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Masafumi Hiramatsu, Kenji Sugiu, Tomoya Ishiguro, Hiro Kiyosue, Kenichi Sato, Keisuke Takai, Yasunari Niimi and Yuji Matsumaru

OBJECTIVE

The aim of this retrospective multicenter cohort study was to assess the details of the angioarchitecture of arteriovenous fistulas (AVFs) at the craniocervical junction (CCJ) and to determine the associations between the angiographic characteristics and the clinical presentations and outcomes.

METHODS

The authors analyzed angiographic and clinical data for patients with CCJ AVFs from 20 participating centers that are members of the Japanese Society for Neuroendovascular Therapy (JSNET). Angiographic findings (feeding artery, location of AV shunt, draining vein) and patient data (age, sex, presentation, treatment modality, outcome) were tabulated and stratified based on the angiographic types of the lesions, as diagnosed by a member of the CCJ AVF study group, which consisted of a panel of 6 neurointerventionalists and 1 spine neurosurgeon.

RESULTS

The study included 54 patients (median age 65 years, interquartile range 61–75 years) with a total of 59 lesions. Five angiographic types were found among the 59 lesions: Type 1, dural AVF (22 [37%] of 59); Type 2, radicular AVF (17 [29%] of 59); Type 3, epidural AVF (EDAVF) with pial feeders (8 [14%] of 59); Type 4, EDAVF (6 [10%] of 59); and Type 5, perimedullary AVF (6 [10%] of 59). In almost all lesions (98%), AV shunts were fed by radiculomeningeal arteries from the vertebral artery that drained into intradural or epidural veins through AV shunts on the dura mater, on the spinal nerves, in the epidural space, or on the spinal cord. In more than half of the lesions (63%), the AV shunts were also fed by a spinal pial artery from the anterior spinal artery (ASA) and/or the lateral spinal artery. The data also showed that the angiographic characteristics associated with hemorrhagic presentations—the most common presentation of the lesions (73%)—were the inclusion of the ASA as a feeder, the presence of aneurysmal dilatation on the feeder, and CCJ AVF Type 2 (radicular AVF). Treatment outcomes differed among the angiographic types of the lesions.

CONCLUSIONS

Craniocervical junction AVFs commonly present with hemorrhage and are frequently fed by both radiculomeningeal and spinal pial arteries. The AV shunt develops along the C-1 or C-2 nerve roots and can be located on the spinal cord, on the spinal nerves, and/or on the inner or outer surface of the dura mater.

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Tomohisa Shimizu, Tomohito Hishikawa, Shingo Nishihiro, Yukei Shinji, Yuji Takasugi, Jun Haruma, Masafumi Hiramatsu, Hirokazu Kawase, Sachiko Sato, Ryoichi Mizoue, Yoshimasa Takeda, Kenji Sugiu, Hiroshi Morimatsu and Isao Date

OBJECTIVE

Although cortical spreading depolarization (CSD) has been observed during the early phase of subarachnoid hemorrhage (SAH) in clinical settings, the pathogenicity of CSD is unclear. The aim of this study is to elucidate the effects of loss of membrane potential on neuronal damage during the acute phase of SAH.

METHODS

Twenty-four rats were subjected to SAH by the perforation method. The propagation of depolarization in the brain cortex was examined by using electrodes to monitor 2 direct-current (DC) potentials and obtaining NADH (reduced nicotinamide adenine dinucleotide) fluorescence images while exposing the parietal-temporal cortex to ultraviolet light. Cerebral blood flow (CBF) was monitored in the vicinity of the lateral electrode. Twenty-four hours after onset of SAH, histological damage was evaluated at the DC potential recording sites.

RESULTS

Changes in DC potentials (n = 48 in total) were sorted into 3 types according to the appearance of ischemic depolarization in the entire hemisphere following induction of SAH. In Type 1 changes (n = 21), ischemic depolarization was not observed during a 1-hour observation period. In Type 2 changes (n = 13), the DC potential demonstrated ischemic depolarization on initiation of SAH and recovered 80% from the maximal DC deflection during a 1-hour observation period (33.3 ± 15.8 minutes). In Type 3 changes (n = 14), the DC potential displayed ischemic depolarization and did not recover during a 1-hour observation period. Histological evaluations at DC potential recording sites showed intact tissue at all sites in the Type 1 group, whereas in the Type 2 and Type 3 groups neuronal damage of varying severity was observed depending on the duration of ischemic depolarization. The duration of depolarization that causes injury to 50% of neurons (P50) was estimated to be 22.4 minutes (95% confidence intervals 17.0–30.3 minutes). CSD was observed in 3 rats at 6 sites in the Type 1 group 5.1 ± 2.2 minutes after initiation of SAH. On NADH fluorescence images CSD was initially observed in the anterior cortex; it propagated through the entire hemisphere in the direction of the occipital cortex at a rate of 3 mm/minute, with repolarization in 2.3 ± 1.2 minutes. DC potential recording sites that had undergone CSD were found to have intact tissue 24 hours later. Compared with depolarization that caused 50% neuronal damage, the duration of CSD was too short to cause histological damage.

CONCLUSIONS

CSD was successfully visualized using NADH fluorescence. It propagated from the anterior to the posterior cortex along with an increase in CBF. The duration of depolarization in CSD (2.3 ± 1.2 minutes) was far shorter than that causing 50% neuronal damage (22.4 minutes) and was not associated with histological damage in the current experimental setting.

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Masafumi Hiramatsu, Tomohito Hishikawa, Koji Tokunaga, Hiroyasu Kidoya, Shingo Nishihiro, Jun Haruma, Tomohisa Shimizu, Yuji Takasugi, Yukei Shinji, Kenji Sugiu, Nobuyuki Takakura and Isao Date

OBJECTIVE

The aim of this study was to evaluate whether combined gene therapy with vascular endothelial growth factor (VEGF) plus apelin during indirect vasoreconstructive surgery enhances brain angiogenesis in a chronic cerebral hypoperfusion model in rats.

METHODS

A chronic cerebral hypoperfusion model induced by the permanent ligation of bilateral common carotid arteries (CCAs; a procedure herein referred to as “CCA occlusion” [CCAO]) in rats was employed in this study. Seven days after the CCAO procedure, the authors performed encephalo-myo-synangiosis (EMS) and injected plasmid(s) into each rat's temporal muscle. Rats were divided into 4 groups based on which plasmid was received (i.e., LacZ group, VEGF group, apelin group, and VEGF+apelin group). Protein levels in the cortex and attached muscle were assessed with enzyme-linked immunosorbent assay (ELISA) on Day 7 after EMS, while immunofluorescent analysis of cortical vessels was performed on Day 14 after EMS.

RESULTS

The total number of blood vessels in the cortex on Day 14 after EMS was significantly larger in the VEGF group and the VEGF+apelin group than in the LacZ group (p < 0.05, respectively). Larger vessels appeared in the VEGF+apelin group than in the other groups (p < 0.05, respectively). Apelin protein on Day 7 after EMS was not detected in the cortex for any of the groups. In the attached muscle, apelin protein was detected only in the apelin group and the VEGF+apelin group. Immunofluorescent analysis revealed that apelin and its receptor, APJ, were expressed on endothelial cells (ECs) 7 days after the CCAO.

CONCLUSIONS

Combined gene therapy (VEGF plus apelin) during EMS in a chronic cerebral hypoperfusion model can enhance angiogenesis in rats. This treatment has the potential to be a feasible option in a clinical setting for patients with moyamoya disease.

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Masafumi Hiramatsu, Kenji Sugiu, Tomohito Hishikawa, Shingo Nishihiro, Naoya Kidani, Yu Takahashi, Satoshi Murai, Isao Date, Naoya Kuwayama, Tetsu Satow, Koji Iihara and Nobuyuki Sakai

OBJECTIVE

Embolization is the most common treatment for dural arteriovenous fistulas (dAVFs). A retrospective, multicenter observational study was conducted in Japan to clarify the nature, frequency, and risk factors for complications of dAVF embolization.

METHODS

Patient data were derived from the Japanese Registry of Neuroendovascular Therapy 3 (JR-NET3). A total of 40,169 procedures were registered in JR-NET3, including 2121 procedures (5.28%) in which dAVFs were treated with embolization. After data extraction, the authors analyzed complication details and risk factors in 1940 procedures performed in 1458 patients with cranial dAVFs treated with successful or attempted embolization.

RESULTS

Transarterial embolization (TAE) alone was performed in 858 cases (44%), and transvenous embolization (TVE) alone was performed in 910 cases (47%). Both TAE and TVE were performed in one session in 172 cases (9%). Complications occurred in 149 cases (7.7%). Thirty-day morbidity and mortality occurred in 55 cases (2.8%) and 16 cases (0.8%), respectively. Non–sinus-type locations, radical embolization as the strategy, procedure done at a hospital that performed dAVF embolization in fewer than 10 cases during the study period, and emergency procedures were independent risk factors for overall complications.

CONCLUSIONS

Complication rates of dAVF embolization in Japan were acceptable. For better results, the risk factors identified in this study should be considered in treatment decisions.

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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.