Pathological and immunohistochemical findings of an autopsy case of adult moyamoya disease

Moyamoya disease is vaso‐occlusive disease involving the arteries of the circle of Willis that is accompanied by a compensatory recruitment of a vascular network. The pathological and immunohistochemical findings of an autopsy case of hemorrhagic moyamoya disease in a 69‐year‐old woman are described in the present report. The autopsy findings of the brain revealed cerebral and intraventricular hemorrhage with edema. The left anterior cerebral artery, bilateral middle cerebral arteries and left posterior cerebral artery were marked narrowing, and the other arteries revealed mild narrowing. Microscopically, the arteries of the circle of Willis showed narrowed lumen, fibrocellular intimal thickening, marked tortuousness of internal elastic lamina and attenuation of media. The thickened intima was composed of smooth muscle cells. The vessels with dilated or irregular‐shaped lumen suggested abnormal vascular networks demonstrated by angiography. In this case, no correlation between the abnormal vascular network and expression of VEGF or VEGF receptor was disclosed. It was hypothesized that abnormal vascular networks might be composed of collateral vessels in relation to various pathological changes of the arteries, such as occlusion and stenosis, and intracranial hemorrhage in patients with moyamoya disease might occur as a result of rupture of arteries including abnormal vascular networks.     

Fetal radiation exposure and moyamoya disease

Moyamoya disease is a progressive occlusive disease of the cerebral vasculature with particular involvement of the circle of Willis. We present the first reported patient with moyamoya disease possibly due to radiation exposure during fetal development. A 10-year-old male, whose mother had undergone radiotherapy when pregnant, presented with moyamoya disease. The relevant literature is discussed.     

Primary Percutaneous Transluminal Angioplasty for Early Moyamoya Disease

Moyamoya disease is a progressive steno-oclusive arteriopathy of the circle of Willis that manifests on cerebral angiography with a characteristic net of vessels at the base of the brain representing collateralization. Described initially in Japan where children present with cerebral ischemia and adults with hemorrhagic stroke, it was recognized to have a more benign course in the United States, mainly causing cerebral ischemic events in young adults. Medical treatment is not intended to stop the progression of the disease and surgery is not exempt of risks. We present a patient with early moyamoya disease in the United States in whom primary transluminal angioplasty, a less invasive procedure, was performed to treat the stenotic arteriopathy with good immediate and sustained clinical and angiographic results, without evidence of restenosis at the site of angioplasty 2 years later.     

Diffusion-weighted imaging in moyamoya disease.

Moyamoya disease is characterized by progressive intracranial vascular stenoses of the circle of Willis, resulting in successive ischemic events. We report serial diffusion-weighted imaging studies in a case of moyamoya disease. A 4-year-old right-handed patient presented with multiple infarcts in the right and left hemispheres. Each new infarct was unambiguously recognized as bright on diffusion-weighted imaging. Previous infarcts, readily detected on other magnetic resonance imaging sequences, were not bright on diffusion-weighted imaging. The patient subsequently underwent bilateral synangiosis. In this case, the diffusion-weighted images were helpful in assessing the extent of infarcts, determining the age of the lesion, and correlation with new clinical findings. We emphasize the usefulness of diffusion-weighted imaging for following the clinical course of children with moyamoya disease, in whom new focal deficits are highly suspicious of new infarcts.     

烟雾病伴发颅内动脉瘤的诊断和治疗

目的 探讨烟雾病伴发颅内动脉瘤的诊断和治疗.方法 回顾性分析78例烟雾病患者的临床表现、影像学特点及治疗方法 .结果 78例烟雾病中,8例合并动脉瘤(10.3%),其中6例表现为颅内出血,2例表现为缺血症状;其中2例位于Willis环远端血管,6例位于Willis环.3例行显微外科手术夹闭,3例行血管内栓塞治疗,2例保守治疗.平均随访26个月(8-40个月),1例在右侧后交通动脉动脉瘤栓塞治疗12个月后,再次出现左侧外囊出血死亡,7例无再次颅内出血.结论 烟雾病患者应行全脑血管造影检查,部分烟雾病可伴发动脉瘤.位于Willis环的动脉瘤可行显微外科手术治疗或血管内栓塞治疗,位于Willis环远端血管的动脉瘤治疗,有待进一步探讨.     

Multiple encephalogaleoperiosteal synangiosis for bilateral carotid artery stenosis in a 13-year-old girl: a case report

Introduction

Encephalogaleoperiosteal synangiosis (EGS) has been widely used to treat children with moyamoya disease (MMD). We present the first case of successful multiple EGS in a patient with brain ischemic disease who presented with different cerebrovascular findings from MMD.

Methods

A 13-year-old girl had an increased frequency of transient ischemic attacks that affected her right extremities. Digital subtraction angiography showed tapering of the internal carotid artery (ICA). The anterior cerebral artery (ACA) and middle cerebral artery (MCA) were visible on vertebral angiogram, but not on carotid angiogram. The intact circle of Willis and lack of hypervascularity of the lenticulostriate arteries were observed. Decreased regional cerebral blood flow (CBF) in the bilateral ACA and MCA territories quantified by ¹²³I-N-isopropyl-p-iodoamphetamine-single photon emission computed tomography indicated the need for extracranial-intracranial bypass surgery. Multiple EGS procedures were performed instead of direct anastomosis, which is the standard procedure for intracranial ICA stenosis, because the space for the craniotomy was limited by transdural anastomosis.

Results

Despite the fact that the diagnosis of MMD was questionable, the hemispheres were well vascularized, and the neurology and CBF improved postoperatively.

Conclusion

The preserved circle of Willis and lack of moyamoya vessels were inconsistent with the features of MMD. However, childhood onset, bilateralness, chronic intracranial ICA stenosis, and transdural anastomosis indicated the same underling pathogenicity as MMD. It is hypothesized that ICA stenosis occurred immediately proximal to the posterior communicating artery in this case. This would have produced the atypical finding of the remaining circle of Willis without growth of the basal moyamoya vessels.

     

颅底动脉环异常与老年人缺血性脑血管病关系临床探讨

目的探讨颅底动脉环(Willis)的形态变异与缺血性脑血管病的关系,为临床治疗方法选择提供解剖依据。方法采用数字减影血管造影技术(DSA)对64例老年缺血性脑血管病患者行主动脉弓和全脑血管造影,应用A1优势征判断Willis前环的完整性,以大脑后动脉供血类型判断Willis后环的完整性。结果本组病人中A1优势征者43.8%;大脑后动脉供血为基底动脉供血型者40.6%;颈动脉供血型者21.9%;混合供血型者37.5%。共检出血管狭窄31例,临床症状和血管狭窄部位符合者23例(74.2%),不符者8例(25.8%)。结论Willis前环的A1优势征和Willis后环中大脑后动脉供血为颈动脉供血型、混合供血型者提示Willis动脉环形态变异;形态异常的Willis动脉环与缺血性脑血管病的发病及发病后的血流动力学代偿密切相关;血流动力学的改变可通过侧支循环造成临床症状和血管狭窄部位不符,可能影响脑梗死后血管活性药物的选择及超选择性动脉溶栓时溶栓部位的选择。     

Moyamoya disease. Posterior cerebral artery occlusion and pattern-reversal visual-evoked potential

Although vascular abnormality in moyamoya disease predominates in the anterior and middle cerebral arteries, the posterior cerebral artery (PCA) has been found to be involved in the course of the disease. To explore PCA occlusion by noninvasive means, we studied visual-evoked potentials in the patients with PCA occlusion (occlusive group), as well as in those without PCA occlusion (nonocclusive group). The results were compared with those of other examinations that also detected an occipital lobe pathologic condition. Abnormalities of those examinations were highly specific to PCA occlusion. Positron emission tomography and pattern-reversal visual-evoked potentials yielded high incidence of abnormality in the occlusive group (86% and 75%, respectively), and expressed the side of PCA occlusion if the occlusion was unilateral. Since pattern-reversal visual-evoked potentials is popular and a low-cost examination compared with positron emission tomography, we conclude that pattern-reversal visual-evoked potentials is the most practical mean to explore PCA occlusion in the course of moyamoya disease.     

Revascularization surgery for moyamoya disease

Moyamoya disease is a disease characterized by chronic occlusion of the circle of Willis with subsequent development of fine vascular networks in the ganglionic region, which is common in Japanese people. The term of ‘moyamoya’ means puff of smoke in the Japanese language and represents the characteristic angiographic findings of subsequent development of fine vascular networks in the ganglionic region. Although reconstructive surgery for moyamoya disease has been widely accepted nowadays^1,2,5-7, there is still no definite consensus as to a surgical indication for patients with an haemorrhagic attack⁶ and as to the selection of an operative method for each individual patient^5-7. This paper presents our overall surgical results and introduces a new operation, devised by Y. Nakagawa (i.e. EMAS). It refers also to surgical intervention for patients with haemorrhagic attacks.     

Revascularization surgery for moyamoya disease

Moyamoya disease is a disease characterized by chronic occlusion of the circle of Willis with subsequent development of fine vascular networks in the ganglionic region, which is common in Japanese people. The term of 'moyamoya' means puff of smoke in the Japanese language and represents the characteristic angiographic findings of subsequent development of fine vascular networks in the ganglionic region. Although reconstructive surgery for moyamoya disease has been widely accepted nowadays, there is still no definite consensus as to a surgical indication for patients with an haemorrhagic attack and as to the selection of an operative method for each individual patient. This paper presents our overall surgical results and introduces a new operation, devised by Y. Nakagawa (i.e. EMAS). It refers also to surgical intervention for patients with haemorrhagic attacks.     

Absent collateral function of the circle of Willis as risk factor for ischemic stroke

BACKGROUND: Autopsy studies show a higher prevalence of circle of Willis anomalies in brains with signs of ischemic infarction. Our goal was to examine the collateral function of the circle of Willis in ischemic stroke patients and to assess in a case-control study if a collateral deficient circle of Willis is a risk factor for ischemic stroke in patients with severe internal carotid artery (ICA) occlusive disease. METHODS: Our case-control study included 109 patients with an acute ischemic stroke in the anterior circulation and 113 patients with peripheral arterial disease and no known history of cerebral ischemia. The collateral function of the anterior and posterior communicating arteries of the circle of Willis was assessed by means of transcranial color-coded duplex ultrasonography (TCCD) and carotid compression tests. RESULTS: TCCD was successfully performed in 75 case patients (mean age 64 years, range 41-91 years) and in 100 control patients (mean age 61 years, range 35-89 years). In 26 cases and 19 controls, a >/=70% stenosis or occlusion of the ICA was found. A nonfunctional anterior collateral pathway in the circle of Willis was found in 33% of the cases and in 6% of the controls (p < 0.001). The posterior collateral pathway was nonfunctional in 57% of the cases and in 43% of the controls (p = 0.02). In patients with severe ICA occlusive disease, the odds ratios of a nonfunctional anterior and a nonfunctional posterior collateral pathway were 7.33 (95% confidence interval, CI, = 1.19-76.52) and 3.00 (95% CI = 0.77-12.04), respectively. CONCLUSIONS: Patients who suffer ischemic stroke in the anterior circulation have a higher incidence of collateral deficient circles of Willis than those with atherosclerotic vascular disease without ischemic cerebrovascular disease. The presence of a nonfunctional anterior collateral pathway in the circle of Willis in patients with severe ICA occlusive disease is strongly associated with ischemic stroke.     

Treatment of moyamoya syndrome in children

Moyamoya syndrome, a known cause of pediatric stroke, is a chronic cerebrovascular occlusive disorder of unknown etiology that can lead to severe, permanent neurologic disability. It is characterized by progressive stenosis of the distal intracranial carotid arteries and branches of the circle of Willis and the nearly simultaneous appearance of basal arterial collateral vessels, which vascularize hypoperfused brain distal to the occluded vessels. Most children with moyamoya syndrome present either with transient ischemic attacks or strokes. This review summarizes the current medical and surgical practices used in the treatment of moyamoya syndrome in children.     

尼莫地平预防烟雾病血管重建术后脑梗死的效果分析

目的 探讨尼莫地平预防烟雾病血管重建术后脑梗死的效果。方法 回顾性分析2016年7月至2019年5月联合血管重建术治疗的73例烟雾病的临床资料。46例使用尼莫地平（观察组），27例未使用尼莫地平（对照组）。术后1周复查颅脑CT或DWI观察新发脑梗死。结果 73例中，术后1周发生脑梗死19例，发生率为26.03%。观察组术后脑梗死发生率（17.39%，8/46）明显低于对照组（40.74%，11/27；P<0.05）。多因素logistic回归分析显示，未使用尼莫地平是烟雾病联合血管重建术后脑梗死独立危险因素（P<0.05）。结论 烟雾病联合血管重建术后脑梗死发生率较高，使用尼莫地平可以有效预防预防脑梗死。     

Hypomelanosis of Ito and Moyamoya disease

Moyamoya disease is a cerebrovascular disease characterized by stenosis and occlusion of the arteries of the circle of Willis, with abnormal telangiectatic collateral circulation at the base of the brain. An association between moyamoya disease and neurofibromatosis 1, a neurocutanoeus disorder, is well established in the literature. However, its association with other neurocutaneous syndromes is infrequently reported. Hypomelanosis of Ito, another neurocutaneous syndrome, is characterized by macular hypopigmented skin whorls and variable neurologic involvement. Only one case study of an association between hypomelanosis of Ito and moyamoya disease has been reported in the English literature. We report a 17-year-old girl with both hypomelanosis of Ito and angiographic moyamoya disease. She presented with intractable seizures, progressive left hemiparesis, and skin manifestations of hypomelanosis of Ito. Although one might consider a coincidental association, this second case points to an association between the two disorders. Detailed neuroimaging, in particular angiography, should be considered in children with hypomelanosis of Ito and abnormal neurologic findings.     

The clinical relevance of fetal variant of the circle of Willis and its influence on the cerebral collateral circulation

In a fetal variation of circle of Willis (CoW) there is an embryological defect of the primary collateral circulation. Besides the fact that collateral flow cannot develop between anterior and posterior circulation, the tentorium namely prevents cerebellar vessels from connecting to the supra-tentorium territory. Therefore patients with a fetal variation of circle of Willis could be more prone to develop vascular insufficiency. An association between the regional cerebral blood volume (rCBV) inter-hemispheric asymmetry and CoW collateralization was observed with a topographic significance of corona radiate rather than centrum semiovale. An overview of the literature is given. We propose a fetal variation of circle of Willis as a risk factor for stroke should be subject of further investigation.     

Usefulness of carotid duplex ultrasonography in a patient with moyamoya disease]

The patient is a 35-year-old man who had a medical history of epilepsy in childhood. He came to our hospital because of transient disturbance of consciousness and left hemiplegia just after evacuation. At first, we thought that he had epilepsy with Todd's palsy. But we had to do a differential diagnosis for a transient ischemic attack such as paradoxical embolism, because his symptoms occurred just after evacuation. An electroencephalogram and brain computerized tomography were immediately performed, but no abnormality was detected. Hematologic studies were normal, and no deep vein thrombosis was detected in the veins of the lower extremities by duplex ultrasonography Doppler. But carotid duplex ultrasonography showed an increase in end-diastolic flow velocity and a decrease in vascular resistance in both external carotid arteries. These findings indicated that there was arteriovenous malformation such as moyamoya disease. Brain magnetic resonance imaging showed spotty high signal lesions in the subcortical areas on a fluid-attenuated inversion-recovery(FLAIR) image, and the middle cerebral artery was not visualized on magnetic resonance angiography (MRA). Cerebral angiography demonstrated moyamoya vessels in the brain and collateral circulation from the external carotid artery. Therefore, we diagnosed him as having moyamoya disease. Duplex ultrasonography of the common and, internal carotid, and vertebral arteries is a widely-used technique. Recently, cerebral angiography, MRA and transcranial Doppler have been applied to detect intracranial vascular malformation. But these results suggested that moyamoya disease could be detected by means of carotid duplex ultrasonography. Finally, we considered that carotid duplex ultrasonography was not only a noninvasive screening method but also a useful for the diagnosis of moyamoya disease.     

Evaluation of cross-circulation through circle of Willis using an ultrasonic Doppler technique. Part I. Comparison between blood flow velocity by ultrasonic Doppler flowmetry and angiogram

In 24 patients with cerebrovascular disease and 6 without organic brain lesions, the increased velocity of blood flow in both the internal carotid and vertebral arteries during a contralateral carotid compression was compared with the angiographic appearance of the circle of Willis. The flow velocity was measured using ultrasonic Doppler flowmetry. It was not possible to investigate fully the relationship between the increase of velocity of blood flow in the internal carotid artery and the anatomical variations of the circle of Willis, specifically the anterior cerebral and communicating arteries. The velocity of flow in the patients with an aplastic proximal portion of the anterior cerebral artery showed no increase. There were no differences in the increase of velocity of flow in the vertebral artery in patients with hypoplastic, normal and fetal posterior communicating arteries. It is considered that although anatomical variations of the circle vessels influence the cross-circulation via the circle of Willis, peripheral vascular factors distal to the circle also play an important role in the quantity of cross-circulation through the circle.     

烟雾病的临床特征及外科治疗的流行病学分析

目的探讨烟雾病的性别、年龄、地区分布特点、临床表现以及外科治疗效果分析。方法回顾性分析2017-01—2019-04河南省人民医院收治的542例烟雾病患者的临床资料,包括性别、年龄、地区分布、临床表现等,分析其手术效果及预后。结果542例烟雾病患者中,男女比例为1∶1.05(男265/女277);年龄(45±12.7)岁(3~75岁),年龄分布呈现双峰形态,好发于9~11岁儿童及46~51岁成人段;河南南方地区发病率明显高于其他区域,呈区域集中现象。儿童成人均以缺血性症状为主;缺血型以头痛、头晕为主要首发症状,出血型中以脑室出血最常见。432例接收手术治疗的烟雾病患者中,行间接血管重建术66例,联合血管重建术366例,18例围手术期出现并发症,其余均恢复顺利,临床症状得到改善,随访结果良好。结论河南地区烟雾病的发病无明显性别差异,年龄呈双峰分布,成人多见,多为缺血型,纳入病例中儿童均为缺血型;豫南地区发病率明显高于其他地区;个体化脑血管重建术具有明确的疗效。     

Moyamoya disease in children A review of the clinical and radiological features and current treatment

Two cases of moyamoya disease observed in two children are reported. The two cases recall the frequency of ischemic strokes, transient ischemic attacks, and seizures revealing the disease. Diagnosis is made by cerebral arteriography showing carotid stenosis and the dense deep arterial collateral as seen in these two cases. Magnetic resonance imaging makes it possible to identify this vascular disease as it reveals vascular varicosities in the basal ganglia, as in case 1. Strokes can sometimes be prevented by constructing an anastomosis between the superficial temporal artery and the middle cerebral artery, as demonstrated in case 1. Thus, the diagnosis of moyamoya disease has been improved by magnetic resonance imaging and there is now a surgical treatment to prevent ischemic stroke.     

Occlusion of unilateral carotid artery in Down syndrome

The association between moyamoya phenomena and Down syndrome (DS) is reported in the literature. This paper reports a case of DS, which at age 9 presented right hemiparesis, secondary to the occulusion of the left internal carotid artery; cerebral angiography (CAG) showed a collateral circulation that mimicks the moyamoya phenomenon. Clinical recovery was almost complete; a second CAG after 15 months showed a persistent occlusion of the left internal carotid artery and an opacification of the left middle cerebral artery from abnormal vessels; but the collateral circulation is not enhanced. This case proves that in DS cerebrovascular occlusions may present moyamoya-like phenomena. These differ however from the true moyamoya disease in a number of aspects: the arterial occlusion is unilateral, the evolution is favorable and revascularization does not occur through the peculiar abnormal vessels of the moyamoya syndrome.