of CSF motion were determined using phase contrast (PC) MRI.

Methods

The authors examined 11 healthy control subjects and 2 patients (1 with hydrocephalus and 1 with Chiari malformation), using 4-dimensional PC (4D-PC) MRI and a newly developed computer analysis method that includes calculation of the pressure gradient from the velocity field. Sagittal slices including the center of the skull and coronal slices of the foramen of Monro and the third ventricle were used.

Results

In the ventricular system, mixing and swirling of the CSF was observed in the third ventricle. The velocity images showed that the CSF was pushed up and back down to the adjacent ventricle and then returned again to the third ventricle. The CSF traveled bidirectionally in the foramen of Monro and sylvian aqueduct. Around the choroid plexus in the lateral ventricle, the CSF motion was stagnant and the CSF pressure gradient was lower than at the other locations. An elevated pressure gradient was observed in the basal cistern of the subarachnoid space. Sagittal imaging showed that the more prominent pressure gradients originated around the cisterna magna and were transmitted in an upward direction. The coronal image showed a pressure gradient traveling from the central to the peripheral subarachnoid spaces that diminished markedly in the convexity of the cerebrum. The 2 patients, 1 with secondary hydrocephalus and 1 with Chiari malformation, were also examined.

Conclusions

The observed velocity and pressure gradient fields delineated the characteristics of the CSF motion and its similarities and differences among the healthy individuals and between them and the 2 patients. Although the present results did not provide general knowledge of CSF motion, the authors' method more comprehensively described the physiological properties of the CSF in the skull than conventional approaches that do not include measurements of pressure gradient fields.

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Satoshi Ushikoshi, Kiyohiro Houkin, Fumio Itoh, Hisatoshi Saitoh, Michimasa Nozaki, Satoshi Kuroda and Hiroshi Abe

✓ The authors describe the case of a 69-year-old man with an intracerebral hemorrhage due to rupture of a nontraumatic aneurysm of the middle meningeal artery (MMA). The ipsilateral posterior cerebral artery (PCA) was occluded, and dural anastomoses developed as the main collateral pathway between the MMA and the cortical branch of the PCA, on which the aneurysm was located. It is considered that increased hemodynamic stress to the collateral pathway contributed to the formation of the aneurysm.

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Hiroshi Yasuda, Satoshi Kuroda, Hideo Shichinohe, Shintaro Kamei, Ryoichi Kawamura and Yoshinobu Iwasaki

Object

In this study the authors' aim was to assess whether fibrin matrix could act as an injectable, valuable scaffold in bone marrow stromal cell (BMSC) transplantation for injured CNS tissue.

Methods

Both clotting time and 3D structure of fibrin matrix were analyzed with various concentrations of fibrinogen and CaCl2. The BMSCs were harvested from green fluorescent protein–transgenic mice and cultured. A cortical lesion was produced in rats by application of a very cold rod to the right cerebral hemisphere. The BMSCs, fibrin matrix, or BMSC–fibrin matrix complex was transplanted into the lesion though a small bur hole 7 days after the insult. Using immunohistochemical analysis, the authors evaluated the survival, migration, and differentiation of the transplanted cells 4 weeks after transplantation.

Results

Based on in vitro observations, the concentrations of fibrinogen and CaCl2 were fixed at 2.5 mg/ml and 2 μM in animal experiments, respectively. Fibrin matrix almost completely disappeared 4 weeks after transplantation. However, immunohistochemical analysis revealed that fibrin matrix exclusively enhanced the retention of the transplanted cells within the lesion, migration toward the lesion boundary zone, and differentiation into the neurons and perivascular cells.

Conclusions

Injectable fibrin matrix enhanced the survival, migration, and differentiation of the BMSCs transplanted into the cortical lesion in rats. The authors believe that it is one of the promising candidates for a potential, minimally invasive scaffold for CNS disorders. The present findings strongly suggest that such a strategy of tissue engineering could be a therapeutic option for CNS regeneration in patients with CNS injuries.

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Yoshiteru Nakano, Etsushi Kuroda, Tomohiro Kito, Satoshi Uematsu, Shizuo Akira, Akira Yokota, Shigeru Nishizawa and Uki Yamashita

Object

Microglia are one of the members of monocyte/macrophage lineage in the central nervous system (CNS) and exist as ramified microglia in a normal resting state, but they are activated by various stimuli, such as tumors. Activated microglia induce immune responses in the CNS, but the precise functions of microglia in glioma microenvironments are not clear. It has been reported that glioma cells produce prostaglandin (PG)E2, which promotes the growth of tumor cells and possesses immunosuppressive activity. The authors previously reported that PGE2 production by peritoneal macrophages was enhanced by glioma-derived soluble factors, which induce an immunosuppressive state. In this study, they investigated PGE2 production by microglia treated with glioma cells and assessed the role of microglia in glioma microenvironments in the mouse.

Methods

Microglia and peritoneal macrophages were cultured in vitro with or without lipopolysaccharide, and tumor necrosis factor (TNF) and PGE2 in the culture supernatant were measured using L929 bioassay and enzyme immunoassay. The expression of mRNA was measured using reverse transcriptase polymerase chain reaction, and the protein expression was assayed with Western blotting. In some experiments glioma cells and conditioned glioma medium were added to the microglia cultures.

Results

Glioma cells studied in this report did not produce a significant amount of PGE2. However, the coculture of microglia with glioma cells or conditioned glioma medium led to the production of a large amount of PGE2. The enhancement of PGE2 production by microglia was more significant than that by peritoneal macrophages. The expression of cyclooxygenase (COX)–2 and particularly the expression of microsomal PGE synthase (mPGES)–1 (a terminal enzyme of the arachidonate cascade) in microglia were enhanced by conditioned glioma medium. The enhancement of mPGES-1 expression in microglia was more significant than that in peritoneal macrophages. The production of TNF was suppressed when culturing microglia with conditioned glioma medium, but this suppression was abrogated by the addition of a COX inhibitor (NS-398) and a PGE2 receptor (EP4) antagonist. Furthermore, TNF production was not suppressed in microglia from mPGES-1–deficient mice.

Conclusions

These results indicate that PGE2 production by microglia is enhanced by conditioned glioma medium, which induces an immunosuppressive state in the CNS. Therefore, the manipulation of microglia, from the standpoint of PGE2, provides investigators with an important strategy to induce an effective antiglioma immune response.

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Daina Kashiwazaki, Naoki Akioka, Naoya Kuwayama, Tomohide Hayashi, Kyo Noguchi, Kortaro Tanaka and Satoshi Kuroda

OBJECTIVE

The roles of endothelial progenitor cells (EPCs) in the development of carotid plaque are still obscure. This study aimed to clarify this by assessing the histological findings of specimens obtained from carotid endarterectomy.

METHODS

This study included 34 patients who underwent carotid endarterectomy. MR imaging was performed to semiquantitatively analyze the components of the carotid plaques in all patients. The surgical specimens were subjected to immunohistochemistry. The distributions of the CD34-, CD133-, VEGF-2R–positive cells in the carotid plaques were precisely analyzed, and their number was quantified. Simultaneously, the CD34-positive microvessels were localized.

RESULTS

The plaque component was judged as lipid-rich plaque in 19 patients, intraplaque hemorrhage (IPH) in 11 patients, and fibrous plaque in 4 patients. The CD34-positive microvessels were densely distributed in the plaque shoulder and interface-to-media regions. The CD34-, CD133-, and VEGF-2R–positive cells were mainly localized around the CD34-positive microvessels. The number of CD34-positive microvessels significantly correlated with the number of CD34-, CD133-, and VEGF-2R–positive cells (R = 0.308, p = 0.009; R = 0.324, p = 0.006; and R = 0.296, p = 0.013, respectively). Vulnerable plaques (lipid-rich and IPH) had significantly higher numbers of the CD34-positive microvessels (p = 0.007) and CD34-, CD133-, and VEGF-2R–positive cells than fibrous plaques (p = 0.031, p = 0.013, and p = 0.002).

CONCLUSIONS

These findings strongly suggest that neovascularization in the plaque shoulder and interface-to-media regions may play a key role in delivering EPCs from the peripheral blood to the carotid plaque, promoting the growth of carotid plaque. Furthermore, the invaded EPCs, especially the CD133-positive immature EPCs, may be related to plaque vulnerability.

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Kiyohiro Houkin, Hiroyasu Kamiyama, Satoshi Kuroda, Tatsuya Ishikawa, Akihiro Takahashi and Hiroshi Abe

✓ Reconstruction of the carotid artery by using a radial artery graft is a useful option that can produce reliable long-term patency for the surgical treatment of giant and/or large aneurysms of the cavernous and paraclinoid internal carotid artery (ICA).

During the past 10 years, 43 patients with intracavernous and paraclinoid giant aneurysms of the ICA have been treated by reconstruction of the ICA with radial artery grafts after ligation of the cervical ICA. The long-term patency of the grafted radial artery was evaluated over more than a 5-year period (mean 7.2 years) in 20 of these patients by using magnetic resonance angiography or conventional angiography. There was no late occlusion of the graft in any of these cases. Stenotic graft changes were observed in two cases.

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Daina Kashiwazaki, Masaki Koh, Haruto Uchino, Naoki Akioka, Naoya Kuwayama, Kyo Noguchi and Satoshi Kuroda

OBJECTIVE

The relationship between intraplaque hypoxia and intraplaque hemorrhage (IPH) has been reported, but the details remain obscure. In this study, the authors aimed to clarify the relationship among intraplaque hypoxia, endothelial progenitor cells (EPCs), and neovascularization, which causes IPH. The histological findings of specimens obtained from carotid endarterectomy were assessed.

METHODS

This study included 49 patients who underwent carotid endarterectomy. Magnetic resonance plaque imaging was performed to analyze the components of the carotid plaques, and surgical specimens were subjected to immunohistochemical analysis. The numbers of hypoxia-inducible factor-1 alpha (HIF-1α)–, CD34-, CD133-, and vascular endothelial growth factor receptor-2 (VEGFR-2)–positive cells in the carotid plaques were precisely quantified, as were the number and maximum diameter of CD31-positive microvessels.

RESULTS

Plaque components were judged as fibrous in 7 samples, lipid-rich in 22, and IPH in 20. The number of CD34-, VEGFR-2–, and CD133-positive cells as an EPC-specific marker was significantly correlated with the number of HIF-1α–positive cells (r = 0.9, r = 0.82, and r = 0.81, respectively). These numbers varied among the 3 plaque components (IPH > lipid-rich > fibrous). The number and maximum luminal diameter of CD31-positive microvessels were also significantly correlated with the number of HIF-1α–positive cells (r = 0.85 and r = 0.89, respectively) and varied among the 3 plaque components (IPH > lipid-rich > fibrous).

CONCLUSIONS

The present findings suggest that intraplaque hypoxia may accelerate abnormal microvessel formation derived from EPCs, which in turn promotes IPH. The results also suggest that microvessel enlargement is a pivotal characteristic of IPH and these enlarged microvessels are immature endothelial tubes with disorganized branching and are fragile and prone to rupture.

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Miki Fujimura, Takeshi Funaki, Kiyohiro Houkin, Jun C. Takahashi, Satoshi Kuroda, Yasutake Tomata, Teiji Tominaga and Susumu Miyamoto

OBJECTIVE

This study was performed to identify the angiographic features of hemorrhagic-onset moyamoya disease (MMD) in comparison with those of patients with ischemic-onset MMD.

METHODS

This case-control study compared the data set of the Japan Adult Moyamoya (JAM) Trial with the angiographic data of adult patients with ischemic-onset MMD. The authors analyzed angiograms obtained at onset, classifying the collaterals into 3 subtypes: lenticulostriate anastomosis, thalamic anastomosis, and choroidal anastomosis. They then compared the extent of these collaterals, as indicated by the collateral development grade from 0 to 2 in each subtype, between the JAM Trial group and the ischemic-onset group. They also compared the involvement of the posterior cerebral artery (PCA) and Suzuki’s angiographic staging between each group.

RESULTS

Among 89 ischemic-onset patients, 103 symptomatic hemispheres in 80 patients were analyzed and compared with 75 hemorrhagic hemispheres from the JAM Trial. The hemorrhagic-onset patients showed a significantly higher proportion of thalamic anastomosis (p = 0.043) and choroidal anastomosis (< 0.001), as indicated by grade 2 in each subtype, compared with ischemic-onset patients. Suzuki’s angiographic staging was significantly higher in the hemorrhagic group (< 0.038). There was no difference in the extent of lenticulostriate anastomosis and PCA involvement between the groups.

CONCLUSIONS

In adult MMD, the characteristic pattern of the abnormal vascular networks at the base of the brain is different between each onset type. In light of the more prominent development of thalamic and choroidal anastomosis in the JAM Trial group in the present study, development of these collaterals, especially the choroidal collateral extending beyond the lateral ventricle, may play a critical role in hemorrhagic presentation in MMD.

Clinical trial registration no. C000000166 (http://www.umin.ac.jp/ctr/index.htm)

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Takeshi Funaki, Jun C. Takahashi, Kiyohiro Houkin, Satoshi Kuroda, Shigekazu Takeuchi, Miki Fujimura, Yasutake Tomata and Susumu Miyamoto

OBJECTIVE

In this paper, the authors set out to identify the angiographic features of moyamoya disease with posterior hemorrhage, which is a strong predictor of rebleeding.

METHODS

This cross-sectional study used the data set of the Japan Adult Moyamoya Trial (clinical trial registration no.: C000000166 [www.umin.ac.jp/ctr/index.htm]). The panel designed the ancillary measurement of angiography at onset, classifying the collateral vessels into 3 subtypes: lenticulostriate anastomosis, thalamic anastomosis, and choroidal anastomosis. The association between each collateral and the hemorrhage site (anterior vs posterior) was assessed in the hemorrhagic hemisphere by using multivariate adjustment for potential confounders, including age, sex, and involvement of the posterior cerebral artery (PCA). The association was confirmed through topographical analysis of bleeding points.

RESULTS

Among the 80 participants, 75 hemorrhagic hemispheres of 75 patients were analyzed. Lenticulostriate anastomosis was detected in 21 (28.0%) hemorrhagic hemispheres, thalamic anastomosis in 22 (29.3%), and choroidal anastomosis in 35 (46.7%). Choroidal anastomosis was a factor associated with posterior hemorrhage (OR 2.77 [95% CI 1.08–7.10], p = 0.034) and remained statistically significant after the multivariate adjustment (OR 2.66 [95% CI 1.00–7.07], p = 0.049). PCA involvement was also associated with posterior hemorrhage in both univariate and multivariate analyses. Topographical analysis revealed good correspondence between bleeding points associated with positive choroidal anastomosis and the anatomical distribution of the choroidal arteries, including the thalamus and the wall of the atrium.

CONCLUSIONS

Choroidal anastomosis and PCA involvement are characteristic of posterior hemorrhage in moyamoya disease. Choroidal anastomosis might be considered a potential source of posterior hemorrhage at high risk of rebleeding.