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Cerebral hemodynamics and metabolism in patients with cerebral arteriovenous malformations: an evaluation using positron emission tomography scanning

Toru Iwama, Kohei Hayashida, Jun C. Takahashi, Izumi Nagata, and Nobuo Hashimoto

Object. The purpose of this study was to evaluate cerebral hemodynamic and metabolic features in patients with arteriovenous malformations (AVMs) by using positron emission tomography (PET) scanning.

Methods. Twenty-four patients with supratentorial cerebral AVMs participated in PET studies in which 15O inhalation steady-state methods were used. The authors recorded the values of regional cerebral blood flow (rCBF), regional cerebral blood volume (rCBV), the regional oxygen extraction fraction (rOEF), and the regional cerebral metabolic rate of O2 (rCMRO2) at three designated regions of interest (ROIs) in each patient. These ROIs included perilesional (ROI-p), ipsilateral remote (ROI-i), and contralateral symmetrical (ROI-c) brain regions. To identify the factors that exert a direct effect on the hemodynamics of brains affected by AVM, we also separated the lesions according to their size and flow type shown on angiograms, and grouped the patients according to the presence or absence of progressive neurological deficits. We then compared the PET parameters at different ROIs in individual patients and evaluated the mean values obtained for all 24 patients according to AVM flow type and size, and the presence or absence of progressive neurological deficits.

Conclusions. Overall, mean rCBV and rOEF values were significantly higher in ROI-p than in ROI-c (p = 0.00046 and p = 0.015, respectively). No significant differences were seen between the ROI-i and ROI-c with respect to rCBF, rCBV, and rOEF. Mean rCMRO2 values were similar in the three ROIs; however, the mean rCBF was significantly lower in the ROI-p than in the ROI-c in patients with high-flow AVMs (p = 0.019), large AVMs (p = 0.017), and progressive neurological deficits (p = 0.021). Furthermore, the mean rOEF values were significantly higher in the ROI-p than in the ROI-c in patients with high-flow AVMs (p = 0.005), large AVMs (p = 0.019), and progressive neurological deficits (p = 0.017). The PET studies revealed hemodynamic impairment characterized by decreased rCBF and increased rOEF and rCBV values in the ROI-p of patients with large, high-flow AVMs regardless of whether they exhibited progressive neurological deficits.

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Endovascular Flow Splitting

Mauro Bergui and Gianni B. Bradac

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Dissecting aneurysms of the vertebral artery: a management strategy

Koji Iihara, Nobuyuki Sakai, Kenichi Murao, Hideki Sakai, Toshio Higashi, Shuji Kogure, Jun C. Takahashi, and Izumi Nagata

Object. The authors present a retrospective analysis of their experience in the treatment of vertebral artery (VA) dissecting aneurysms and propose a management strategy for such aneurysms, with special emphasis on the most formidable VA dissecting aneurysms, which involve the origin of the posterior inferior cerebellar artery (PICA).

Methods. Since 1998, 18 patients with VA dissecting aneurysms, 11 of whom presented with subarachnoid hemorrhage (SAH), have been treated by endovascular surgery at the authors' institution. Obliteration of the entire segment of the dissected site with coils (internal trapping) was performed for aneurysms without involvement of the origin of the PICA (12 cases; among these the treatment-related morbidity rate was 16.7%). The treatment strategy applied to PICA-involved VA dissecting aneurysms presenting with SAH (three cases) included proximal occlusion of the parent artery followed by internal trapping of the aneurysm (one case), proximal occlusion of the parent artery followed by occipital artery (OA)—PICA bypass (one case), and two-staged internal trapping of the aneurysm involving double PICAs (one case). For PICA-involved VA dissecting aneurysms that were not associated with SAH at presentation (three cases), OA—PICA bypass was performed and followed by internal trapping of the aneurysm (two cases). In the remaining case in which a fetal-type posterior communicating artery was present, internal trapping was performed following successful balloon test occlusion (BTO). Overall, there was no sign of infarction in the PICA territory, despite complete occlusion of aneurysms involving the PICA. There was no recurrent bleeding or ischemic symptoms during the follow-up periods. The overall treatment-related morbidity rate for the VA dissecting aneurysms involving the PICA was 16.7%.

Conclusions. Dissecting VA aneurysms that do not involve the PICA can be safely treated by internal trapping. For those lesions that do involve the PICA, a decision-making algorithm is advocated to maximize the efficacy of the treatment as well as to minimize the risks of treatment-related morbidity based on BTO.

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Impact of cortical hemodynamic failure on both subsequent hemorrhagic stroke and effect of bypass surgery in hemorrhagic moyamoya disease: a supplementary analysis of the Japan Adult Moyamoya Trial

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


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.


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.


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).


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 (

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Effect of choroidal collateral vessels on de novo hemorrhage in moyamoya disease: analysis of nonhemorrhagic hemispheres in the Japan Adult Moyamoya Trial

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


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.


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.


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.


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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Clinical implications of the cortical hyperintensity belt sign in fluid-attenuated inversion recovery images after bypass surgery for moyamoya disease

Eika Hamano, Hiroharu Kataoka, Naomi Morita, Daisuke Maruyama, Tetsu Satow, Koji Iihara, and Jun C. Takahashi


Transient neurological symptoms are frequently observed during the early postoperative period after direct bypass surgery for moyamoya disease. Abnormal signal changes in the cerebral cortex can be seen in postoperative MR images. The purpose of this study was to reveal the radiological features of the “cortical hyperintensity belt (CHB) sign” in postoperative FLAIR images and to verify its relationship to transient neurological events (TNEs) and regional cerebral blood flow (rCBF).


A total of 141 hemispheres in 107 consecutive patients with moyamoya disease who had undergone direct bypass surgery were analyzed. In all cases, FLAIR images were obtained during postoperative days (PODs) 1–3 and during the chronic period (3.2 ± 1.13 months after surgery). The CHB sign was defined as an intraparenchymal high-intensity signal within the cortex of the surgically treated hemisphere with no infarction or hemorrhage present. The territory of the middle cerebral artery was divided into anterior and posterior parts, with the extent of the CHB sign in each part scored as 0 for none; 1 for presence in less than half of the part; and 2 for presence in more than half of the part. The sum of these scores provided the CHB score (0–4). TNEs were defined as reversible neurological deficits detected both objectively and subjectively. The rCBF was measured with SPECT using N-isopropyl-p-[123I]iodoamphetamine before surgery and during PODs 1–3. The rCBF increase ratio was calculated by comparing the pre- and postoperative count activity.


Cortical hyperintensity belt signs were detected in 112 cases (79.4%) and all disappeared during the chronic period. Although all bypass grafts were anastomosed to the anterior part of the middle cerebral artery territory, CHB signs were much more pronounced in the posterior part (p < 0.0001). TNEs were observed in 86 cases (61.0%). Patients with TNEs showed significantly higher CHB scores than those without (2.31 ± 0.13 vs 1.24 ± 0.16, p < 0.0001). The CHB score, on the other hand, showed no relationship with the rCBF increase ratio (p = 0.775). In addition, the rCBF increase ratio did not differ between those patients with TNEs and those without (1.15 ± 0.033 vs 1.16 ± 0.037, p = 0.978).


The findings strongly suggest that the presence of the CHB sign during PODs 1–3 can be a predictor of TNEs after bypass surgery for moyamoya disease. On the other hand, presence of this sign appears to have no direct relationship with the postoperative local hyperperfusion phenomenon. Vasogenic edema can be hypothesized as the pathophysiology of the CHB sign, because the sign was transient and never accompanied by infarction in the present series.

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Correlation between reduction in microvascular transit time after superficial temporal artery–middle cerebral artery bypass surgery for moyamoya disease and the development of postoperative hyperperfusion syndrome

Tao Yang, Yoshifumi Higashino, Hiroharu Kataoka, Eika Hamano, Daisuke Maruyama, Koji Iihara, and Jun C. Takahashi


Hyperperfusion syndrome (HPS) is a notable complication that causes various neurological symptoms after superficial temporal artery (STA)–middle cerebral artery (MCA) bypass surgery for moyamoya disease (MMD). The authors used intraoperative indocyanine green (ICG) videoangiography to measure the change in microvascular transit time (MVTT) after bypass surgery. An analysis was then conducted to identify the correlation between change in MVTT and presence of postoperative HPS.


This study included 105 hemispheres of 81 patients with MMD who underwent STA-MCA single bypass surgery between January 2010 and January 2015. Intraoperative ICG videoangiography was performed before and after bypass surgery. The MVTT was calculated from the ICG time intensity curve recorded in the pial arterioles and venules. Multivariate logistic regression analysis was conducted to test the effect of multiple variables, including the change in MVTT after bypass surgery, on postoperative HPS.


Postoperative HPS developed in 28 (26.7%) of the 105 hemispheres operated on. MVTT was reduced significantly after bypass surgery (prebypass 5.34 ± 2.00 sec vs postbypass 4.12 ± 1.60 sec; p < 0.001). The difference between prebypass and postbypass MVTT values, defined as ΔMVTT, was significantly greater in the HPS group than in the non-HPS group (2.55 ± 2.66 sec vs 0.75 ± 1.78 sec; p < 0.001). Receiver operating characteristic curve analysis revealed that the optimal cutoff point of ΔMVTT was 2.6 seconds (sensitivity 46.4% and specificity 85.7% as a predictor of postoperative HPS). A ΔMVTT > 2.6 seconds was an independent predictor of HPS in multivariate analysis (hazard ratio 4.88, 95% CI 1.76–13.57; p = 0.002).


MVTT in patients with MMD was reduced significantly after bypass surgery. Patients with a ΔMVTT > 2.6 seconds tended to develop postoperative HPS. Because ΔMVTT can be easily measured during surgery, it is a useful diagnostic tool for identifying patients at high risk for HPS after STA-MCA bypass surgery for MMD.

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Successful obliteration and shrinkage of giant partially thrombosed basilar artery aneurysms through a tailored flow reduction strategy with bypass surgery

Clinical article

Susumu Miyamoto, Takeshi Funaki, Koji Iihara, and Jun C. Takahashi


The authors evaluated the efficacy of a new flow reduction strategy for giant partially thrombosed upper basilar artery (BA) aneurysms, for which proximal parent artery occlusion is not always effective.


Eight consecutive patients with severely symptomatic, partially thrombosed, giant upper BA aneurysms were treated with a tailored flow reduction strategy, or received conservative therapies. The flow reduction strategy comprised isolation of several branches from the upper BA at their origins with bypasses in addition to parent artery occlusion.


The median follow-up period of all 8 patients was 15.0 months (range 4–31 months). In 6 patients treated with flow reduction, the mean decrease in residual blood lumen was −10.7 mm (95% CI −19.7 to −1.7 mm; p = 0.029) and the mean decrease in diameter of the aneurysms was −11.5 mm (95% CI −25.1 to 2.1 mm; p = 0.082). Complete or virtually complete thrombosis was achieved in all but 1 aneurysm (83%) and shrinkage was observed in 4 (67%). In those in whom complete or virtually complete thrombosis was achieved, significant shrinkage of the aneurysm was observed (mean decrease in diameter −14.8 mm; 95% CI −28.8 to −0.8 mm; p = 0.043). Improvement or stabilization of symptoms occurred in 67% of the patients who received flow reduction treatment. Both patients who received conservative treatment had unfavorable outcomes.


The flow reduction strategy is effective at promoting complete thrombosis of the aneurysm. This strategy can also induce shrinkage of the aneurysm if successful thrombosis is achieved. Although the neurological outcome of the treatment appears favorable considering its intractable nature, further study of the treatment is necessary to confirm its clinical efficacy and safety.

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Successful “blind-alley” formation with bypass surgery for a partially thrombosed giant basilar artery tip aneurysm refractory to upper basilar artery obliteration

Case report

Jun C. Takahashi, Kenichi Murao, Koji Iihara, Yuko Nonaka, Junya Taki, Izumi Nagata, and Susumu Miyamoto

✓Partially thrombosed giant aneurysms that are located at the basilar artery (BA) bifurcation and are not amenable to clip application are among the most challenging lesions for neurosurgeons. They compress vital structures such as the brainstem and the thalamus, and the prognosis is extremely poor when they are left untreated. Although obliteration of the upper BA is a promising approach for these aneurysms, some lesions are refractory to this treatment, and effective additional strategies have not been clearly established. The authors report a case treated by placement of clips in the unilateral posterior cerebral artery (PCA) and posterior communicating artery as well as by superficial temporal artery–PCA bypass after unsuccessful upper BA obliteration. Complete thrombosis and dramatic shrinkage of the aneurysm were obtained.

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Unruptured paraclinoid aneurysms: a management strategy

Koji Iihara, Kenichi Murao, Nobuyuki Sakai, Atsushi Shindo, Hideki Sakai, Toshio Higashi, Shuji Kogure, Jun C. Takahashi, Katsuhiko Hayashi, Toshihiro Ishibashi, and Izumi Nagata

Object. To elucidate an optimal management strategy for unruptured paraclinoid aneurysms, the authors retrospectively reviewed their experience in the treatment of 100 patients who underwent 112 procedures for 111 paraclinoid aneurysms performed using direct surgery and/or endovascular treatment.

Methods. Between 1997 and 2002, 111 unruptured paraclinoid aneurysms categorized according to a modified al-Rodhan classification (Group Ia, 30 anterior wall lesions; Group Ib, 25 ventral paraclinoid lesions; Group II, 18 true ophthalmic artery lesions; Group III, 37 carotid cave lesions; and Group IV, one transitional lesion) were treated by direct surgery (35 lesions) and/or endovascular treatment (77 lesions) (one aneurysm was treated by both procedures). In lesions in Groups Ia, Ib, II, and III that were treated by endovascular treatment, complete aneurysm obliteration was achieved in 50, 65, 50, and 78%, respectively, and the combined transient and permanent morbidity rates due to cerebral embolic events were 20, 25, 20, and 13.9%, respectively. Overall, the transient morbidity rate after endovascular treatment was 14.3% and the permanent morbidity rate was 6.5%. Notably, permanent visual deficits caused by retinal embolism occurred after endovascular treatment in two patients with Group II aneurysms. Direct surgery was mainly performed in Groups Ia (20 lesions), Ib (five lesions), and II (eight lesions), with complete neck clip occlusion achieved in 80, 80, and 71.4%, respectively; the transient and permanent morbidity rates associated with aneurysms treated by surgery were 8.6 and 2.9%, respectively.

Conclusions. Endovascular therapy for superiorly projecting paraclinoid aneurysms (Groups Ia and II) is associated with lower rates of complete obliteration than direct surgery, and with rates of cerebral embolic events comparable to those of endovascular treatment in the other groups. Furthermore, endovascular treatment for Group II aneurysms entails additional risks of retinal embolism. Therefore, direct surgery is recommended for the treatment of paraclinoid aneurysms projecting superiorly. For other groups, especially for Group III, endovascular treatment is the acceptable first line of therapy.