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Yoshitaka Kurosaki, Kazumichi Yoshida, Ryu Fukumitsu, Nobutake Sadamasa, Akira Handa, Masaki Chin, and Sen Yamagata

OBJECT

Plaque characteristics and morphology are important indicators of plaque vulnerability. MRI-detected intraplaque hemorrhage has a great effect on plaque vulnerability. Expansive remodeling, which has been considered compensatory enlargement of the arterial wall in the progression of atherosclerosis, is one of the criteria of vulnerable plaque in the coronary circulation. The purpose of this study was risk stratification of carotid artery plaque through the evaluation of quantitative expansive remodeling and MRI plaque signal intensity.

METHODS

Both preoperative carotid artery T1-weighted axial and long-axis MR images of 70 patients who underwent carotid endarterectomy (CEA) or carotid artery stenting (CAS) were studied. The expansive remodeling ratio (ERR) was calculated from the ratio of the linear diameter of the artery at the thickest segment of the plaque to the diameter of the artery on the long-axis image. Relative plaque signal intensity (rSI) was also calculated from the axial image, and the patients were grouped as follows: Group A = rSI ≥ 1.40 and ERR ≥ 1.66; Group B = rSI< 1.40 and ERR ≥ 1.66; Group C = rSI 1.40 and ERR < 1.66; and Group D = rSI < 1.40 and ERR < 1.66. Ischemic events within 6 months were retrospectively evaluated in each group.

RESULTS

Of the 70 patients, 17 (74%) in Group A, 6 (43%) in Group B, 7 (44%) in Group C, and 6 (35%) in Group D had ischemic events. Ischemic events were significantly more common in Group A than in Group D (p = 0.01).

CONCLUSIONS

In the present series of patients with carotid artery stenosis scheduled for CEA or CAS, patients with plaque with a high degree of expansion of the vessel and T1 high signal intensity were at higher risk of ischemic events. The combined assessment of plaque characterization with MRI and morphological evaluation using ERR might be useful in risk stratification for carotid lesions, which should be validated by a prospective, randomized study of asymptomatic patients.

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Takeshi Funaki, Jun C. Takahashi, Yasushi Takagi, Takayuki Kikuchi, Kazumichi Yoshida, Takafumi Mitsuhara, Hiroharu Kataoka, Tomohisa Okada, Yasutaka Fushimi, and Susumu Miyamoto

OBJECT

Unstable moyamoya disease, reasonably defined as cases exhibiting either rapid disease progression or repeated ischemic stroke, represents a challenge in the treatment of moyamoya disease. Despite its overall efficacy, direct bypass for such unstable disease remains controversial in terms of safety. This study aims to reveal factors associated with unstable disease and to assess its impact on postoperative silent or symptomatic ischemic lesions.

METHODS

This retrospective cohort study included both pediatric and adult patients with moyamoya disease who had undergone 140 consecutive direct bypass procedures at Kyoto University Hospital. “Unstable moyamoya disease” was defined as either the rapid progression of a steno-occlusive lesion or repeat ischemic stroke, either occurring within 6 months of surgery. The extent of progression was determined through a comparison of the findings between 2 different MR angiography sessions performed before surgery. The clinical variables of the stable and unstable disease groups were compared, and the association between unstable disease and postoperative diffusion-weighted imaging (DWI)–detected lesion was assessed through univariate and multivariate analyses with generalized estimating equations.

RESULTS

Of 134 direct bypass procedures performed after patients had undergone at least 2 sessions of MR angiography, 24 (17.9%) were classified as cases of unstable disease. Age younger than 3 years (p = 0.029), underlying disease causing moyamoya syndrome (p = 0.049), and radiographic evidence of infarction (p = 0.030) were identified as factors associated with unstable disease. Postoperative DWI-defined lesions were detected after 13 of 140 procedures (9.3%), although only 4 lesions (2.9%) could be classified as a permanent complication. The incidence of postoperative DWI-detected lesions in the unstable group was notable at 33.3% (8 of 24). Univariate analysis revealed that unstable disease (p < 0.001), underlying disease (p = 0.028), and recent stroke (p = 0.012) were factors associated with DWI-detected lesions. Unstable disease remained statistically significant after adjustment for covariates in both the primary and sensitivity analyses (primary analysis: OR 6.62 [95% CI 1.79–24.5]; sensitivity analysis: OR 5.36 [95% CI 1.47–19.6]).

CONCLUSIONS

Unstable moyamoya disease, more prevalent in younger patients and those with underlying disease, is a possible risk factor for perioperative ischemic complications. Recognition of unstable moyamoya disease may contribute to an improved surgical result through focused perioperative management based on appropriate surgical risk stratification.

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Kazumichi Yoshida, Tao Yang, Yu Yamamoto, Yoshitaka Kurosaki, Takeshi Funaki, Takayuki Kikuchi, Akira Ishii, Hiroharu Kataoka, and Susumu Miyamoto

OBJECTIVE

Accumulated findings in the pathophysiology of atherosclerosis have demonstrated that not only luminal narrowing but also plaque characteristics influence the risk of future ischemic events. The morphology of the carotid artery (CA) changes in response to atherosclerotic development by expansive remodeling (ER), the clinical significance of which remains unclear. This study aimed to define associations between ER and local risk factors, including CA geometry and traditional systemic risk factors for ischemic events, to determine whether ER could serve as a clinical marker of carotid vulnerable plaque.

METHODS

The authors retrospectively analyzed 66 patients with CA stenosis who were scheduled to undergo carotid endarterectomy or CA stenting. They calculated ER ratios in the internal CA (ICA) from long-axis MR images and as the maximal distance between the lumen and the outer borders of the plaque perpendicular to the axis of the ICA/the maximal luminal diameter of the distal ICA at a region unaffected by atherosclerosis. Relative overall signal intensity (roSI) was calculated to assess intraplaque hemorrhage and defined as the signal intensity of plaque on an axial T1-weighted image with maximal stenosis relative to that of the adjacent sternocleidomastoid muscle. The authors evaluated CA geometry by calculating the angles between the common CA (CCA) and ICA, and between the CCA and external CA (ECA) using digital subtraction angiography. The ER ratios, age, sex, percentage of stenosis, roSI, hypertension, hyperlipidemia, low-density lipoprotein, statin medication, diabetes, smoking habit, and ischemic heart disease were compared between 33 symptomatic and 33 asymptomatic patients. The authors also compared symptomatic status, age, sex, percentage of stenosis, ICA angle, ECA angle, roSI, and other traditional atherosclerotic risk factors between groups with extensive and slight ER.

RESULTS

The ER ratio was significantly greater in symptomatic than in asymptomatic patients (1.91 ± 0.46 vs 1.68 ± 0.40, p < 0.05). The ICA angle was significantly larger in the group with extensive ER than in those with slight ER (33.9° ± 20.2° vs 21.7° ± 13.8°, p < 0.01). The roSI, ECA angle, percentage stenosis, or any other traditional vascular risk factors were not associated with ER.

CONCLUSIONS

Carotid ER might be an independent indicator of carotid vulnerable plaque, which should be validated in a longitudinal study of patients with carotid atherosclerosis, including those with nonstenotic to moderate stenosis.

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Kazumichi Yoshida, Hideki Endo, Nobutake Sadamasa, Osamu Narumi, Masaki Chin, Katsumi Inoue, Kazuaki Mitsudo, and Sen Yamagata

Object

The goal of this study was to evaluate the usefulness of long-axis black-blood MR (BB–MR) imaging for assessing plaque morphology and distribution in patients with atherosclerotic carotid artery (CA) stenosis.

Methods

Sixty-eight carotid arteries in 67 patients who were scheduled to undergo CA endarterectomy or CA stent placement due to atherosclerotic stenosis were included in this study. The patients had undergone CA BB–MR imaging and digital subtraction (DS) angiography within 3 weeks of revascularization. The DS angiography studies were performed using the transfemoral artery approach with selective common CA catheterization. The BB–MR images were acquired using a 1.5-T whole-body MR imaging unit, and T1-weighted images parallel to the long axis of the artery at 1-mm intervals were obtained. Plaque distribution was evaluated by measuring the distance between the CA bifurcation and the point that appeared to be the distal extent of the plaque on BB–MR imaging (D–MR imaging) and DS angiography images (D–DS angiography).

Results

Plaque distribution was clearly shown in 88.2% of the cases using long-axis BB–MR images, except for 8 arteries with poor image quality. In 4 arteries, D–DS angiography could not be obtained because the distal plaque end could not be confirmed. In 56 vessels, both the D–DS angiography and D–MR imaging could be measured; the mean D–MR imaging (19.75 ± 6.85 mm [standard deviation]) was significantly longer than the average D–DS angiography (16.32 ± 7.07 mm).

Conclusions

Long-axis BB–MR imaging can provide a noninvasive and accurate way to show CA plaque distribution; it is of great use not only for stroke risk assessment in patients with CA atherosclerosis but also for preoperative evaluation in patients requiring CA endarterectomy or CA stent placement.

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Takeshi Funaki, Jun C. Takahashi, Kazumichi Yoshida, Yasushi Takagi, Yasutaka Fushimi, Takayuki Kikuchi, Yohei Mineharu, Tomohisa Okada, Takaaki Morimoto, and Susumu Miyamoto

OBJECT

The authors’ aim in this paper was to determine whether periventricular anastomosis, a novel term for the abnormal collateral vessels typical of moyamoya disease, is reliably measured with MR angiography and is associated with intracranial hemorrhage.

METHODS

This cross-sectional study sampled consecutive patients with moyamoya disease or moyamoya syndrome at a single institution. Periventricular anastomoses were detected using MR angiography images reformatted as sliding-thin-slab maximum-intensity-projection coronal images and were scored according to 3 subtypes: lenticulostriate, thalamic, and choroidal types. The association between periventricular anastomosis and hemorrhagic presentation at onset was evaluated using multivariate analyses.

RESULTS

Of 136 eligible patients, 122 were analyzed. Eighteen (14.8%) patients presented with intracranial hemorrhage with neurological symptoms at onset. Intra- and interrater agreement for rating of the periventricular anastomosis score was good (κw = 0.65 and 0.70, respectively). The prevalence of hemorrhagic presentation increased with the periventricular anastomosis score: 2.8% for Score 0, 8.8% for Score 1, 18.9% for Score 2, and 46.7% for Score 3 (p < 0.01 for trend). Univariate analysis revealed that age (p = 0.02) and periventricular anastomosis score (p < 0.01) were factors tentatively associated with hemorrhagic presentation. The score remained statistically significant after adjustment for age (OR 3.38 [95% CI 1.84–7.00]).

CONCLUSIONS

The results suggest that periventricular anastomosis detected with MR angiography can be scored with good intra- and interrater reliability and is associated with hemorrhagic presentation at onset in moyamoya disease. The clinical utility of periventricular anastomosis as a predictor for hemorrhage should be validated in further prospective studies.

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Kazumichi Yoshida, Ryu Fukumitsu, Yoshitaka Kurosaki, Takeshi Funaki, Takayuki Kikuchi, Jun C. Takahashi, Yasushi Takagi, Sen Yamagata, and Susumu Miyamoto

OBJECT

The purpose of the present study was to investigate the association between carotid artery (CA) expansive remodeling (ER) and symptoms of cerebral ischemia.

METHODS

One hundred twenty-two consecutive CAs scheduled for CA endarterectomy (CEA) or CA stent placement (CAS) were retrospectively studied. After excluding 22 CAs (2 were contraindicated for MRI, 8 had near-occlusion, 6 had poor image quality, and 6 had restenosis after CEA or CAS), there were 100 CAs (100 patients) included in the final analysis. The study included 50 symptomatic patients (mean age 73.6 ± 8.9 years, 6 women, mean stenosis 68.5% ± 21.3%) and 50 asymptomatic patients (mean age 72.0 ± 5.9 years, 5 women, mean stenosis 79.4% ± 8.85%). Expansive remodeling was defined as enlargement of the internal carotid artery (ICA) with outward plaque growth. The ER ratio was calculated by dividing the maximum distance between the lumen and the outer borders of the plaque perpendicular to the axis of the ICA by the maximal luminal diameter of the distal ICA at a region unaffected by atherosclerosis using long-axis, high-resolution MRI.

RESULTS

The ER ratio of the atherosclerotic CA was significantly greater than that of normal physiological expansion (carotid bulb; p < 0.01). The ER ratio of symptomatic CA stenosis (median 1.94, interquartile range [IQR] 1.58–2.23) was significantly greater than that of asymptomatic CA stenosis (median 1.52, IQR 1.34–1.81; p = 0.0001). When the cutoff value of the ER ratio was set to 1.88, the sensitivity and specificity to detect symptoms were 0.6 and 0.78, respectively. The ER ratio of symptomatic patients was consistently high regardless of the degree of stenosis.

CONCLUSIONS

There was a significant correlation between ER ratio and ischemic symptoms. The ER ratio might be a potential indicator of vulnerable plaque, which requires further validation by prospective observational study of asymptomatic patients.

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Tao Yang, Kazumichi Yoshida, Takakuni Maki, Yasutaka Fushimi, Kiyofumi Yamada, Masakazu Okawa, Yu Yamamoto, Naoki Takayama, Keita Suzuki, and Susumu Miyamoto

OBJECTIVE

Carotid webs (CWs) have increasingly been recognized as a cause of recurrent ischemic stroke. However, the natural history and clinical course of CWs remain unclear. The authors aimed to clarify the prevalence, imaging features, and optimal treatment of CWs in a Japanese cohort study.

METHODS

A series of 444 consecutive Japanese patients who had undergone CTA of the head and neck between April 2011 and October 2016 was retrospectively reviewed. CW was diagnosed on CT angiograms as a membrane-like intraluminal filling defect along the posterior wall of the carotid bulb or the origin of the internal carotid artery (ICA) on oblique sagittal images and a corresponding thin septum on axial images.

RESULTS

Two patients with CWs were identified among 132 patients with suspected stroke. The prevalence of CWs among symptomatic patients with suspected stroke was 1.5%. The prevalence of asymptomatic CWs was 2.2% (7 of 312 cases). The CWs were located in the posterior wall of the carotid bulb in 7 patients and just distal to the ICA origin in 2 patients. There were no apparent differences in the location or lesion length between symptomatic and asymptomatic CWs. Four of the 7 asymptomatic CWs remained asymptomatic for at least 2 years of follow-up. Two patients with symptomatic CWs developed recurrent cerebral infarction and transient ischemic attack despite being on a regimen of oral antiplatelet agents, and carotid endarterectomy was performed as radical treatment. Patients with CWs were younger than controls (median age 55 vs 69 years, p = 0.003) and were less frequently male than controls (33% vs 72%, p = 0.025). CW cases showed significantly fewer common atherosclerosis risk factors than the control group (p < 0.05).

CONCLUSIONS

Although limited to CTA patients, this study reported on the prevalence and common site of CWs, focusing on symptomatic and asymptomatic Japanese patients. Extensive cross-sectional and prospective observational studies are warranted to elucidate the overall prevalence and natural history of CWs.

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Takeshi Funaki, Jun C. Takahashi, Yasushi Takagi, Kazumichi Yoshida, Yoshio Araki, Takayuki Kikuchi, Hiroharu Kataoka, Koji Iihara, and Susumu Miyamoto

Object

In the study of pediatric moyamoya disease, information on long-term social outcomes and risk factors for unfavorable social outcomes remains insufficient. The authors analyzed the long-term results of surgical revascularization for pediatric patients with moyamoya disease to determine whether the involvement of a stenoocclusive lesion in the posterior cerebral artery (PCA), relatively common in pediatric moyamoya disease, represents an underlying predictor for unfavorable social outcomes.

Methods

Prospectively collected data on 61 consecutive patients with moyamoya disease who had undergone combined bypass surgery were analyzed. Neuroradiological features and other baseline clinical factors were incorporated into univariate and multivariate analyses to determine any association with an unfavorable social outcome, defined as difficulty attending regular school or obtaining regular employment.

Results

Posterior cerebral artery involvement detected by angiography on admission was noted in 22 (36.1%) of the 61 patients. Follow-up data were acquired in 56 patients (91.8%), and the mean follow-up period was 15.8 years. While transient ischemic attacks were eliminated in 52 (92.9%) of these 56 patients after surgery, and late-onset ischemic stroke was observed in only 1 patient during the follow-up period, 10 (17.9%) experienced an unfavorable social outcome. Although younger age at onset, longer duration between onset and surgery, infarction present on preoperative neuroradiological images, and PCA involvement had been identified as risk factors for an unfavorable social outcome in univariate analysis, only infarction present on preoperative images and PCA involvement remained statistically significant after multivariate adjustment.

Conclusions

Posterior cerebral artery involvement can be considered one of the underlying risk factors for unfavorable social outcome and should be studied further to improve social outcome in pediatric moyamoya disease.

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Masaomi Koyanagi, Akira Ishii, Hirotoshi Imamura, Tetsu Satow, Kazumichi Yoshida, Hitoshi Hasegawa, Takayuki Kikuchi, Yohei Takenobu, Mitsushige Ando, Jun C. Takahashi, Ichiro Nakahara, Nobuyuki Sakai, and Susumu Miyamoto

OBJECTIVE

Long-term follow-up results of the treatment of unruptured intracranial aneurysms (UIAs) by means of coil embolization remain unclear. The aim of this study was to analyze the frequency of rupture, retreatment, stroke, and death in patients with coiled UIAs who were followed for up to 20 years at multiple stroke centers.

METHODS

The authors retrospectively analyzed data from cases in which patients underwent coil embolization between 1995 and 2004 at 4 stroke centers. In collecting the late (≥ 1 year) follow-up data, postal questionnaires were used to assess whether patients had experienced rupture or retreatment of a coiled aneurysm or any stroke or had died.

RESULTS

Overall, 184 patients with 188 UIAs were included. The median follow-up period was 12 years (interquartile range 11–13 years, maximum 20 years). A total of 152 UIAs (81%) were followed for more than 10 years. The incidence of rupture was 2 in 2122 aneurysm-years (annual rupture rate 0.09%). Nine of the 188 patients with coiled UIAs (4.8%) underwent additional treatment. In 5 of these 9 cases, the first retreatment was performed more than 5 years after the initial treatment. Large aneurysms were significantly more likely to require retreatment. Nine strokes occurred over the 2122 aneurysm-years. Seventeen patients died in this cohort.

CONCLUSIONS

This study demonstrates a low risk of rupture of coiled UIAs with long-term follow-up periods of up to 20 years. This suggests that coiling of UIAs could prevent rupture for a long period of time. However, large aneurysms might need to be followed for a longer time.