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Roberto C. Heros

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Nobutaka Horie, Nobuaki Takahashi, Shoji Furuichi, Katsuharu Mori, Masanari Onizuka, Keisuke Tsutsumi and Shobu Shibata

✓ Three cases of giant fusiform aneurysms in the middle cerebral artery (MCA) presenting with hemorrhages of different origins are reported, and appropriate literature is reviewed to investigate the characteristics of these lesions. Two patients had suffered a subarachnoid hemorrhage and the other had an intramural hemorrhage (dissection). Pathologically, these aneurysms presented with hemorrhages of different origins; classic rupture type (Case 1), dissection type (Case 2), and atherosclerosis-related thrombosis type (Case 3).

Based on surgical and pathological investigations in these three cases and a review of the reported literature, the authors propose that giant fusiform aneurysms in the MCA are characterized by weaknesses in the internal elastic lamina with intimal thickening. Therefore, these lesions have the potential to present with hemorrhage in each of the three types. This finding indicates that there is a strong relationship between the pathological features of giant fusiform aneurysms and their clinical course, and that it is necessary to determine appropriate therapy for giant fusiform aneurysms in the MCA by evaluating cerebral blood flow, even if the lesions are found incidentally.

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Nobutaka Horie, Minoru Morikawa, Shuji Fukuda, Kentaro Hayashi, Kazuhiko Suyama and Izumi Nagata

Blood blister–like aneurysms (BBAs) tend to have a more precipitous clinical course, enlarging rapidly and rebleeding frequently. Nevertheless, they often present a diagnostic challenge because of the characteristic morphological features of a wide neck and shallow outpouching of the medial wall. The authors present the case of a 34-year-old woman who suffered a subarachnoid hemorrhage whose cause could not be determined on the initial imaging with digital subtraction (DS) angiography and CT angiography. Interestingly, MR imaging studies obtained on the 7th day revealed an intramural hematoma on the dorsal wall of the left internal carotid artery, which helped in the diagnosis of BBA on the third DS angiography study obtained on the 8th day, and in the surgical intervention on the 10th day. This case supports the hypothesis that focal dissection contributes to the formation of BBAs. Use of MR imaging in the subacute stage, in addition to DS and CT angiography, might be helpful in the diagnosis of BBAs.

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Nobutaka Horie, Minoru Morikawa, Shuji Fukuda, Kentaro Hayashi, Kazuhiko Suyama and Izumi Nagata

The authors present the case of a 78-year-old man who presented with a subarachnoid hemorrhage due to rupture of an aneurysm at the origin of the persistent primitive olfactory artery (PPOA). Interestingly, the PPOA was originating from the A1 segment of the anterior cerebral artery and coursed anteromedially along the olfactory tract. Moreover, the PPOA in this case had 2 branches: the branch making a hairpin turn and supplying the distal part of the anterior cerebral artery territory (Type 1), and the branch extending to the cribriform plate to supply the nasal cavity (Type 2). To the best of the authors' knowledge, this is a new variant (Type 3) of PPOA associated with a ruptured aneurysm. The clinical implications of this case are discussed in terms of the embryological aspects.

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Progressive perianeurysmal edema induced after endovascular coil embolization

Report of three cases and review of the literature

Nobutaka Horie, Naoki kitagawa, Minoru Morikawa, Keisuke Tsutsumi, Makio Kaminogo and Izumi Nagata

✓The authors report three cases of progressive vasogenic brain edema surrounding a cerebral aneurysm after endovascular coil embolization. In all three cases embolization was incomplete due to the aneurysms' large sizes and wide necks. Follow-up magnetic resonance imaging revealed de novo vasogenic brain edema surrounding the aneurysms 3 to 6 months after the initial treatment. The edema progressed in parallel with regrowth of the aneurysms. All three aneurysms were deep in the brain parenchyma and showed intramural enhancement, suggesting hemorrhage or inflammation. Each patient underwent a second embolization for the aneurysm regrowth, which resulted in improvement of the edema.

Based on the findings in these cases and review of the literature, it is suggested that incomplete occlusion of larger aneurysms that are deep within the brain may lead to a disorganized intraluminal thrombosis, aneurysm pulsing, and intramural hemorrhage or inflammation, all of which are associated with brain edema following aneurysm recanalization and regrowth. It should be kept in mind that incomplete embolization of larger aneurysms may cause such malignant change and that this complication may occur after endovascular treatment.

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Nobutaka Horie, Yoichi Morofuji, Minoru Morikawa, Yohei Tateishi, Tsuyoshi Izumo, Kentaro Hayashi, Akira Tsujino and Izumi Nagata

OBJECT

Recent studies have demonstrated that plaque morphology can contribute to identification of patients at high risk of carotid artery atherosclerosis as well as the degree of stenosis in those with carotid atherosclerosis. Neovascularization of carotid plaques is associated with plaque vulnerability. However, the mechanism of neovascularization in intraplaque hemorrhage (IPH) and its clinical contribution remain undetermined. In this study, the authors aimed to clarify the characteristics of neovessel appearance with a focus on inwardly projecting neovessels, which are reportedly important in plaque advancement.

METHODS

Consecutive patients with moderate to severe carotid atherosclerosis who underwent carotid endarterectomy were prospectively analyzed from 2010 to 2014. The neovessel appearance was categorized into 3 groups based on intraoperative indocyanine green (ICG) videoangiography: early appearance of neovessels from the endothelium (NVe), late appearance of neovessels from the vasa vasorum (NVv), and no appearance of vessels. Each neovessel pattern was evaluated with respect to clinical, radiological, and pathological findings including IPH, neovascularization, hemosiderin spots, and inflammation.

RESULTS

Of 57 patients, 13 exhibited NVe, 33 exhibited NVv, and 11 exhibited no neovessels. Overall, the interobserver and intraobserver reproducibilities of neovessel appearance were substantial for ICG videoangiography (κ = 0.76) and at 7 days postoperatively (κ = 0.76). There were no significant differences in baseline characteristics among the 3 groups, with the exception of a higher percentage of symptomatic presentations in patients with NVe (artery-to-artery embolic infarction in 61.5% and transient ischemic attack in 23.1%). Moreover, patients with NVe exhibited larger infarctions than did those with NVv (9675.0 ± 5601.9 mm3 vs 2306.6 ± 856.9 mm3, respectively; p = 0.04). Pathologically, patients with NVe had more severe IPH (47.2 ± 8.3 mm2 vs 19.8 ± 5.2 mm2, respectively; p < 0.01), hemosiderin spots (0.5 ± 0.2 mm2 vs 0.2 ± 0.1 mm2, respectively; p = 0.04), neovessels (0.4 ± 0.7 mm2 vs 0.1 ± 0.4 mm2, respectively; p = 0.11), and inflammation (1.0 ± 1.1 mm2 vs 0.6 ± 0.9 mm2, respectively; p = 0.26) around the endothelium than did patients with NVv, and all of these parameters were correlated with hyperintensity on time-of-flight MRI. However, the neovessel and inflammation differences were nonsignificant. Interestingly, inflammation was significantly correlated with neovessel formation (r = 0.43, p = 0.0008), hemosiderin spots (r = 0.62, p < 0.0001), and IPH (r = 0.349, p = 0.0097), suggesting that inflammation may be a key factor in plaque vulnerability.

CONCLUSIONS

Communication of inwardly projecting neovessels with the lumen and inflammation synergistically contribute to IPH and symptomatic presentations in patients with carotid stenosis and are more specific than the vasa vasorum. This condition could be a new therapeutic target, and regression of luminal neovessel sprouting and inflammation may help to prevent IPH development and a symptomatic presentation.

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Lesheng Wang and Jincao Chen

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Nobutaka Horie, Shuntaro Sato, Makio Kaminogo, Yoichi Morofuji, Tsuyoshi Izumo, Takeo Anda and Takayuki Matsuo

OBJECTIVE

Aneurysm rebleeding is a major cause of death and morbidity in patients with aneurysmal subarachnoid hemorrhage (SAH). Recognizing the predictors of rebleeding might help to identify patients who will benefit from acute management. This study was performed to investigate the predictors of aneurysm rebleeding and their impact on clinical outcomes in the preoperative, intraoperative, and postoperative periods.

METHODS

The incidence of rebleeding, demographic data, and clinical data from 4933 patients with aneurysmal SAH beginning in the year 2000 were retrospectively analyzed in the Nagasaki SAH Registry Study. The authors performed multiple logistic regression analyses to identify the risk factors contributing to rebleeding and outcome after SAH.

RESULTS

Preoperative rebleeding occurred in 7.2% of patients. Patient age (p = 0.01), multiple aneurysms (p < 0.01), aneurysm size (p < 0.0001), and heart disease (p = 0.03) were significantly associated with preoperative rebleeding. Conversely, intraoperative rebleeding occurred in 11.2% of patients. Aneurysm location (anterior communicating artery [ACoA]), family history (p = 0.02), preoperative rebleeding (p < 0.01), and clipping/coiling (p < 0.0001) were significantly associated with intraoperative rebleeding. Interaction analysis showed that clipping significantly affected intraoperative rebleeding at the ACoA (OR 4.00; 95% CI 1.82–8.80; p < 0.001). Postoperative rebleeding occurred in 2.4% of patients. Coiling/clipping (p < 0.0001) and intraoperative rebleeding (p < 0.01) were significantly associated with postoperative rebleeding. Rebleeding in all time periods examined significantly contributed to the clinical outcome after SAH.

CONCLUSIONS

Aneurysm rebleeding after SAH has specific characteristics in the preoperative, intraoperative, and postoperative periods, and all of these characteristics contribute to the clinical outcome. The ACoA has a higher risk of intraoperative rebleeding, and endovascular coiling could be a good candidate in terms of techniques for preventing intraoperative rebleeding, although complete aneurysm obliteration should be accomplished.

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Nobutaka Horie, Yoichi Morofuji, Yusuke Iki, Eisaku Sadakata, Tadashi Kanamoto, Yohei Tateishi, Tsuyoshi Izumo, Takeo Anda, Minoru Morikawa, Akira Tsujino and Takayuki Matsuo

OBJECTIVE

Regional ischemic vulnerability of the brain reportedly differs between the cortex and basal ganglia and has been poorly assessed in the setting of endovascular mechanical thrombectomy. This study was conducted to determine the fate of an ischemic basal ganglia and its contribution to the clinical outcome after successful endovascular recanalization for acute ischemic stroke with large vessel occlusion involving the lenticulostriate arteries.

METHODS

Clinical and radiological findings were retrospectively analyzed in consecutive patients with acute ischemic stroke characterized by large vessel occlusion involving the lenticulostriate arteries. Mechanical thrombectomy was performed in all patients using a stent retriever. The fate of ischemic basal ganglia based on location (lentiform nucleus, caudate nucleus, and internal capsule) and insular cortex was assessed according to the Alberta Stroke Programme Early CT Score (ASPECTS).

RESULTS

Of 170 patients with large intracranial vessel occlusion who achieved successful endovascular recanalization, defined as a thrombolysis in cerebral infarction grade of ≥ 2B, involvement of the lenticulostriate arteries was seen in 55 patients (internal carotid artery, n = 35; proximal middle cerebral artery, n = 20). Preoperative infarction was detected in the lentiform nucleus (66.7%), internal capsule (11.1%), and caudate nucleus (33.3%), all of which showed secondary advancement despite successful recanalization (85.4%, 27.3%, and 54.5%, respectively; p < 0.05). Lenticulostriate arteries with a lateral proximal and/or medial proximal origin significantly affected the development of mature infarction in the lentiform nucleus. Postoperative hemorrhagic transformation was detected in 25 of 55 patients, mostly in the lentiform nucleus. Involvement of insular ribbon infarction was significantly high in patients with hemorrhagic transformation in the basal ganglia. Age, initial National Institutes of Health Stroke Scale (NIHSS) score, initial ASPECTS, postoperative ASPECTS, postoperative infarction in the insular ribbon, and lesions in the middle cerebral artery area (M1–M6) were significantly different between patients with good and poor modified Rankin Scale scores. Interestingly, no differences were detected in postoperative infarction or hemorrhagic transformation in the basal ganglia. Multivariate analysis showed that only age (p = 0.02, OR 0.88) and the initial NIHSS score (p = 0.01, OR 0.86) independently affected favorable clinical outcomes.

CONCLUSIONS

The basal ganglia are vulnerable and readily develop secondary infarction and hemorrhagic transformation despite successful recanalization. However, this does not have a significant impact on the clinical outcome of acute ischemic stroke with large vessel occlusion involving the lenticulostriate arteries.

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Keisuke Takai, Toshiki Endo, Takao Yasuhara, Toshitaka Seki, Kei Watanabe, Yuki Tanaka, Ryu Kurokawa, Hideaki Kanaya, Fumiaki Honda, Takashi Itabashi, Osamu Ishikawa, Hidetoshi Murata, Takahiro Tanaka, Yusuke Nishimura, Kaoru Eguchi, Toshihiro Takami, Yusuke Watanabe, Takeo Nishida, Masafumi Hiramatsu, Tatsuya Ohtonari, Satoshi Yamaguchi, Takafumi Mitsuhara, Seishi Matsui, Hisaaki Uchikado, Gohsuke Hattori, Nobutaka Horie, Hitoshi Yamahata and Makoto Taniguchi

OBJECTIVE

Spinal arteriovenous shunts are rare vascular lesions and are classified into 4 types (types I–IV). Due to rapid advances in neuroimaging, spinal epidural AVFs (edAVFs), which are similar to type I spinal dural AVFs (dAVFs), have recently been increasingly reported. These 2 entities have several important differences that influence the treatment strategy selected. The purposes of the present study were to compare angiographic and clinical differences between edAVFs and dAVFs and to provide treatment strategies for edAVFs based on a multicenter cohort.

METHODS

A total of 280 consecutive patients with thoracic and lumbosacral spinal dural arteriovenous fistulas (dAVFs) and edAVFs with intradural venous drainage were collected from 19 centers. After angiographic and clinical comparisons, the treatment failure rate by procedure, risk factors for treatment failure, and neurological outcomes were statistically analyzed in edAVF cases.

RESULTS

Final diagnoses after an angiographic review included 199 dAVFs and 81 edAVFs. At individual centers, 29 patients (36%) with edAVFs were misdiagnosed with dAVFs. Spinal edAVFs were commonly fed by multiple feeding arteries (54%) shunted into a single or multiple intradural vein(s) (91% and 9%) through a dilated epidural venous plexus. Preoperative modified Rankin Scale (mRS) and Aminoff-Logue gait and micturition grades were worse in patients with edAVFs than in those with dAVFs. Among the microsurgical (n = 42), endovascular (n = 36), and combined (n = 3) treatment groups of edAVFs, the treatment failure rate was significantly higher in the index endovascular treatment group (7.5%, 31%, and 0%, respectively). Endovascular treatment was found to be associated with significantly higher odds of initial treatment failure (OR 5.72, 95% CI 1.45–22.6). In edAVFs, the independent risk factor for treatment failure after microsurgery was the number of intradural draining veins (OR 17.9, 95% CI 1.56–207), while that for treatment failure after the endovascular treatment was the number of feeders (OR 4.11, 95% CI 1.23–13.8). Postoperatively, mRS score and Aminoff-Logue gait and micturition grades significantly improved in edAVFs with a median follow-up of 31 months.

CONCLUSIONS

Spinal epidural AVFs with intradural venous drainage are a distinct entity and may be classified as type V spinal vascular malformations. Based on the largest multicenter cohort, this study showed that primary microsurgery was superior to endovascular treatment for initial treatment success in patients with spinal edAVFs.