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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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Shusuke Yamamoto, Satoshi Hori, Daina Kashiwazaki, Naoki Akioka, Naoya Kuwayama, and Satoshi Kuroda

OBJECTIVE

This study aimed to assess longitudinal changes in the collateral channels originating from the lenticulostriate artery (LSA), posterior communicating artery (PCoA), and anterior and posterior choroidal arteries (AChA and PChA, respectively) during disease progression and/or aging. The impact of collateral channels on onset type was also examined.

METHODS

This study included 71 involved hemispheres in 41 patients with moyamoya disease. The disease was categorized into 6 stages according to Suzuki’s angiographic staging system. The degree of development of each moyamoya vessel was categorized into 3 grades.

RESULTS

The LSA started to dilate in stage 2, showed the most prominent development in stage 3, and decreased in more advanced stages (p < 0.001). The AChA most notably developed in stage 3 and gradually shrank (p = 0.04). The PCoA started to dilate in stage 3 and showed the most prominent development in stage 4 (p = 0.03). The PChA started to dilate in stage 3 and showed the most prominent development in stages 4 to 5 (p < 0.001). Patient age was negatively related to LSA development (p = 0.01, R = 0.30) and was positively associated with the abnormal dilation and extension of the PCoA (p = 0.02, R = 0.28) and PChA (p < 0.001, R = 0.45). The PCoA, AChA, and PChA more distinctly developed in hemispheres with intracerebral or intraventricular hemorrhage than in hemispheres with ischemic stroke or transient ischemic attack (p < 0.001, p = 0.03, and p = 0.03, respectively).

CONCLUSIONS

This study suggests that the collateral channels through moyamoya vessels longitudinally shift from the anterior to posterior component during disease progression and aging, which may be closely related to the onset of hemorrhagic stroke in adult moyamoya disease.

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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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Jonathan J. Russin, Amir R. Dehdashti, Peter Vajkoczy, Satoshi Kuroda, and Ying Mao

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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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Tomohide Hayashi, Seiji Yamamoto, Takeru Hamashima, Hisashi Mori, Masakiyo Sasahara, and Satoshi Kuroda

OBJECTIVE

This study aimed to clarify the underlying mechanism of pathognomonic angiogenesis between the temporal muscle and neocortex after indirect bypass for moyamoya disease by shedding light on the role of platelet-derived growth factor receptor–α (PDGFRα) in angiogenesis.

METHODS

The gene for PDGFRα was systemically inactivated in adult mice (α-KO mice). The Pdgfra-preserving mice (Flox mice) and α-KO mice were exposed to bilateral common carotid artery stenosis (BCAS) by using microcoils. One week later the animals underwent encephalomyosynangiosis (EMS) on the right side. Cerebral blood flow (CBF) was serially measured using a laser Doppler flowmeter. Histological analysis was performed on the distribution of CD31-positive vessels and collagen deposit at 28 days after BCAS. Reverse transcription polymerase chain reaction (RT-PCR) was performed to assess the expression of collagen mRNA in the skin fibroblasts derived from Flox and α-KO mice.

RESULTS

BCAS significantly reduced CBF up to approximately 70% of the control level at 28 days after the onset. There was no significant difference in CBF between Flox and α-KO mice. EMS significantly enhanced the improvement of CBF on the ipsilateral side of Flox mice, but not α-KO mice. EMS significantly induced the development of CD31-positive vessels in both the neocortex and temporal muscle on the ipsilateral side of Flox mice, but not α-KO mice. Deposition of collagen was distinctly observed between them in Flox mice, but not α-KO mice. Expression of mRNA of collagen type 1 alpha 1 (Col1a1) and collagen type 3 alpha 1 (Col3a1) was significantly downregulated in the skin fibroblasts from α-KO mice.

CONCLUSIONS

This is the first study that denotes the role of a specific growth factor in angiogenesis after EMS for moyamoya disease by inactivating its gene in mice. The findings strongly suggest that PDGFRα signal may play an important role in developing spontaneous angiogenesis between the temporal muscle and neocortex after EMS in moyamoya disease.

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

OBJECTIVE

Choroidal collateral vessels typical of moyamoya disease have received attention as a potential bleeding source. The authors’ previous angiographic cross-sectional analysis suggested a possible association between choroidal collaterals and posterior hemorrhage, indicating a high risk for rebleeding. The present longitudinal analysis is intended to determine whether choroidal collaterals are a predictor of rebleeding in hemorrhagic moyamoya disease.

METHODS

The Japan Adult Moyamoya Trial group designed an ancillary cohort study using 5-year follow-up data on 37 patients included in the nonsurgical arm of the original randomized controlled trial and compared the rebleeding rate of those with and those without choroidal collaterals, represented by the connection between the anterior or posterior choroidal arteries and the medullary arteries. An expert panel determined whether a choroidal collateral was present in each patient through the measurement of baseline angiography studies. The rebleeding rate comparison was adjusted for age, diagnosis of hypertension, and involvement of the posterior cerebral artery.

RESULTS

Choroidal collaterals were present in 21 patients (56.8%). The rebleeding rate was 13.1% per year in the collateral-positive group as compared with 1.3% in the negative group (p = 0.008, log-rank test). The adjusted hazard ratio for rebleeding in the collateral-positive group relative to the negative group remained statistically significant (HR 11.10, 95% CI 1.37–89.91). Radiographic assessment of the collateral-positive group revealed good correspondence between the distribution of collaterals and rebleeding sites.

CONCLUSIONS

Results of this study suggest that choroidal collaterals are a bleeding source with a high risk for hemorrhagic recurrence and a predictor of rebleeding in hemorrhagic moyamoya disease.

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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.

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

OBJECTIVE

Here, the authors aimed to determine whether the presence of cerebral hemodynamic failure predicts subsequent bleeding attacks and how it correlates with the effect of direct bypass surgery in hemorrhagic moyamoya disease.

METHODS

Data from the Japanese Adult Moyamoya (JAM) Trial were used in this study: 158 hemispheres in 79 patients. A newly formed expert panel evaluated the SPECT results submitted at trial enrollment and classified the cortical hemodynamic state of the middle cerebral artery territory of each hemisphere into one of the following three groups: SPECT stage (SS) 0 as normal, SS1 as decreased cerebrovascular reserve (CVR), and SS2 as decreased CVR with decreased baseline blood flow. In the nonsurgical cohort of the JAM Trial, the subsequent hemorrhage rate during the 5-year follow-up was compared between the SS0 (hemodynamic failure negative) and SS1+2 (hemodynamic failure positive) groups. The effect of direct or combined direct/indirect bypass surgery on hemorrhage prevention was examined in each subgroup.

RESULTS

The hemodynamic grade was SS0 in 59 (37.3%) hemispheres, SS1 in 87 (55.1%), and SS2 in 12 (7.6%). In the nonsurgical cohort, subsequent hemorrhage rates in the SS0 and SS1+2 groups were 12 cases per 1000 person-years and 67 cases per 1000 person-years, respectively. Kaplan-Meier analysis revealed that hemorrhagic events were significantly more common in the SS1+2 group (p = 0.019, log-rank test). Cox regression analysis showed that hemodynamic failure was an independent risk factor for subsequent hemorrhage (HR 5.37, 95% CI 1.07–27.02). In the SS1+2 subgroup, bypass surgery significantly suppressed hemorrhagic events during 5 years (p = 0.001, HR 0.16, 95% CI 0.04–0.57), with no significant effect in the SS0 group (p = 0.655, HR 1.56, 95% CI 0.22–11.10). Examination of effect modification revealed that the effect of surgery tended to differ nonsignificantly between these two subgroups (p = 0.056).

CONCLUSIONS

Hemodynamic failure is an independent risk factor for subsequent hemorrhage in hemorrhagic moyamoya disease. Direct bypass surgery showed a significant preventive effect in the hemodynamically impaired hemispheres. Thus, hemodynamic failure, as well as previously proposed factors such as choroidal anastomosis, should be considered for the surgical indication in hemorrhagic moyamoya disease.

Clinical trial registration no.: C000000166 (umin.ac.jp)