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Toshiaki Hayashi, Reizo Shirane, Miki Fujimura and Teiji Tominaga

Object

Young patients with moyamoya disease frequently exhibit extensive cerebral infarction at the time of initial presentation, and even in the early postoperative period. To investigate clinical characteristics in the early postoperative period, the authors prospectively analyzed findings of MR imaging, MR angiography, and SPECT before and after surgery. The authors focused in particular on how postoperative neurological deterioration occurred.

Methods

Between August 2005 and June 2009, 22 patients younger than 18 years of age with moyamoya disease were treated at Miyagi Children's Hospital. The mean patient age (± SD) was 8.58 ± 4.55 years (range 2–17 years). Superficial temporal artery–middle cerebral artery bypass and indirect bypass of encephalosynangiosis between the brain surface and the temporal muscle, galea, and dura mater were performed in 35 hemispheres. Magnetic resonance imaging and MR angiography were performed before surgery, at 7 days postoperatively, and 3–6 months after surgery. A 123I-isopropyl iodoamphetamine SPECT scan was also obtained pre- and postoperatively.

Results

During the postoperative period, neurological deterioration was observed after 15 operations (10 cases of motor paresis, 1 of aphasia, and 4 of sensory disturbance) in 13 patients. All symptoms had resolved by the time of discharge, except in 2 patients who suffered cerebral infarction. All patients exhibited disappearance (94.3%) or reduction (5.7%) of transient ischemic attacks (TIAs) during the follow-up period. Perioperative studies revealed 2 different types of radiological findings, focal uptake decrease on SPECT indicative of cerebral ischemia due to dynamic change in cerebral hemodynamics caused by bypass flow, the so-called watershed shift, and perioperative edematous lesions on MR imaging due to cerebral hyperperfusion. The frequent occurrence of preoperative TIAs was significantly associated with watershed shift, whereas preoperative MR imaging findings and preoperative SPECT findings were not. Age at operation was the only factor significantly associated with postoperative hyperperfusion.

Conclusions

In young patients, moyamoya disease exhibits rapid progression, resulting in poor clinical outcome. The risk of postoperative neurological deterioration in very young moyamoya patients with frequent TIAs should be noted. The findings in this study showed that direct bypass is not completely safe in patients with moyamoya disease because it causes dynamic change in postoperative cerebral hemodynamics.

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Yasuo Nishijima, Kuniyasu Niizuma, Miki Fujimura, Yosuke Akamatsu, Hiroaki Shimizu and Teiji Tominaga

OBJECT

Numerous studies have attempted to reveal the pathophysiology of ischemic neuronal injury using a representative transient global cerebral ischemia (tGCI) model in rodents; however, most of them have used gerbil or rat models. Recent advances in transgene and gene-knockout technology have enabled the precise molecular mechanisms of ischemic brain injury to be investigated. Because the predominant species for the study of genetic mutations is the mouse, a representative mouse model of tGCI is of particular importance. However, simple mouse models of tGCI are less reproducible; therefore, a more complex process or longer duration of ischemia, which causes a high mortality rate, has been used in previous tGCI models in mice. In this study, the authors aimed to overcome these problems and attempted to produce consistent unilateral delayed hippocampal CA1 neuronal death in mice.

METHODS

C57BL/6 mice were subjected to short-term unilateral cerebral ischemia using a 4-mm silicone-coated intraluminal suture to obstruct the origin of the posterior cerebral artery (PCA), and regional cerebral blood flow (rCBF) of the PCA territory was measured using laser speckle flowmetry. The mice were randomly assigned to groups of different ischemic durations and histologically evaluated at different time points after ischemia. The survival rate and neurological score of the group that experienced 15 minutes of ischemia were also evaluated.

RESULTS

Consistent neuronal death was observed in the medial CA1 subregion 4 days after 15 minutes of ischemia in the group of mice with a reduction in rCBF of < 65% in the PCA territory during ischemia. Morphologically degenerated cells were mostly positive for terminal deoxynucleotidyl transferase–mediated deoxyuridine triphosphate nick-end labeling and cleaved caspase 3 staining 4 days after ischemia. The survival rates of the mice 24 hours (n = 24), 4 days (n = 15), and 7 days (n = 7) after being subjected to 15 minutes of ischemia were 95.8%, 100%, and 100%, respectively, and the mice had slight motor deficits.

CONCLUSIONS

The authors established a model of delayed unilateral hippocampal neuronal death in C57BL/6 mice by inducing ischemia in the PCA territory using an intraluminal suture method and established inclusion criteria for PCAterritory rCBF monitored by laser speckle flowmetry. This model may be useful for investigating the precise molecular mechanisms of ischemic brain injury.

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Kuniyasu Niizuma, Miki Fujimura, Toshiyuki Takahashi, Akira Takahashi, Mika Watanabe and Teiji Tominaga

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Yosuke Akamatsu, Hiroaki Shimizu, Atsushi Saito, Miki Fujimura and Teiji Tominaga

Object

In the intraluminal suture model of middle cerebral artery occlusion (MCAO) in the mouse, disturbance of blood flow from the internal carotid artery to the posterior cerebral artery (PCA) may affect the size of the infarction. In this study, PCA involvement in the model was investigated and modified for consistent MCAO without involving the PCA territory.

Methods

Thirty-seven C57Bl/6 mice were randomly divided into 4 groups according to the length of coating over the tip of the suture (1, 2, 3, or 4 mm) and subjected to transient MCAO for 2 hours. Real-time topographical cerebral blood flow was monitored over both hemispheres by laser speckle flowmetry. After 24 hours of reperfusion, the infarct territories and volumes were evaluated.

Results

The 1- and 2-mm coating groups showed all lesions in the MCA territory. In the 3- and 4-mm coating groups, 62.5% and 75% of mice, respectively, showed lesions in both the MCA and the PCA territories and other lesions in the MCA territory. Mice in the 1- and 2-mm coating groups had significantly smaller infarct volumes than the 3- and 4-mm groups. Laser speckle flowmetry was useful to distinguish whether the PCA territory would undergo infarction.

Conclusions

Small changes in the coating length of the intraluminal suture may be critical, and 1–2 mm of coating appeared to be optimal to produce consistent MCAO without involving the PCA territory. Laser speckle flowmetry could predict the territory of infarction and improve the consistency of the infarct size.

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Tomohiro Kawaguchi, Atsuhiro Nakagawa, Toshiki Endo, Miki Fujimura, Yukihiko Sonoda and Teiji Tominaga

OBJECT

Neuroendoscopic surgery allows minimally invasive surgery, but lacks effective methods to control bleeding. Water jet dissection with continuous flow has been used in liver and kidney surgery since the 1980s, and is effective for tissue manipulation with vascular preservation, but involves some potential risks, such as elevation of intracranial pressure during application in the ventricles. The authors previously reported the efficacy of the actuator-driven pulsed water jet device (ADPJ) to dissect soft tissue with vascular preservation in microscopic neurosurgery. This feasibility study investigated the use of the ADPJ to reduce the amount of water usage, leading to more safety with sustained efficacy.

METHODS

A small-diameter pulsed water jet device was developed for use with the flexible neuroendoscope. To identify the optimal conditions for the water jet, the flow rate, water pressure, and distance between the nozzle and target were analyzed in an in vitro study by using a gelatin brain phantom. A ventricle model was used to monitor the internal pressure and temperature. For ex vivo experiments the porcine brain was harvested and ventricle walls were exposed, and subsequently immersed into physiological saline. For in vivo experiments the cortex was microsurgically resected to make the small cortico-ventricle window, and then the endoscope was introduced to dissect ventricle walls.

RESULTS

In the in vitro experiments, water pressure was approximately 6.5 bar at 0.5 mm from the ADPJ nozzle and was maintained at 1 mm, but dropped rapidly toward 50% at 2 mm, and became 10% at 3.5 mm. The ADPJ required less water to achieve the same dissection depth compared with the continuous-flow water jet. With the ventricle model, the internal pressure and temperature were well controlled at the baseline, with open water drainage. These results indicated that the ADPJ can be safely applied within the ventricles. The ADPJ was introduced into a flexible endoscope and the ventricle walls were dissected in both the ex vivo and in vivo conditions. The ventricle wall was dissected without obscuring the view, and the vascular structures were anatomically preserved under direct application. Histological examination revealed that both the vessels on the ventricle wall and the fine vessels in the parenchyma were preserved.

CONCLUSIONS

The ADPJ can safely and effectively dissect the ventricle wall, with vascular preservation in immersed conditions. To achieve the optimal result of tissue dissection with minimal surgical risk, the ADPJ is a potential device for neuroendoscopic surgery of the ventricles.

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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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Hidenori Endo, Shin-ichiro Sugiyama, Toshiki Endo, Miki Fujimura, Hiroaki Shimizu and Teiji Tominaga

The most frequently used option to reconstruct the anterior cerebral artery (ACA) is an ACA-ACA side-to-side anastomosis. The long-term outcome and complications of this technique are unclear. The authors report a case of a de novo aneurysm arising at the site of A3-A3 anastomosis. A 53-year-old woman underwent A3-A3 side-to-side anastomosis for the treatment of a ruptured right A2 dissecting aneurysm. At 44 months after surgery, a de novo aneurysm developed at the site of anastomosis. The aneurysm developed in the front wall of the anastomosis site, and projected to the anterosuperior direction. A computational fluid dynamics (CFD) study showed the localized region with high wall shear stress coincident with the pulsation in the front wall of the anastomosis site, where the aneurysm developed. A Y-shaped superficial temporal artery (STA) interposition graft was used successfully to reconstruct both ACAs, and then the aneurysm was trapped. To the authors’ knowledge, this is the first case of a de novo aneurysm that developed at the site of an ACA-ACA side-to-side anastomosis. A CFD study showed that hemodynamic stress might be an underlying cause of the aneurysm formation. A Y-shaped STA interposition graft is a useful option to treat this aneurysm. Long-term follow-up is necessary to detect this rare complication after ACA-ACA anastomosis.

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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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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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Atsuhiro Nakagawa, Miki Fujimura, Tatsuhiko Arafune, Ichiro Sakuma and Teiji Tominaga

Object

Surgical revascularization for moyamoya disease prevents cerebral ischemic attacks by improving cerebral blood flow (CBF). Symptomatic cerebral hyperperfusion is a potential complication of this procedure, but its treatment is contradictory to that for ischemia. Because intraoperative techniques to detect hyperperfusion are still lacking, the authors performed intraoperative infrared monitoring in moyamoya disease using a novel infrared imaging system.

Methods

During superficial temporal artery–middle cerebral artery anastomosis in 25 patients (26 hemispheres) with moyamoya disease, the authors monitored the brain surface temperature intraoperatively with the IRIS-V infrared imaging system. The average gradation value change (indicating temperature change) was calculated using commercial software. Magnetic resonance imaging, MR angiography, and N-isopropyl-p-[123I]iodoamphetamine SPECT studies were performed routinely before and within 10 days after surgery.

Results

Patency of bypass, detailed local hemodynamics, and changes in cortical surface temperature around the anastomosis site were well recognized by the IRIS-V infrared imaging system in all cases. In the present study, 10 patients suffered transient neurological symptoms accompanied by an increase in CBF around the anastomosis site, recognized as symptomatic hyperperfusion. The increase in temperature was significantly higher in these patients. Intensive blood pressure control was undertaken, and free-radical scavengers were administered. No patient in the present study suffered a permanent neurological deficit.

Conclusions

Although the present method does not directly monitor surface CBF, temperature rise around the anastomosis site during surgery might be an indicator of postoperative hyperperfusion. Prospective evaluation with a larger number of patients is necessary to validate this technique.