Arteriovenous Malformation with an Occlusive Feeding Artery Coexisting with Unilateral Moyamoya Disease

Background

Arteriovenous malformations (AVMs) with vascular abnormalities, including aneurysms, have been reported frequently. However, the coexistence of AVM and unilateral moyamoya disease is rare. We report herein an AVM patient who presented with acute ischemic stroke with unilateral moyamoya disease and occlusion of the feeding artery.

Case Report

A-41-year old man was admitted with sudden dysarthria and facial palsy. Brain computed tomography and magnetic resonance imaging revealed an acute infarction adjacent to a large AVM in the right frontal lobe. Cerebral angiography revealed occlusions of the proximal right middle cerebral and proximal anterior cerebral arteries, which were the main feeders of the AVM. Innumerable telangiectatic moyamoya-type vessels between branches of the anterior cerebral artery and dilated lenticulostriate arteries on the occluded middle cerebral artery were detected. However, a nidus of the AVM was still opacified through the distal right callosomarginal artery, which was supplied by the remaining anterior cerebral artery and leptomeningeal collaterals from the posterior cerebral artery.

Conclusions

While AVM accompanied by unilateral moyamoya disease is rare, our case suggests an association between these two dissimilar vascular diseases.     

Analysis of ischemic cerebral lesions using 3.0-T diffusion-weighted imaging and magnetic resonance angiography after revascularization surgery for ischemic disease

Background

Cerebral revascularization surgery (CRS) is increasingly recognized as an important component in the treatment of complex cerebral vascular disease and tumors. CRS requires that the incidence of perioperative neurological complications should be minimized, because CRS for ischemic disease is often not the goal of treatment, but rather a prophylactic surgery. CRS carries the risk of focal postoperative neurological deficits. Little has been established concerning mechanisms of post-CRS ischemia. We used 3.0-T diffusion-weighted magnetic resonance imaging (DWI) and magnetic resonance angiography (MRA) to analyze the incidence and mechanism of ischemic lesions.

Methods

We studied the anterior circulation territory after 20 CRS procedures involving 33 vascular anastomosis procedures (13 double anastomoses and 7 single anastomoses) in 12 men and 8 women between June 2007 and October 2011. The operations included single or double superficial temporal artery–middle cerebral artery (STA–MCA) anastomosis to treat internal carotid artery/MCA occlusions or severe MCA stenosis. A combined STA–MCA anastomosis and indirect bypass were performed for moyamoya disease. Postoperative DWI and MRA were obtained in all patients between 24 and 96 h after surgery to detect thromboembolism, hypoperfusion, or procedural ischemic complications and vasospasms of the donor STA.

Results

Follow-up DWI and MRA were carried out 1.8 ± 0.6 days after CRS (range, 1–4 days). Temporary occlusion time for anastomoses averaged 18.9 min (range, 16–32 min). Asymptomatic new hyperintensities occurred in the ipsilateral hemisphere of 2 patients on postoperative DWI (10% patients/6.0% anastomoses), and 1 moyamoya patient (5.0% patients/3.0% anastomoses) developed a symptomatic hyperintensity in the ipsilateral occipital lobe in response to the operation. Two abnormal small (<5 mm) cortical DWI lesions were caused by sacrifices of a small branch of the recipient MCA.

Conclusion

This study is the first postoperative 3.0-T DWI study of CRS and related clinical events. The incidence of symptomatic postoperative DWI abnormalities was restricted to 1 moyamoya patient representing 5.0% of total patients and 3.0% anastomoses. Although some postoperative DWI abnormalities occurred, CRS was found to be safe with a low risk of symptomatic ischemia.     

Determinants of intellectual outcome after surgical revascularization in pediatric moyamoya disease: a multivariate analysis

Objects The aim of this study was to clarify predictors for poor intellectual outcome in pediatric moyamoya disease.Methods Fifty-two pediatric patients were included. Clinical diagnosis was transient ischemic attacks (TIA) in 35 and completed stroke in 17. Ten patients underwent indirect synangiosis through small craniotomy, whereas the other 42 underwent superficial temporal artery (STA)–middle cerebral artery (MCA) anastomosis and indirect synangiosis through large craniotomy. Full-scale IQ (FSIQ) was measured using the Wechsler intelligence scale for children (WISC) after surgery. Multivariate logistic regression models were applied to test the effect of clinical factors on intellectual outcome.Results and conclusion Eight patients revealed mentally impaired status (FSIQ<70). Multivariate analysis revealed that completed stroke and small craniotomy surgery were significantly associated with poor intellectual outcome. Odds ratios of each factor were 33.4 (95% CI, 2.4–474) and 19.6 (95% CI, 1.8–215) respectively. Early diagnosis and the revascularization procedure over as wide an area as possible may be essential to improve their intellectual outcome.     

Cerebral hemodynamics and “re-build-up” phenomenon on electroencephalogram in children with moyamoya disease

Re-build-up phenomenon, induced by hyperventilation, is a characteristic finding on electroencephalogram (EEG) in children with moyamoya disease, and suggests close correlation with cerebral ischemic attack. Its mechanism, however, remains obscure. In this study, we examined the relationship between the cerebral hemodynamics and this phenomenon before and after vascular reconstructive surgery. Regional cerebral blood flow and its reactivity to acetazolamide were analyzed using the xenon-133 inhalation method and single photon emission computed tomography in six children with moyamoya disease. These results were compared with the EEG. Regional vasoreactivity to acetazolamide was significantly lower in re-build-up-positive regions than in re-build-up-negative regions. Postoperative studies revealed a significant improvement of reactivity in the regions where the re-build-up phenomenon disappeared after surgery. These results suggest that the re-build-up phenomenon represents a focal reduction of the cerebral perfusion reserve in moyamoya disease.     

Varied presentations of moyamoya disease in a tertiary care hospital of north-east India

Introduction:

Moyamoya disease is a chronic progressive cerebrovascular disorder, characterized by stenosis or occlusion of bilateral internal carotid arteries (ICAs), anterior cerebral arteries (ACAs) and middle cerebral arteries (MCAs), accompanied by a collateral network of vessels formed at the base of the brain. Ischemia and intracranial hemorrhage are the common typical manifestations. However moyamoya disease has been associated with atypical presentations like headache, seizures and involuntary movements. Although frequently reported from Asian countries like Japan, China and Korea, only few studies reported on clinical manifestations of moyamoya disease from India.

Objectives:

To study the varied presentations of moyamoya disease in a tertiary care hospital of north-east India.

Material and Methods:

Relevant investigations were done to rule out other causes of moyamoya syndrome.

Results:

We report 6 cases of moyamoya disease with varied presentations from a tertiary care referral government hospital. Case 1, 2 and 6 presented with alternating hemiparesis. Case 3 had amaurosis fugax. Case 4 had history suggestive of ischemic stroke and presented with hemichorea. Case 4 had focal seizure as the only manifestation. Cases 4 and 5 notably had stenosis of posterior cerebral artery (PCA) in addition to stenosis of bilateral ICAs, ACAs and MCAs.

Conclusion:

Owing to its low incidence in India, moyamoya disease is easily overlooked as a possible diagnosis. However, because of its progressive nature, it is imperative to diagnose this disease early and offer surgical treatment to the patients.     

Moyamoya disease associated with Behcet's disease.

A 32-year-old woman with Behcet's disease suffered repeated transient ischemic attacks (TIA) consisting of left hemiparesis. Cerebral angiography revealed the typical findings of moyamoya disease, with occlusion of the supraclinoid portion of both internal carotid arteries, coupled with abnormal collateral vessels. She underwent right superficial temporal artery to middle cerebral artery (STA-MCA) anastomosis and encephalomyosynangiosis, due to decreased reserve capacity demonstrated on acetazolamide single positron emission computed tomography (SPECT). Postoperatively, the TIA symptoms subsided. This is the first report of moyamoya disease associated with Behcet's disease, and moyamoya disease should be considered in the differential diagnosis of cerebrovascular events in patients with Behcet's disease. Revascularization surgery is recommended for the prevention of ischemic insults resulting in permanent deficits.     

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.     

Diagnosis of Moyamoya Disease with Transcranial Doppler Sonography: Correlation Study with Magnetic Resonance Angiography

BACKGROUND AND PURPOSE: Although the diagnosis of moyamoya disease may be confirmed by digital subtraction angiography, recent studies have shown the accuracy of magnetic resonance angiography. Characteristics of transcranial Doppler, a noninvasive and cost-effective method, and specific transcranial Doppler parameters reflecting distinct vascular status in moyamoya disease are explored. METHOD AND PATIENTS: Consecutive patients (> 15 years of age) diagnosed with moyamoya disease by a typical clinical history and digital sub traction angiography or magnetic resonance angiography were included. The statuses of the anterior, middle, and posterior cerebral arteries were graded as stage 1, stage 2, and stage 3 by magnetic resonance angiography. Mean flow velocity and pulsatility index were compared between these groups, and the receiver operating characteristic analysis was used to define transcranial Doppler criteria for distinct vascular status. RESULTS: Forty-five patients were included (37 women; mean age, 34.9 +/- 11.4 years). Mean flow velocity was higher and pulsatility index was lower in stage 2 (P < .01), while mean flow velocity was lower and pulsatility index was higher in stage 3 than in stage 1 (P < .01). Cutoff values reflecting stenosis or occlusion with substantial sensitivity and specificity were as follows: mean flow velocity > 85 cm/s or pulsatility index < 0.60 for stage 2, and mean flow velocity < 50 cm/s for stage 3 of middle cerebral artery; mean flow velocity > 80 cm/s or pulsatility index < 0.60 for stage 2 of anterior cerebral artery; and mean flow velocity > 60 cm/s or pulsatility index < 0.60 for stage 2 of posterior cerebral artery. CONCLUSION: Transcranial Doppler may help to refine magnetic resonance angiography findings and thus help clinicians differentiate severity or stages of moyamoya disease.     

Sickle cell anemia with moyamoya disease: outcomes after EDAS procedure

Moyamoya disease is a relatively uncommon neurovascular complication of sickle cell anemia. We report a case series of six patients with sickle cell anemia who developed moyamoya disease and underwent encephaloduroarteriosynangiosis procedures. These six patients presented with either cerebrovascular accidents, transient ischemic attacks, or seizures, and subsequent magnetic resonance imaging scans were suggestive of moyamoya-like changes in the cerebral vasculature. Conventional cerebral angiography was used to confirm the diagnosis in all six patients. Four of six patients manifested a cerebrovascular accident before surgery, and two of these patients were compliant on a transfusion protocol at the time of their cerebrovascular accident. Bilateral (n = 4) or unilateral (n = 2) encephaloduroarteriosynangiosis procedures were performed without any complications. The patient who was stroke-free preoperatively had a cerebrovascular accident 2 weeks after the procedure; otherwise, all patients have remained free of neurovascular complications with an average follow-up of 33 months. Collateral anastomoses between external and internal carotid arteries were established by magnetic resonance angiography in three patients. The encephaloduroarteriosynangiosis procedure is a safe and effective treatment option in patients with sickle cell anemia who develop moyamoya disease.     

Accelerated intracranial occlusive disease, oral contraceptives, and cigarette use.

We report clinical and angiographic features of accelerated intracranial occlusive disease resembling moyamoya vasculopathy in five young women who used oral contraceptives (OCs) and smoked cigarettes, but generally had no other obvious risk factors for cerebrovascular disease. Three women had been on OCs for at least 4 years, one woman each had been on OCs for 3 months and for 2 weeks. All five women had smoked cigarettes for at least eight pack-years. Intermittent and progressive multifocal cognitive, visual, motor, or sensory hemispheric symptoms and signs developed in all. All patients developed strokes, four preceded by transient ischemic attacks. Cerebral angiography demonstrated bilateral supraclinoid internal carotid artery stenosis in four patients and proximal posterior cerebral artery stenosis in one. Additional features included rete mirabile, telangiectasias, prominent lenticulostriate collaterals, and multifocal distal cerebral branch occlusions. Three had mild abnormalities of serum fibrinogen, antinuclear antibody, erythrocyte sedimentation rate, or CSF IgG. After discontinuing OCs and reducing cigarette use, four women have not had further strokes over a mean follow-up of approximately 5 years. In certain young women, clinical and angiographic features resembling moyamoya may develop with the use of OCs and cigarettes. We speculate that an immunologically mediated vasculopathy may explain, in part, this unusual cerebrovascular syndrome in otherwise healthy young women.     

A case of internal carotid artery occlusion successfully treated by encephalo-duro-arterio-synangiosis

In many cases, intracranial occlusive strokes in children are treated symptomatically, with a diagnosis of acute infantile hemiplegia. This is because angiography is more difficult in children and, even if occlusive cerebral arterial disease is diagnosed, there is no definite therapeutic procedure. A case is reported of left internal carotid artery occlusion presenting with acute infantile hemiplegia and followed by repeated transient ischemic attacks. Encephalo-duro-arterio-synangiosis — developed as an operation for moyamoya disease — was performed on this patient, resulting in a marked revascularization of the brain in 8 postoperative months with good improvement in symptoms. This suggests that the operation may be effective in chronic cerebral ischemic diseases other than moyamoya disease.     

Stroke in neonates with cardiac right-to-left shunt.

Neonatal focal cerebral arterial infarction has been rarely reported in the literature, in contrast to the watershed infarctions, which are common entities among asphyxiated infants. In neonatal postmortem series, thromboembolism was the commonest cause of cerebral arterial occlusion; the source of emboli was associated to different risk factors. Our four cases are the first alive patients reported with congenital heart disease and right-to-left shunt, who suffered a cerebral infarct with its clinical neurological correlates in the neonatal period. We assume that the most probable mechanism was paradoxical embolism, once pulmonary filter is obviated as a result of the altered hemodynamics in these patients. Our data demonstrate the value of ultrasound scanning for assessment of focal cerebral ischemic lesions. Thus, although abnormal neurological signs in this particular group of infants could be attributed to hypoxemia or specific treatments as prostaglandins, we suggest routine cerebral ultrasounds in neonates with congenital heart disease and neurological disabilities, as early complications could be not so infrequent.     

数字减影血管造影对缺血性脑血管病诊断及治疗的意义

目的:探讨数字减影血管造影检查(DSA)对缺血性脑血管病血管病变诊断的意义。方法:选取有脑缺血症状的经TCD检查发现血管狭窄的21例病人,行DSA检查。结果:颈内动脉系统TIA患者3例,DSA证实为大脑中动脉狭窄2例,烟雾病1例,椎基底动脉供血不足8例中双侧椎动脉发育不全1例,一侧或双侧椎动脉狭窄5例,锁骨下动脉盗血2例。8例脑梗塞患者中已经出现一侧颈内动脉闭塞的有两例,但均已出现侧枝循环的建立,另6例均为颈内动脉或大脑中动脉的狭窄,2例脑干梗塞患者均有椎动脉的狭窄。结论:数字减影血管造影是评价头颈部血管狭窄、闭塞和选择治疗方案的金标准,它对缺血性脑血管病的进一步治疗起着重要的作用。     

甲状腺功能亢进症合并烟雾综合征

目的 分析和探讨经颅多普勒超声（TCD）筛查的甲状腺功能亢进症（甲亢）合并烟雾综合征的临床和 血管病变特征。 方法 总结北京协和医院和解放军307医院2000～2007年经TCD筛查诊断烟雾综合征患者13例，8例经 磁共振血管成像（MRA）、5例经数字减影血管造影（DSA）明确诊断；所有患者经协和医院内分泌科确 诊为甲亢，且甲状腺球蛋白抗体（TGAb）和髓过氧化物酶抗体（TPOAb）高，除外血管狭窄的其他常见 原因。 结果 13例患者中，男1例，女12例；11例表现为缺血性卒中（2例合并不自主运动），1例仅表现为不自 主运动，1例以头晕为临床主诉，后2例经TCD筛查发现血管狭窄。血管病变分布：11例为典型的颈内动脉 终末端（TICA）、大脑中动脉（MCA）、大脑前动脉（ACA）狭窄或闭塞，1例为颈内动脉虹吸段狭窄，1例 为双侧颈内动脉起始严重狭窄或闭塞。2例患者同时合并大脑后动脉（PCA）狭窄。随访发现，1例患者因 甲亢控制不佳复查TCD血管病变加重；而1例甲状腺功能稳定，缺血临床症状明显改善。4例患者行颞浅 动脉－大脑中动脉（MCA）血管融通术，术后缺血发作减少。 结论 TCD的临床应用使越来越多的甲亢合并烟雾综合征得以诊断；烟雾综合征患者常规行甲状腺 功能筛查十分必要；血管成形术可能是预防缺血性卒中的有效方法之一。     

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.     

Reduced hypercapnic vasoreactivity in moyamoya disease

We measured cerebral perfusion at rest and in response to CO2 in eight patients with moyamoya disease (MMD), using the 133xenon inhalation method to determine the effect of large-vessel occlusive disease on vasoreactivity. We studied three other groups for comparison, including four with bilateral internal carotid artery occlusions (BICAO), 11 with unilateral carotid occlusion (UICAO), and six with unilateral middle cerebral artery stem occlusion (UMCAO). Resting flows appeared to correlate with the severity of occlusive disease overall. Normocapnic perfusion was lowest in the group with BICAO and decreased in proportion to the degree of contralateral stenosis in the group with UICAO. Hypercapnic perfusion correlated with the apparent adequacy of angiographic collaterals. Reactivity was lowest in the MMD group (0.79%/mm Hg) whose collateral supply was limited to leptomeningeal anastomosis from the posterior cerebral artery, but highest in the patients with BICAO (2.72%/mm Hg), each of whom showed excellent posterior communicating artery flow. The clinical course of the MMD group was compatible with the syndrome of perfusion insufficiency with repeated ischemic attacks or a saltatory progression of an ischemic deficit; CT showed infarction in the borderzone territory. These results suggest that a severely reduced hypercapnic response may help to identify patients with ischemic syndromes due to perfusion failure in the borderzones, as in MMD.     

Differentiating subtotal carotid artery stenoses from occlusions by colour-coded duplex sonography

During a 9-month period the carotid arteries of 2420 consecutive patients were investigated by conventional Doppler and duplex ultrasonography as well as by colour-coded duplex sonography. Of 186 internal carotid arteries showing a diameter reduction at the bifurcation level of 95% or more by conventional techniques, 131 underwent X-ray angiography which revealed a subtotal stenosis in 25 and an occlusion in 106 cases. Using a total of ten criteria for describing the colour-coded duplex findings, the distal colour filling, a combination of three single criteria, could be found in all subtotal stenoses and none of the occlusions. Distal colour filling was diagnosed if a colour signal was present for a length of at least 1.5 cm directly behind an assumed stenosis comprising the whole area between the vessel walls. Our results suggest that non-invasive colour-coded duplex sonography is superior to conventional Doppler and duplex techniques and comparable to invasive X-ray angiography in differentiating extracranial subtotal carotid artery stenoses from occlusions.     

Brain damage after open heart surgery in patients with acute cardioembolic stroke

We evaluated 14 patients with acute cardiogenic embolism who underwent open heart surgery soon after the onset to determine the cerebral and cardiac factors that influence neurologic outcome. The mean interval from onset of cerebral embolism to surgery was 5.3 (range 1-16) days. Five of the 14 patients had vegetations from infective endocarditis (including prosthetic valve endocarditis) as embolic sources, eight had intracardiac thrombi, and one had atrial myxoma. The diagnosed site of infarction before surgery was based on computed tomographic and/or angiographic findings. Of the 14 patients, four had infarcts due to major artery occlusion, seven due to cortical branch occlusion, and two due to perforating artery occlusion; one patient presented with a transient ischemic attack without computed tomographic abnormalities. Ten patients (71%) showed no clinical aggravation after open heart surgery; however, two patients died of massive cerebral hemorrhage, one died of deterioration of brain edema, and another became comatose from midbrain hemorrhage immediately after surgery. The four patients with clinical aggravation comprised three with septic embolism and one with aseptic occlusion of a major artery. From these results, infective endocarditis and a large infarct appear to be possible aggravating factors when patients with recent cerebral embolism undergo open heart surgery.     

Transcranial doppler CO2 test for the detection of hemodynamically critical carotid artery stenoses and occlusions

Summary Cerebral CO₂-reactivity was tested by transcranial Doppler sonography (Doppler CO₂ test) in 232 patients. Time averaged flow velocity in the middle cerebral artery at the 40 mm Hg blood PCO₂ level was taken as a reference point, and the relative increase of flow in hypercapnia of 46.5 mm Hg pCO₂ was defined as Normalized Autoregulatory Response (NAR). A total of 82 patients with no evidence of cerebrovascular disease gave normal values for NAR (23.2 ± 5.2 SD). In 150 patients with 233 stenoses and occlusions of the internal carotid artery NAR was significantly decreased in highergrade stenoses (P = 0.01 for 80% diameter reduction, P < 10^–6 for 90% or more). In such stenoses, patients with NAR < 14 had suffered more frequently (P < 0.01) from ipsilateral transient ischemic attacks and/or stroke during the previous 6 months than patients with normal NAR. Preoperative NAR < 14 always improved to normal values following carotid surgery, while preoperative NAR > 19 remained unchanged (60 cases). The transcranial Doppler CO₂ test is thought to be a reliable noninvasive method to detect hemodynamically critical carotid stenoses and occlusions. This may be of interest in selecting patients for superficial temporal artery-middle cerebral artery bypass and carotid surgery. For practical use 4 categories of NAR are suggested.