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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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Yoshimichi Sato, Toshiki Endo, Tomoo Inoue, Miki Fujimura, and Teiji Tominaga

The authors report on the case of a 65-year-old man suffering progressive gait disturbance and hearing impairment due to superficial siderosis (SS). According to the literature, repeated hemorrhage into the subarachnoid space causes SS; however, the bleeding source remains unknown in half of SS patients. In the presented case, preoperative MRI revealed a fluid-filled intraspinal cavity extending from C2 to T8 with a dural defect at the ventral C7 level. During surgery, the dural defect was seen to connect to the intraspinal cavity filled with xanthochromic fluid. Importantly, endoscopic observation verified that the rupture of fragile bridging veins in the cavity was the definite bleeding source. Postoperative MRI confirmed disappearance of the intraspinal cavity, and the patient’s symptoms gradually improved. The use of endoscopy helped to establish the diagnosis and led to definite treatment. Fragile bridging veins in the fluid-filled interdural layers were novelly verified as a bleeding source in SS. Recognizing this phenomenon is important since it can establish closure of the dural defect as a definite treatment in SS with an intraspinal cavity.

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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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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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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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Takashi Inoue, Hiroaki Shimizu, Miki Fujimura, Atsushi Saito, and Teiji Tominaga

Object

In this paper, the authors' goals were to clarify the characteristics of growing unruptured cerebral aneurysms detected by serial MR angiography and to establish the recommended follow-up interval.

Methods

A total of 1002 patients with 1325 unruptured cerebral aneurysms were retrospectively identified. These patients had undergone follow-up evaluation at least twice. Aneurysm growth was defined as an increase in maximum aneurysm diameter by 1.5 times or the appearance of a bleb.

Results

Aneurysm growth was observed in 18 patients during the period of this study (1.8%/person-year). The annual rupture risk after growth was 18.5%/person-year. The proportion of females among patients with growing aneurysms was significantly larger than those without growing aneurysms (p = 0.0281). The aneurysm wall was reddish, thin, and fragile on intraoperative findings. Frequent follow-up examination is recommended to detect aneurysm growth before rupture.

Conclusions

Despite the relatively short period, the annual rupture risk of growing unruptured cerebral aneurysms detected by MR angiography was not as low as previously reported. Surgical or endovascular treatment can be considered if aneurysm growth is detected during the follow-up period.

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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.

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

OBJECTIVE

Following hemorrhagic stroke in moyamoya disease, de novo intracranial hemorrhage can occur in the previously unaffected nonhemorrhagic hemisphere. In the present analysis the authors intended to determine whether the presence in the nonhemorrhagic hemisphere of choroidal collateral vessels, which have been the focus of attention as a source of bleeding, affects the risk of de novo hemorrhage.

METHODS

The subject of focus of the present cohort study was the nonhemorrhagic hemispheres of adult patients with hemorrhagic moyamoya disease enrolled in the Japan Adult Moyamoya Trial and allocated to the nonsurgical arm. The variable of interest was the presence of choroidal collaterals (also termed choroidal anastomoses), identified with baseline angiography and represented by a connection (anastomosis) between the anterior or posterior choroidal arteries and the medullary arteries. The outcome measure was de novo hemorrhage during the 5-year follow-up period, assessed in all nonhemorrhagic hemispheres. The incidence of de novo hemorrhage in the collateral-positive and -negative groups was compared.

RESULTS

Choroidal collaterals were present in 15 of 36 (41.7%) nonhemorrhagic hemispheres analyzed. The overall annual risk of de novo hemorrhage was 2.0%. Three de novo hemorrhages occurred in the collateral-positive group, whereas no hemorrhage occurred in the collateral-negative group. The annual risk of de novo hemorrhage was significantly higher in the collateral-positive group than in the collateral-negative group (5.8% per year vs 0% per year; p = 0.017). All hemorrhage sites corresponded to the distribution of choroidal collaterals.

CONCLUSIONS

The present preliminary results suggest that the presence of choroidal collaterals affects the risk of de novo hemorrhage in the nonhemorrhagic hemisphere, subject to verification in larger studies. Further studies are needed to determine the optimal treatment strategy for nonhemorrhagic hemispheres and asymptomatic patients.

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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)