A Vessel Wall MRI Investigation in Patients With Moyamoya or Quasi-Moyamoya Disease: Diagnosis, Features, and Outcomes.

BACKGROUND AND PURPOSE: None of the previous studies have investigated the pathologic authenticity of affected arteries in moyamoya disease (MMD) and Quasi-MMD diagnosed by angiography. This study aimed to confirm the angiographic diagnosis of moyamoya as well as investigate the pathologic mechanisms in angiographically proven MMD and Quasi-MMD using high-resolution magnetic resonance imaging (MRI) in a large sample. METHODS: We prospectively studied 116 patients who had angiographically proven MMD and Quasi-MMD. Each affected internal carotid artery, and middle cerebral artery was independently evaluated. In addition, clinical features and postoperative outcomes were compared between hemispheres with MMD and moyamoya syndrome (MMS). RESULTS: Among 116 patients analyzed, 88 and 22 patients had angiographically proven MMD and Quasi-MMD, respectively. high-resolution magnetic resonance imaging confirmed bilateral MMD in 73 (83.0%) patients, 1 hemisphere with MMD and the other with intracranial atherosclerotic disease (ICAD) in 10 (11.4%) patients, and bilateral hemispheres with different vasculopathies in 5 (5.7%) patients. Detailed analysis of 204 affected hemispheres showed that several combinations of different vasculopathies were observed in the internal carotid artery and middle cerebral artery of the same hemisphere, such as ICAD-ICAD, ICAD-MMD, dissection-ICAD, and dissection-MMD. Hemispheres were assigned to MMD and MMS groups according to their vasculopathies. Transient ischemic attack occurred more frequently in hemispheres with MMD (48.1% versus 21.1%, P =0.024), whereas symptomatic ischemia was more common in hemispheres with MMS (57.9% versus 24.9%, P =0.002). However, postoperative cerebral infarction, symptom improvement and neo-formative collaterals showed no significant difference between hemispheres with MMD and MMS ( P >0.05). CONCLUSIONS: Patients with angiographically proven MMD or Quasi-MMD needed more accurate evaluation combined with high-resolution magnetic resonance imaging. Highly selected patients with MMS might also obtain benefits from surgical revascularization.

Different aspects of cognitive function in adult patients with moyamoya disease and its clinical subtypes.

OBJECTIVE: Although a few reports suggested that cognitive function impairment could be found in adult patients with moyamoya disease (MMD), there were still many aspects that are unclear. The aim of our study was to assess the cognitive function of adult patients with MMD and its clinical subtypes. METHODS: 49 patients with MMD and 23 healthy controls were asked to take cognitive function tests. Cognitive function tests included IQ, prospective memory (PM), immediate memory (IM), verbal fluency (VF), visual breadth, attention, retrospective memory (RM), Stroop test, Wisconsin Card Sorting Test, Trail-Making Test Part A (TMT-A) and Continuous Performance Test (CPT). Independent t-analysis, one-way analysis of variance and Pearson correlation were used to seek for differences between subgroups and the correlation between cognitive variables. RESULTS: Compared with healthy controls, adult patients with MMD had a comprehensive cognitive impairment, including IQ, PM, VF, attention, RM, Stroop, CPT and TMT-A, with more serious impairment in PM and attention. PM and RM were separated, indicating that they were independent of each other. Pattern of attention was significantly different from healthy controls. Female patients were better than male patients, where significant differences in PM, IM, Stroop and WCST could be found. The haemorrhagic patients exhibited poorer in the dimension of PM and RM than the ischaemic. The headache subtype exhibited poorer than healthy controls. PM, RM, attention and executive function were moderately correlated with each other. CONCLUSIONS: Adult patients with MMD had a wide range of cognitive impairment with more serious impairment in memory and attention. Differences in cognitive function existed between the different subtypes of adult MMD.

Supraorbital keyhole versus pterional craniotomies for ruptured anterior communicating artery aneurysms: a propensity score-matched analysis.

The safety and efficacy of the supraorbital keyhole approach for aneurysm surgery have not been well researched through a high-quality controlled study. The objective of the study was to compare the safety and efficacy of the supraorbital and pterional approaches for ruptured anterior communicating aneurysm (AComAn). A total of 140 patients, with 70 patients in each group, were enrolled after 1:1 propensity score matching. Clinical variables, postoperative complications, and long-term outcomes were retrospectively compared. Baseline characteristics were equivalent between the two groups. Significantly shorter operative time and less intraoperative blood loss were observed in the supraorbital group compared to the pterional group (141.9 min vs. 184.5 min, P < 0.001; 160.4 ml vs. 250.7 ml, P = 0.008). The incidence of intraoperative aneurysm rupture was similar between the groups (20% vs. 18.6%, P = 0.830). The rate of procedural complications involving subdural hematoma and intracranial infection was lower in patients treated through the supraorbital (10.0%) vs. the pterional approach (32.9%, P < 0.001), but no significant difference was observed for the incidence of ischemic events (15.7% vs. 18.6%, P = 0.654). Within a median 33.4-month (range, 11-67 months) follow-up, a similar proportion of patients achieved a favorable outcome (Glasgow Outcome Scale IV or V) across the two groups (83.6% vs. 80.0%, P = 0.285), while better cosmetic results were observed in the supraorbital group (94.0%) vs. the pterional group (86.2%, P = 0.129). According to our results, we recommend the keyhole approach for AComAn surgery for neurosurgeons who have gained sufficient experience with this technique due to its advantages over the pterional approach.

Cerebral Revascularization Accelerates the Angiographic Staging Progression of the Operated Hemisphere in a Pediatric Patient With Moyamoya Disease.

BACKGROUND AND OBJECTIVE: Angiographic staging progression in the operated hemisphere of patient with moyamoya disease (MMD) is a common phenomenon that neurosurgeons may encounter. However, few studies have been carried out to demonstrate the correlation between the operation and angiographic staging progression. This study aimed to reveal whether cerebral revascularization would affect the stage progression in patient with MMD. METHODS: A total of 20 pediatric patients with bilateral MMD were included in this study. All enrolled patients were at the similar Suzuki angiographic staging on bilateral hemispheres and cerebral revascularization was performed in unilateral hemisphere. Angiographic examination was performed in the first year after the operation to evaluate the progression of the lesions. RESULTS: Cerebral revascularizations including direct bypass or encephaloduroarteriosynangiosis were performed in 20 hemispheres. During the follow-up, the incidence of stage progression in the operated hemisphere was significantly higher than in the contralateral side (80.0% versus 20.0%, respectively; P = 0.036) and the interval of disease progression was significantly shorter in the operated side than in the contralateral side (mean interval time, 7.3 versus 10 months). Earlier Suzuki stage on hemisphere represented faster pace of stage progression compared with server Suzuki stage (OR = -0.612, P = 0.004), while neoformative collaterals had not significant correlation with the progression pace. The leptomeningeal collaterals from the posterior circulation decreased in almost all operated hemisphere, while gradually increasing in the contralateral hemisphere. Symptoms were improved in all patients after operation. CONCLUSION: Cerebral revascularization would significantly accelerate the angiographic staging progression on the treated hemisphere, while it would not cause the deterioration of the patient's condition. The progression pace was associated with Suzuki stage.

Clinical Features, Surgical Treatment, and Long-Term Outcome of a Multicenter Cohort of Pediatric Moyamoya.

Objective: This study aims to investigate the clinical features, long-term outcomes, and prognostic predictors of a multicenter cohort of children with moyamoya disease. Methods: A series of 303 consecutive pediatric moyamoya disease (MMD) patients were screened in the present study. The clinical characteristics were retrospectively collected, and long-term outcomes was evaluated. Furthermore, logistic regression analyses were performed to determine the prognostic predictors for the clinical outcome. Results: The mean onset age at diagnosis was 9.4 years old. The gender ratio (girl-to-boy ratio) was 1.1:1.0. Among these 303 patients, 13 patients underwent different surgical modalities in bilateral hemispheres, while eight patients failed to follow-up, and were excluded. Therefore, a total of 282 patients were analyzed. Among these patients, 17 patients underwent combined bypass (CB), 47 patients underwent direct bypass (DB), 150 patients underwent indirect bypass (IB), and 68 patients underwent conservative treatment. Furthermore, recurrent stroke events were observed in 35 patients (12.4%). The Kaplan-Meier analysis demonstrated that there was no significant difference in either ischemia or hemorrhage-free time among the different surgical modalities (P = 0.67 and 0.79, respectively). Furthermore, longer ischemia-free time was observed in the surgical group, when compared to the conservative group (P < 0.01). In addition, 82.7% (177/214) of patients who underwent surgical treatment obtained good outcomes (mRS 0-1), which were significantly higher than the rate of patients who underwent conservative treatment (52.9%, 36/68; P < 0.01). The rate of patients with improved symptoms was also significantly different (93.0 vs. 16.2%, P < 0.01). However, no significant difference was observed in the rate of good outcomes, disability, and improved symptoms among the different surgical modalities. The logistic regression analyses revealed that postoperative ischemic events were the only risk factor associated with unfavorable clinical outcome (OR:3.463; 95% CI:1.436-8.351; P < 0.01). Conclusion: CB, DB, and IB might have similar effects on long-term clinical outcome in pediatric MMD. However, surgical revascularization is superior, when compared to conservative treatment. Furthermore, postoperative ischemic events were confirmed as potential prognostic factors associated with unfavorable clinical outcome.

Changing Ischemic Lesion Patterns and Hemodynamics of the Posterior Cerebral Artery in Moyamoya Disease.

OBJECTIVE: The aim of this study was to determine how hemodynamics of the posterior cerebral artery (PCA) are associated with cerebral ischemic lesions in moyamoya disease (MMD). METHODS: Thirty-six patients with ischemic MMD (Suzuki grade IV-V) were retrospectively analyzed. Hemodynamic parameters of the PCA were measured by transcranial color-coded sonography. We classified the range of ischemic lesions into 3 grades and perfusion levels into 3 grades according to computed tomography (CT) results. PCA steno-occlusion and leptomeningeal collaterals were confirmed by digital subtraction angiography. Ultrasonographic parameters in the PCA were compared with these radiographic findings. RESULTS: The velocity in the involved PCA (mean flow velocity [MFV] median, 42.00 [range, 34.50-58.00] cm/s) was significantly lower than that in the normal PCA (MFV median, 95.00 [range, 76.50-119.50] cm/s) (P < .001). The velocity in the PCA increased significantly as the leptomeningeal collateral stage advanced (MFV stage 1: median, 38.50 [range, 29.75-63.50] cm/s; stage 2: median, 55.00 [range, 44.00-96.00] cm/s; stage 3: median, 94.00 [range, 54.00-118.25] cm/s; stage 4: median, 85.50 [range, 70.50-117.75] cm/s, respectively) (P < .05). Decreased PCA velocities were associated with a larger ischemic area on CT (P ≤ .001). PCA velocity had no correlation with CT perfusion level of the temporal and frontal lobes. PCA velocity had significant correlations with perfusion level in the occipital (P < .001) and parietal lobes (P < .05). CONCLUSIONS: Our results suggest ischemic lesion patterns (as demonstrated on CT imaging) are associated with PCA velocity measurements in the advanced stage of MMD. Thus, monitoring PCA velocity in patients with advanced MMD may provide additional information to assist in managing these patients.

Management of Residual and Recurrent Aneurysms After Clipping or Coiling: Clinical Characteristics, Treatments, and Follow-Up Outcomes.

BACKGROUND: Recurrent intracranial aneurysms (RAs) remain a daunting challenge for neurosurgeons. This study aimed to explore a potential optimal management strategy of RAs by reviewing the characteristics and management outcomes of 117 RAs. METHODS: A total of 117 patients with RAs were treated in a single neurosurgical center from January 2011 to January 2017. The demographic and angiographic characteristics of the patients, treatment approaches, and follow-up outcomes were evaluated. RESULTS: Of the 117 patients with RAs, 16 (13.7%) and 101 (86.3%) initially underwent microsurgical clipping and endovascular coiling, respectively. Coil embolization was used in 75 cases, microsurgical clipping was used in 32 cases, and conservative treatment occurred in 10 cases. Complete clipping was achieved in all 32 aneurysms by microsurgery, and remnants were observed in 25 aneurysms after coiling (33.3%, P < 0.001). Operation-related cerebral infarction occurred in 4 cases (12.5%) with complex and large RA in the clipping group and in 1.3% (1/75) of patients treated with coiling (P = 0.027). Follow-up found similar favorable outcomes in patients after coiling, clipping, and conservative treatment (90.3% vs. 86.7% vs. 80%, respectively; P = 0.711). Follow-up rates of recurrence were significantly higher in the coiling group than the clipping group (26% vs. 0%, respectively; P = 0.003). CONCLUSIONS: The follow-up outcomes appeared to be acceptable and comparable between the 2 groups. However, in large or giant recurrent aneurysms, sound judgment and the careful selection of treatment are strongly suggested because direct microsurgery has a higher morbidity, even in experienced hands, whereas endovascular coiling is complicated with a higher incomplete occlusion rate.

Management of recurrent intracranial aneurysms after coil embolization: a novel classification scheme based on angiography.

OBJECTIVERecurrent aneurysms after coil embolization remain a challenging issue. The goal of the present study was to report the authors' experience with recurrent aneurysms after coil embolization and to discuss the radiographic classification scheme and recommended management strategy.METHODSAneurysm treatments from a single institution over a 6-year period were retrospectively reviewed. Ninety-seven aneurysms that recurred after initial coiling were managed during the study period. Recurrent aneurysms were classified into the following 5 types based on their angiographic characteristics: I, pure recanalization inside the aneurysm sac; II, pure coil compaction without aneurysm growth; III, new aneurysm neck formed without coil compaction; IV, new aneurysm neck formed with coil compaction; and V, newly formed aneurysm neck and sac.RESULTSAneurysm recurrences resulted in rehemorrhages in 6 cases (6.2%) of type III-V aneurysms, but in none of type I-II aneurysms. There was a significantly higher proportion of ophthalmic artery aneurysms and complex internal carotid artery aneurysms presenting as types I and II than presented as the other 3 types (63.3% vs 16.4%, p < 0.001). In contrast, for posterior communicating artery aneurysms and anterior communicating artery aneurysms, a higher proportion of type III-V aneurysms was observed than for the other 2 types, but without a significant difference in the multivariate model (56.7% vs 23.3%). In addition, giant (> 25 mm) aneurysms were more common among type I and II lesions than among type III and IV aneurysms (36.7% vs 9.0%, p = 0.001), which exhibited a higher proportion of small (< 10 mm) lesions (65.7% vs 13.3%, p < 0.001). A single reembolization procedure was sufficient to occlude 80.0% of type I recurrences and 83.3% of type II recurrences from coil compaction but only 65.6% of type III-V recurrences from aneurysm regrowth.CONCLUSIONSAneurysm size and location represent the determining factors of the angiographic recurrence types. Type I and II recurrences were safely treated by reembolization, whereas type III-V recurrences may be best managed surgically when technically feasible.

Novel alternatively spliced isoforms of MEF2A and their mRNA expression patterns in pigs.

The present study aimed to identify the alternatively spliced isoforms of pig MEF2A gene and to determine theirmRNA expression patterns. Four alternatively spliced isoforms of pig MEF2A gene (i.e. MEF2A1, MEF2A2, MEF2A3 and MEF2A4) were cloned according to the results of transcriptome sequencing. The fifth to eighth exons of MEF2A1 were normally spliced. In MEF2A2, the fifth exon was missing; the sixth exon had an extra 138 bp at its 5' end, and the seventh exon had an extra 102 bp at its 3' end. In MEF2A3, the fifth exon was missing, and the sixth exon had an additional 138 bp at its 5' end. In MEF2A4, the seventh exon had an extra 102 bp at its 3' end. Quantitative real-time polymerase chain reaction (qPCR) analysis indicated that the expression profiles of the four alternatively spliced transcripts in the longissimus dorsi differed between the Mashen and Large White pigs. MEF2A1 and MEF2A2 expression levels were the highest at 90 days of age and lowest at 180 days of age. MEF2A3 and MEF2A4 expression levels increased with age (in days). The four alternatively spliced isoforms of MEF2A were also expressed in the small intestine, cerebellum, pancreas, heart and lung. The discovery of new alternatively spliced transcripts of the MEF2A gene may be utilized in understanding its biological functions.

Surgical management of giant intrapetrous internal carotid aneurysm presenting with coil exposure after endovascular treatment.

Giant intrapetrous internal carotid aneurysms (petrous ICA aneurysm) are rare. A giant petrous ICA aneurysm presenting with otorrhagia and coil exposure to the external auditory meatus (EAM) after endovascular treatment has never been documented before. The authors report here a case of successful surgical trapping with bypass intervention of a giant petrous ICA aneurysm presenting with coil exposure after endovascular treatment. A 58-year-old man presented with persistent otorrhagia having been admitted to our hospital because of the recurrence of a giant petrous ICA aneurysm after repeated embolization treatments with coils. An electronic otoscope examination demonstrated that a piece of coil escaped into his right EAM. After multidisciplinary consultation, an extracranial-intracranial (EC-IC) bypass with ICA occlusion and coil removal with a closed EAM filling were performed in stages. The patient recovered quickly without any neurological deficits. A digital subtraction angiography confirmed the absence of the aneurysm and patency of the bypass graft.

Carotid endarterectomy for treatment of carotid in-stent restenosis: long-term follow-up results and surgery experiences from one single centre.

OBJECTIVE: Few studies have reported the surgical treatment of carotid in-stent restenosis (ISR), more data and longer follow-up are needed. We describe the surgical treatment of ISR by standard carotid endarterectomy (CEA) with stent removal, including long-term follow-up in 10 patients from our centre. METHODS: Ten patients from our centre who underwent CEA with stent removal for ISR were retrospectively analysed, including nine symptomatic and one asymptomatic ISR of at least 70% with mean age 67.3, the median time between carotid artery stenting and CEA was 17 months (range, 2-54 months). RESULTS: Standard CEA with stent removal was performed in all 10 patients without much technical difficulty (9 male and 1 female, mean age 67.3). Two cases were performed in hybrid operation room. There were a total of three complications that happened in three patients (30%) respectively. An asymptomatic dissecting aneurysm was formed on the petrous internal carotid artery in one patient who was followed up without intervention. In the second case, dissection occurred in the arterial wall distal to the site of the stent after stent removal revealed by intraoperative angiography, and another stent was implanted. The patient sustained temporary hypoglossal nerve dysfunction postoperatively. The third patient suffered cerebral hyperperfusion with complete recovery when discharged. No neurological complications occurred in other seven patients. After follow-up of 25 months (range, 11-54 months), one patient died of rectal cancer without ischaemic attack and restenosis 4 years postoperation; in one patient occurred recurrent symptomatic restenosis (90%) 1 year later; all other patients remained asymptomatic and without recurrent restenosis (>50%) by follow-up carotid ultrasound or CT angiography. CONCLUSION: It seems that CEA with stent removal is a reasonable choice, by experienced hand, for symptomatic ISR with higher but acceptable complications. The indication of stent removal for asymptomatic ISR needs further observation.

Role of Ring Finger Protein 213 in Moyamoya Disease.

OBJECTIVE: The aim of this study was to help people comprehensively understand the research advances related to ring finger protein 213 (RNF213) in moyamoya disease (MMD) and to understand the disease at the molecular level to provide a new perspective of the diagnosis of the disease. DATA SOURCES: This review was based on data in articles published between 2005 and 2015 that were retrieved from the PubMed database. The search terms included RNF213, MMD, intracranial major artery stenosis /occlusion (ICASO), genotype, phenotype, mutant and variants, and the combinations of these terms. STUDY SELECTION: Articles related to MMD and RNF213 were selected for review, and we also reviewed publications related to ICASO. RESULTS: RNF213 is not only associated with MMD but also associated with intracranial major artery stenosis. In addition, RNF213 variants exhibit apparent ethnic diversity; specifically, the c.14576G>A variant is mainly detected in Korean, Chinese, and Japanese populations, particularly the latter population. The genotypes of RNF213 correlate with the phenotypes of MMD; for example, the homozygous c.14576G>A variant is associated with early-onset, severe symptoms, and an unfavorable prognosis. Furthermore, the RNF213 c.14576G>A variant should be considered during the diagnosis of MMD because no patients with quasi-MMD have been reported to carry the RNF213 c.14576G>A variant whereas 66 of 78 patients with definite MMD have been found to carry this variant. CONCLUSIONS: The growing literature demonstrates that MMD is primarily caused by the synergy of genetic and environmental factors, and unknown genetic modifiers might play roles in the etiology of MMD. Further research should be conducted to clarify the pathogenic mechanism of MMD.

More Precise Imaging Analysis and Diagnosis of Moyamoya Disease and Moyamoya Syndrome Using High-Resolution Magnetic Resonance Imaging.

BACKGROUND: The diagnosis of moyamoya disease (MMD) is often uncertain. Moyamoya syndrome (MMS) is often misdiagnosed as MMD. High-resolution magnetic resonance imaging (HR-MRI) enables vessel wall assessment to obtain more precise diagnoses. The aim of this study was to determine the true etiologies of arterial steno-occlusion in patients with an angiographic diagnosis of MMD or MMS using HR-MRI. METHODS: HR-MRI was performed in 21 adult patients with angiographically proven MMD or MMS. A definite diagnosis was based on the HR-MRI findings. The diagnoses made via the 2 different imaging technologies were compared, and significant findings were analyzed. RESULTS: A total of 21 patients were enrolled, including 7 patients with angiographically proven MMD and 14 patients with angiographically proven MMS. Among the 7 patients with MMD, HR-MRI confirmed the diagnosis of MMD in 6; the remaining patient was considered to have atherosclerosis in the bilateral distal internal carotid arteries (ICAs) and the left middle cerebral artery. Among the 14 patients with MMS, HR-MRI confirmed MMD in 6 patients (including 2 patients with unilateral MMD), atherosclerosis in 5 patients (including 3 patients with bilateral atherosclerosis and 2 with unilateral atherosclerosis), arterial dissection of the left ICA in 1 patient, and MMD in the left cerebral hemisphere with atherosclerosis in the right hemisphere in 2 patients. CONCLUSIONS: Differentiating MMD from MMS is difficult in certain situations, and HR-MRI may help provide a more in-depth understanding of MMD and MMS, thereby achieving a more reliable diagnosis.

High-resolution Magnetic Resonance Imaging of Moyamoya Disease.

OBJECTIVE: To introduce the imaging characteristics of moyamoya disease (MMD) using high-resolution magnetic resonance imaging (HR-MRI) and to discuss the role of HR-MRI in differentiating MMD from other intracranial artery diseases, especially intracranial atherosclerotic disease (ICAD). DATA SOURCES: This review was based on the data in articles published between 2005 and 2015, which were obtained from PubMed. The keywords included HR-MRI, MMD, ICAD, and intracranial artery diseases. STUDY SELECTION: Articles related to HR-MRI for MMD or other intracranial artery diseases were selected for review. RESULTS: There are differences between the characteristic patterns of HR-MRI in MMD and ICAD. MMD is associated with inward remodeling, smaller outer diameters, concentric occlusive lesions and homogeneous signal intensity, while ICAD is more likely to be associated with outward remodeling, normal outer diameters, eccentric occlusive lesions, and heterogeneous signal intensity. Other intracranial artery diseases, such as dissection and vasculitis, also have distinctive characteristics in HR-MRI. HR-MRI may become a useful tool for the differential diagnosis of MMD in the future. CONCLUSIONS: HR-MRI of MMD provides a more in-depth understanding of MMD, and it is helpful in evaluating pathological changes in the vessel wall and in differentiating MMD from other intracranial artery steno-occlusive diseases, particularly ICAD.