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  • Author or Editor: Kuniyasu Niizuma x
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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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Sherif Rashad, Shin-ichiro Sugiyama, Kuniyasu Niizuma, Kenichi Sato, Hidenori Endo, Shunsuke Omodaka, Yasushi Matsumoto, Miki Fujimura and Teiji Tominaga

OBJECTIVE

Risk factors for aneurysm rupture have been extensively studied, with several factors showing significant correlations with rupture status. Several studies have shown that aneurysm shape and hemodynamics change after rupture. In the present study the authors investigated a static factor, the bifurcation angle, which does not change after rupture, to understand its effect on aneurysm rupture risk and hemodynamics.

METHODS

A hospital database was retrospectively reviewed to identify patients with cerebral aneurysms treated surgically or endovascularly in the period between 2008 and 2015. After acquiring 3D rotational angiographic data, 3D stereolithography models were created and computational fluid dynamic analysis was performed using commercially available software. Patient data (age and sex), morphometric factors (aneurysm volume and maximum height, aspect ratio, bifurcation angle, bottleneck ratio, and neck/parent artery ratio), and hemodynamic factors (inflow coefficient and wall shear stress) were statistically compared between ruptured and unruptured groups.

RESULTS

Seventy-one basilar tip aneurysms were included in this study, 22 ruptured and 49 unruptured. Univariate analysis showed aspect ratio, bifurcation angle, bottleneck ratio, and inflow coefficient were significantly correlated with a ruptured status. Logistic regression analysis showed that aspect ratio and bifurcation angle were significant predictors of a ruptured status. Bifurcation angle was inversely correlated with inflow coefficient (p < 0.0005), which in turn correlated directly with mean (p = 0.028) and maximum (p = 0.014) wall shear stress (WSS) using Pearson's correlation coefficient, whereas aspect ratio was inversely correlated with mean (0.012) and minimum (p = 0.018) WSS.

CONCLUSIONS

Bifurcation angle and aspect ratio are independent predictors for aneurysm rupture. Bifurcation angle, which does not change after rupture, is correlated with hemodynamic factors including inflow coefficient and WSS, as well as rupture status. Aneurysms with the hands-up bifurcation configuration are more prone to rupture than aneurysms with other bifurcation configurations.

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Alaa Elkordy, Hidenori Endo, Kenichi Sato, Yasushi Matsumoto, Ryushi Kondo, Kuniyasu Niizuma, Toshiki Endo, Miki Fujimura and Teiji Tominaga

OBJECTIVE

The anterior and posterior choroidal arteries are often recruited to supply arteriovenous malformations (AVMs) involving important paraventricular structures, such as the basal ganglia, internal capsule, optic radiation, lateral geniculate body, and medial temporal lobe. Endovascular embolization through these arteries is theoretically dangerous because they supply eloquent territories, are of small caliber, and lack collaterals. This study aimed to investigate the safety and efficacy of embolization through these arteries.

METHODS

This study retrospectively reviewed 13 patients with cerebral AVMs who underwent endovascular embolization through the choroidal arteries between 2006 and 2014. Embolization was performed as a palliative procedure before open surgery or Gamma Knife radiosurgery. Computed tomography and MRI were performed the day after embolization to assess any surgical complications. The incidence and type of complications and their association with clinical outcomes were analyzed.

RESULTS

Decreased blood flow was achieved in all patients after embolization. Postoperative CT detected no hemorrhagic complications. In contrast, postoperative MRI detected that 4 of the 13 patients (30.7%) developed infarctions: 3 patients after embolization through the anterior choroidal artery, and 1 patient after embolization through the lateral posterior choroidal artery. Two of the 4 patients in whom embolization was from the cisternal segment of the anterior choroidal artery (proximal to the plexal point) developed symptomatic infarction of the posterior limb of the internal capsule, 1 of whom developed morbidity (7.7%). The treatment-related mortality rate was 0%. Additional treatment was performed in 12 patients: open surgery in 9 and Gamma Knife radiosurgery in 3 patients. Complete obliteration was confirmed by angiography at the last follow-up in 10 patients. Recurrent bleeding from the AVMs did not occur in any of the cases during the follow-up period.

CONCLUSIONS

Ischemic complications are possible following the embolization of cerebral AVMs through the choroidal artery, even with modern neurointerventional devices and techniques. Although further study is needed, embolization through the choroidal artery may be an appropriate treatment option when the risk of surgery or radiosurgery is considered to outweigh the risk of embolization.

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Kenichi Sato, Toshiki Endo, Kuniyasu Niizuma, Miki Fujimura, Takashi Inoue, Hiroaki Shimizu and Teiji Tominaga

Object

Dural arteriovenous fistulas (DAVFs) and perimedullary arteriovenous fistulas (PAVFs) are uncommonly associated in the craniocervical junction. The purpose of this study was to describe the clinical and angiographic characteristics of such concurrent lesions.

Methods

Authors reviewed 9 cases with a coexistent DAVF and PAVF at the craniocervical junction. Clinical presentation, angiographic characteristics, intraoperative findings, and treatment outcomes were assessed.

Results

All patients (male/female ratio 5:4; mean age 66.3 years) presented with subarachnoid hemorrhage. Angiography revealed that 8 patients had both a DAVF and PAVF on the same side, whereas 1 patient had 3 arteriovenous fistulas, 1 DAVF, and 1 PAVF on the right side and 1 DAVF on the left side. All of the fistulas shared dilated perimedullary veins (anterior spinal vein, 7 cases; anterolateral spinal vein, 2 cases) as a main drainage route. The shared drainage route was rostrally directed in 8 of 9 cases. Eight patients exhibited an arterial aneurysm on the distal side of the feeding arteries to the PAVF, and the aneurysm in each case was intraoperatively confirmed as a bleeding point. One patient had ruptured venous ectasia at the perimedullary fistulous point. All patients underwent direct surgery via a posterolateral approach. No recurrence was observed in the 4 patients who underwent postoperative angiography, and no rebleeding event was recorded among any of the 9 patients during the follow-up period (mean 38.4 months).

Conclusions

The similarity of the angioarchitecture and the close anatomical relationship between DAVF and PAVF at the craniocervical junction suggested that these lesions are pathogenetically linked. The pathophysiological mechanism and anatomical features of these lesions represent a unique vascular anomaly that should be recognized angiographically to plan a therapeutic strategy.

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Miki Fujimura, Naoto Kimura, Masayuki Ezura, Kuniyasu Niizuma, Hiroshi Uenohara and Teiji Tominaga

The development of a de novo arteriovenous malformation (AVM) in patients with moyamoya disease is extremely rare. A 14-year-old girl developed an AVM in the right occipital lobe during the 4-year postoperative period following successful bilateral revascularization surgeries. She suffered a transient ischemic attack with hemodynamic compromise of the bilateral hemispheres at the age of 10 years. Results of an initial examination by 1.5-T MRI and MR angiography satisfied the diagnostic criteria of moyamoya disease but failed to detect any vascular malformation. Bilateral direct and indirect revascularization surgeries in the anterior circulation relieved her symptoms, and she underwent MRI and MR angiography follow-up every year after surgery. Serial T2-weighted MRI revealed the gradual appearance of flow voids in the right occipital lobe during the follow-up period. Magnetic resonance angiography ultimately indicated the development of an AVM 4 years after these surgeries when catheter angiography confirmed the diagnosis of an AVM in the right occipital lobe. The AVM remained asymptomatic, and the patient remained free of cerebrovascular events during the time she was observed by the authors. Acquired AVM in moyamoya disease is extremely rare, with only 3 pediatric cases including the present case being reported in the literature. The development of a de novo AVM in a postoperative patient with moyamoya disease appears to be unique, and this case may provide insight into the dynamic pathology of AVMs.

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Shunsuke Omodaka, Hidenori Endo, Kuniyasu Niizuma, Miki Fujimura, Takashi Inoue, Toshiki Endo, Kenichi Sato, Shin-ichiro Sugiyama and Teiji Tominaga

OBJECTIVE

Recent MR vessel wall imaging studies have indicated intracranial aneurysms in the active state could show circumferential enhancement along the aneurysm wall (CEAW). While ruptured aneurysms frequently show CEAW, CEAW in unruptured aneurysms at the evolving state (i.e., growing or symptomatic) has not been studied in detail. The authors quantitatively assessed the degree of CEAW in evolving unruptured aneurysms by comparing it separately to that in stable unruptured and ruptured aneurysms.

METHODS

A quantitative analysis of CEAW was performed in 26 consecutive evolving aneurysms using MR vessel wall imaging. Three-dimensional T1-weighted fast spin echo sequences were obtained before and after contrast media injection, and the contrast ratio of the aneurysm wall against the pituitary stalk (CRstalk) was calculated as the indicator of CEAW. Aneurysm characteristics of evolving aneurysms were compared with those of 69 stable unruptured and 67 ruptured aneurysms.

RESULTS

The CRstalk values in evolving aneurysms were significantly higher than those in stable aneurysms (0.54 vs 0.34, p < 0.0001), and lower than those in ruptured aneurysms (0.54 vs 0.83, p < 0.0002). In multivariable analysis, CRstalk remained significant when comparing evolving with stable aneurysms (odds ratio [OR] 12.23, 95% confidence interval [CI] 3.53–42.41), and with ruptured aneurysms (OR 0.083, 95% CI 0.022–0.310).

CONCLUSIONS

The CEAW in evolving aneurysms was higher than those in stable aneurysms, and lower than those in ruptured aneurysms. The degree of CEAW may indicate the process leading to rupture of intracranial aneurysms, which can be useful additional information to determine an indication for surgical treatment of unruptured aneurysms.

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Ahmed Mansour, Kuniyasu Niizuma, Sherif Rashad, Akira Sumiyoshi, Rie Ryoke, Hidenori Endo, Toshiki Endo, Kenichi Sato, Ryuta Kawashima and Teiji Tominaga

OBJECTIVE

The cognitive deficits of vascular dementia and the vasoocclusive state of moyamoya disease have often been mimicked with bilateral stenosis/occlusion of the common carotid artery (CCA) or internal carotid artery. However, the cerebral blood flow (CBF) declines abruptly in these models after ligation of the CCA, which differs from “chronic” cerebral hypoperfusion. While some modified but time-consuming techniques have used staged occlusion of both CCAs, others used microcoils for CCA stenosis, producing an adverse effect on the arterial endothelium. Thus, the authors developed a new chronic cerebral hypoperfusion (CCH) model with cognitive impairment and a low mortality rate in rats.

METHODS

Male Sprague-Dawley rats were subjected to unilateral CCA occlusion and contralateral induction of CCA stenosis (modified CCA occlusion [mCCAO]) or a sham operation. Cortical regional CBF (rCBF) was measured using laser speckle flowmetry. Cognitive function was assessed using a Barnes circular maze (BCM). MRI studies were performed 4 weeks after the operation to evaluate cervical and intracranial arteries and parenchymal injury. Behavioral and histological studies were performed at 4 and 8 weeks after surgery.

RESULTS

The mCCAO group revealed a gradual CBF reduction with a low mortality rate (2.3%). White matter degeneration was evident in the corpus callosum and corpus striatum. Although the cellular density declined in the hippocampus, MRI revealed no cerebral infarctions after mCCAO. Immunohistochemistry revealed upregulated inflammatory cells and angiogenesis in the hippocampus and cerebral cortex. Results of the BCM assessment indicated significant impairment in spatial learning and memory in the mCCAO group. Although some resolution of white matter injury was observed at 8 weeks, the animals still had cognitive impairment.

CONCLUSIONS

The mCCAO is a straightforward method of producing a CCH model in rats. It is associated with a low mortality rate and could potentially be used to investigate vascular disease, moyamoya disease, and CCH. This model was verified for an extended time point of 8 weeks after surgery.