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Tao Yu, Xingwen Sun, Yan You, Jie Chen, Jun-mei Wang, Shuo Wang, Ning Lin, Buqing Liang and Jizong Zhao

Brain capillary telangiectasias (BCTs) are usually small and benign with a predilection in the pons and basal ganglion. Reports of large and symptomatic BCTs are rare. Large BCTs have a much higher risk of causing uncontrolled bleeding and severe neurological defects, and they can be fatal if left untreated. Therefore, large BCTs should be managed with special caution. Because of the lack of reports, diagnosis of large BCTs has been difficult. Strategies of management are undefined for large or giant BCTs.

The current study presents 5 cases of giant and large BCTs. To the authors’ knowledge, this is the largest series of this disease ever reported. Radiological findings, histopathological characteristics, clinical presentations, and surgical management were analyzed in 5 symptomatic, unusually large BCTs (mean diameter 5.06 cm, range 1.8–8 cm).

Four patients presented with focal or generalized seizures, and 1 patient presented with transient vision loss attributed to the lesions. Gross-total resection of the lesion was achieved in all patients. After surgery, the 4 patients with seizures were symptom free for follow-up periods varying from more than 1 to 5 years with no additional neurological deficits.

The unique location, radiological characteristics, and clinical course suggest that giant BCTs could be a different entity from small BCTs. Surgery might be a good option for treatment of patients with intractable neurological symptoms, especially in those with surgically accessible locations. Complete removal would be anticipated to provide relief of the symptoms without causing new neurological deficits.

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Meng Zhao, Xiaofeng Deng, Dong Zhang, Shuo Wang, Yan Zhang, Rong Wang and Jizong Zhao

OBJECTIVE

The risk factors and clinical significance of postoperative complications in moyamoya disease are still unclear. The aim of this study was to investigate the predictors of postoperative complications in moyamoya disease and examine the impact of complications on outcomes.

METHODS

The authors reviewed consecutive cases involving adult moyamoya disease patients who underwent indirect, direct, or combined bypass surgery in their hospital between 2009 and 2015. Preoperative clinical characteristics and radiographic features were recorded. Postoperative complications within 14 days after surgery were examined. Multivariate logistic regression analyses were performed to identify the risk factors for either postoperative ischemia or postoperative cerebral hyperperfusion. Outcome data, including recurrent strokes and neurological status (modified Rankin Scale [mRS]) during follow-up, were collected. Outcomes were compared between patients who had complications with those without complications, using propensity-score analysis to account for between-group differences in baseline characteristics.

RESULTS

A total of 500 patients (610 hemispheres) were included in this study. Postoperative complications were observed in 74 operations (12.1%), including new postoperative ischemia in 30 cases (4.9%), hyperperfusion in 27 (4.4%), impaired wound healing in 12 (2.0%), and subdural effusion in 6 (1.0%). The complication rates for different surgery types were as follows: 12.6% (n = 25) for indirect bypass, 12.7% (n = 37) for direct bypass, and 10.0% (n = 12) for combined bypass (p = 0.726). Postoperative ischemic complications occurred in 30 hemispheres (4.9%) in 30 different patients, and postoperative symptomatic hyperperfusion occurred after 27 procedures (4.4%). Advanced Suzuki stage (OR 1.669, 95% CI 1.059–2.632, p = 0.027) and preoperative ischemic presentation (OR 5.845, 95% CI 1.654–20.653, p = 0.006) were significantly associated with postoperative ischemia. Preoperative ischemic presentation (OR 5.73, 95% CI 1.27–25.88, p = 0.023) and admission modified Rankin Scale (mRS) score (OR 1.81, 95% CI 1.06–3.10, p = 0.031) were significantly associated with symptomatic postoperative cerebral hyperperfusion syndrome (CHS). Compared with patients without postoperative complications, patients who experienced any postoperative complications had longer hospital stays and worse mRS scores at discharge (both p < 0.0001). At the final follow-up, no significant differences in functional disability (mRS score 3–6, 11.9% vs 4.5%, p = 0.116) and future stroke events (p = 0.513) between the 2 groups were detected.

CONCLUSIONS

Advanced Suzuki stage and preoperative ischemic presentation were independent risk factors for postoperative ischemia; the mRS score on admission and preoperative ischemic presentation were independently associated with postoperative CHS. Although patients with postoperative complications had worse neurological status at discharge, postoperative complications had no associations with future stroke events or functional disability during follow-up.

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Xing-ju Liu, Dong Zhang, Shuo Wang, Yuan-li Zhao, Mario Teo, Rong Wang, Yong Cao, Xun Ye, Shuai Kang and Ji-Zong Zhao

OBJECT

The aim of this study was to describe the baseline clinical features and long-term outcomes of patients with moyamoya disease (MMD) based on a 25-year period at a single center in China.

METHODS

 Data obtained in 528 consecutive patients with MMD treated at the authors' hospital from 1984 to 2010 were reviewed retrospectively. Events of transient ischemic attack, new infarction, and hemorrhage were included. The Kaplan-Meier risk of stroke was calculated.

RESULTS

 The mean (± SD) patient age was 26 ± 13 years (range 2–67 years), and the female/male ratio was 0.9:1. There were 332 cases of ischemia and 196 hemorrhages. Adults had a higher rate of bleeding than children (50.7% vs 14.0%, respectively; p < 0.001). One hundred twenty-two patients were treated conservatively, and 406 patients underwent revascularization procedures. Of 528 patients, 331 (62.7%) had at least 1 year of follow-up (median 39.5 months) and data from these patients were analyzed. Rebleeding and mortality rates in patients with hemorrhagic MMD (n = 104) were higher than in those with ischemic MMD (n = 227) (26.9% vs 2.2% [p < 0.001] and 4.8% vs 0.4% [p < 0.05], respectively). Twenty-five of 60 (41.7%) conservatively treated patients and 8 of 271 (2.9%) surgically treated patients experienced rebleeding events, a difference that was significant in the Kaplan-Meier curve of rebleeding (p < 0.01). An improvement in perfusion was found in 164 of 224 (73.2%) surgically treated patients 1 month after discharge. However, there was no significant difference in the rate of ischemic events in the surgical and conservative groups (18.8% and 28.3%, respectively; p = 0.09). Among the 104 hemorrhagic cases, rebleeding attacks were observed in 25 patients in the nonsurgical group (n = 60) and 3 patients in the surgical group (n = 44) (41.7% and 6.8%, respectively; OR 9.7 [95% CI 2.7–35.0]; p < 0.01).

CONCLUSIONS

 There was no difference in the sex distribution of Chinese patients with MMD. Patients with hemorrhagic MMD had a much higher rate of rebleeding and poorer prognosis than those with the ischemic type. Surgical revascularization procedures can improve cerebral perfusion and have a positive impact in preventing rebleeding in patients with hemorrhagic MMD.

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Xiaofeng Deng, Faliang Gao, Dong Zhang, Yan Zhang, Rong Wang, Shuo Wang, Yong Cao, Yuanli Zhao, Yuesong Pan, Xingju Liu, Qian Zhang and Jizong Zhao

OBJECTIVE

The optimal surgical modality for moyamoya disease (MMD) remains unclear. The aim of this study was to compare the surgical effects of direct bypass (DB) and indirect bypass (IB) in the treatment of adult ischemic-type MMD.

METHODS

Adult patients with ischemic-type MMD who underwent either DB or IB from 2009 to 2015 were identified retrospectively from a prospective database. Patients lost to follow-up or with a follow-up period less than 12 months were excluded. Recurrent stroke events and modified Rankin Scale (mRS) scores at the last follow-up were compared between the 2 surgical groups after 1:1 propensity score matching.

RESULTS

A total of 220 patients were considered, including 143 patients who underwent DB and 77 patients who underwent IB. After propensity score matching, 70 pairs were obtained. The median follow-up period was 40.5 months (range 14–75 months) in the DB group and 31.5 months (range 14–71 months) in the IB group (p = 0.004). Kaplan-Meier analysis showed that patients who received DB had a longer stroke-free time (mean 72.1 months) compared with patients who received IB (mean 61.0 months) (p = 0.045). Good neurological status (mRS score ≤ 2) was achieved in 64 patients in the DB group (91.4%) and 66 patients in the IB group (94.3%), but there was no significant difference (p = 0.512).

CONCLUSIONS

Although neurological function outcome was not determined by the surgical modality, DB is more effective in preventing recurrent ischemic strokes than IB for adult ischemic-type MMD.

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Xiaofeng Deng, Faliang Gao, Dong Zhang, Yan Zhang, Rong Wang, Shuo Wang, Yong Cao, Yuanli Zhao, Yuesong Pan, Xun Ye, Xingju Liu, Qian Zhang, Jia Wang, Ziwen Yang, Meng Zhao and Jizong Zhao

OBJECTIVE

Bypass surgery is the most common treatment for moyamoya disease (MMD), but there is controversy over which surgical modality is best. The objective of this study was to evaluate the clinical outcome of patients with MMD after undergoing different surgical modalities.

METHODS

A series of 696 consecutive MMD patients treated between June 2009 and May 2015 were screened in this prospective cohort study. Patients who did not undergo revascularization surgeries and those who underwent different surgical modalities in bilateral hemispheres were excluded. Finally, 529 patients who were observed for at least 12 months were included: 438 patients underwent unilateral surgery, and 91 patients underwent bilateral surgery. Of these, 241 patients underwent direct bypass (DB); 81, a combined bypass (CB); and 207, an indirect bypass (IB). Three clinical outcomes were evaluated and compared between surgical groups: recurrent stroke events, modified Rankin Scale (mRS) scores, and change in the main symptoms.

RESULTS

The mean follow-up period was 40 months. During the follow-up period, recurrent stroke was observed in 43 patients, including 15 patients with hemorrhage, 26 patients with ischemia (transient ischemic attack in 19 patients and infarction in 7 patients), and 2 patients with both hemorrhage and cerebral infarction. Kaplan-Meier analysis showed that patients who underwent a CB or DB had a longer ischemia-free time than those who underwent IB (p = 0.013); however, there was no significant difference in the hemorrhage-free time between the different surgical modalities (p = 0.534). A good neurological status (mRS score ≤ 2) was achieved in 495 patients (93.6%) and was significantly achieved by more children (98.2%) than adults (92.3%; p = 0.022). Surgical modalities were not significantly associated with outcome neurological status (p = 0.860). Moreover, improvement in symptoms was observed in 449 patients (84.9%) and was also significantly more common in children (93.0%) than in adults (82.7%; p = 0.006). No significant difference was observed between the different surgical modalities (p = 0.548).

CONCLUSIONS

CB and DB are more effective at preventing recurrent ischemic strokes than IB. However, there is no evidence that these 3 surgical modalities demonstrate significant differences in preventing recurrent hemorrhage.

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Hao Li, Haiyan Yue, Yajing Hao, Haowen Li, Shuo Wang, Lanbing Yu, Dong Zhang, Yong Cao and Jizong Zhao

OBJECTIVE

The pathogenesis of cerebral aneurysms (CAs) remains largely unknown. Long noncoding RNAs (lncRNAs) were reported recently to play crucial roles in many physiological and biological processes. Here, the authors compared the gene-expression profiles of CAs and their control arteries to investigate the potential functions of lncRNAs in the formation of CAs.

METHODS

A prospective case-control study was designed to identify the changes in expression of lncRNAs and mRNAs between 12 saccular CA samples (case group) and 12 paired superficial temporal artery samples (control group). Microarray analysis was performed to investigate the expression of lncRNAs and messenger RNAs (mRNAs), and reverse-transcription quantitative polymerase chain reaction was used to validate the microarray analysis findings. Then, an lncRNA target-prediction program and gene ontology and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analyses were applied to explore potential lncRNA functions.

RESULTS

A comparison between the case and control groups revealed that 1518 lncRNAs and 2545 mRNAs were expressed differentially. By using target-prediction program analysis, the authors constructed a complex network consisting of 2786 matched lncRNA-mRNA pairs, in which ine1 mRNA was potentially targeted by one to tens of lncRNAs, and vice versa. The results of further gene ontology and KEGG pathway analyses indicated that lncRNAs were involved mainly in regulating immune/inflammatory processes/pathways and vascular smooth muscle contraction, both of which are known to have crucial pathobiological relevance in terms of CA formation.

CONCLUSIONS

By comparing CAs with their control arteries, the authors created an expression profile of lncRNAs in CAs and propose here their possible roles in the pathogenesis of CAs. The results of this study provide novel insight into the mechanisms of CA pathogenesis and shed light on developing new therapeutic intervention for CAs in the future.

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Qian Zhang, Yaping Liu, Dong Zhang, Rong Wang, Yan Zhang, Shuo Wang, Lanbing Yu, Chaoxia Lu, Fang Liu, Jian Zhou, Xue Zhang and Jizong Zhao

OBJECTIVE

Moyamoya disease (MMD) is a rare, genetically heterogeneous cerebrovascular disease. The authors conducted a genetic study of really interesting new gene (RING) finger protein 213 (RNF213); actin alpha 2 (ACTA2); BRCA1/BRCA2-containing complex subunit 3 (BRCC3); and guanylate cyclase 1, soluble, alpha 3 (GUCY1A3) as well as a clinical phenotype analysis in Chinese MMD patients to determine whether genetic differences are responsible for the different clinical features that appear in MMD in different ethnicities.

METHODS

A panel was designed to identify disease-causing mutations in MMD genes and those involved in related disorders (RNF213, ACTA2, BRCC3, and GUCY1A3). The panel was used to detect disease-causing mutations in 255 Chinese MMD patients. Genotype and allele frequencies were compared between patients and 300 controls. A mutation segregation analysis was performed in 34 families, and genotype-phenotype correlations were made.

RESULTS

Twenty-seven rare missense variants of RNF213 were identified and were not found in controls. Among them, p.R4810K was identified in 31.4% of patients (80 of 255) with MMD. Significantly higher frequencies of the A allele and G/A genotype of p.R4810K were observed in MMD patients compared with controls (χ2 = 104.166, p < 0.000). Twenty-five rare variants were identified in 10.6% of patients (27 of 255) without p.R4810K variants. Segregation analysis supported an association between MMD and 3 variants. No possible disease-causing mutations were identified in ACTA2, BRCC3, or GUCY1A3. Compared with patients without the rare variants in RNF213, the p.R4810K heterozygous patients were younger at diagnosis (25 vs 29 years old, p = 0.049) and had more familial cases (24% vs 4.4%, p = 0.000), ischemic cases (81.3% vs 67.5%, p = 0.037), and involvement of the posterior cerebral artery (52% vs 32.5%, p = 0.007).

CONCLUSIONS

RNF213 is the major susceptibility gene in Chinese MMD patients. The spectrum of rare variants identified in Chinese MMD patients was diverse. Compared to patients without the rare variants in RNF213, the p.R4810K heterozygous patients exhibited different clinical features.

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Xiaofeng Deng, Yan Zhang, Long Xu, Bo Wang, Shuo Wang, Jun Wu, Dong Zhang, Rong Wang, Jia Wang and Jizong Zhao

OBJECT

Cerebral arteriovenous malformations (AVMs) are congenital malformations that may grow in the language cortex but usually do not lead to aphasia. In contrast, language dysfunction is a common presentation for patients with a glioma that involves language areas. The authors attempted to demonstrate the difference in patterns of language cortex reorganization between cerebral AVMs and gliomas by blood oxygen level–dependent (BOLD) functional MRI (fMRI) evaluation.

METHODS

The authors retrospectively reviewed clinical and imaging data of 63 patients with an unruptured cerebral AVM (AVM group) and 38 patients with a glioma (glioma group) who underwent fMRI. All the patients were right handed, and all their lesions were located in the left cerebral hemisphere. Patients were further categorized into 1 of the 2 following subgroups according to their lesion location: the BA subgroup (overlying or adjacent to the inferior frontal or the middle frontal gyri [the Broca area]) and the WA subgroup (overlying or adjacent to the supramarginal, angular, or superior temporal gyri [the Wernicke area]). Lateralization indices of BOLD signal activations were calculated separately for the Broca and Wernicke areas. Statistical analysis was performed to identify the difference in patterns of language cortex reorganization between the 2 groups.

RESULTS

In the AVM group, right-sided lateralization of BOLD signal activations was observed in 23 patients (36.5%), including 6 with right-sided lateralization in the Broca area alone, 12 in the Wernicke area alone, and 5 in both areas. More specifically, in the 34 patients in the AVM-BA subgroup, right-sided lateralization of the Broca area was detected in 9 patients (26.5%), and right-sided lateralization of the Wernicke area was detected in 4 (11.8%); in the 29 patients in the AVM-WA subgroup, 2 (6.9%) had right-sided lateralization of the Broca area, and 13 (44.8%) had right-sided lateralization of the Wernicke area. In the glioma group, 6 patients (15.8%) showed right-sided lateralization of the Wernicke area, including 2 patients in the glioma-BA subgroup and 4 patients in the glioma-WA subgroup. No patient showed right-sided lateralization of the Broca area. Moreover, although the incidence of right-sided lateralization was higher in cases of low-grade gliomas (5 in 26 [19.2%]) than in high-grade gliomas (1 in 12 [8.3%]), no significant difference was detected between them (p = 0.643). Compared with the AVM group, the incidence of aphasia was significantly higher (p < 0.001), and right-sided lateralization of language areas was significantly rarer (p = 0.026) in the glioma group.

CONCLUSIONS

Right-sided lateralization of BOLD signal activations was observed in patients with a cerebral AVM and in those with a glioma, suggesting that language cortex reorganization may occur with both diseases. However, the potential of reorganization in patients with gliomas seems to be insufficient compared with patients AVMs, which is suggested by clinical manifestations and the fMRI findings. Moreover, this study seems to indicate that in patients with an AVM, a nidus near the Broca area mainly leads to right-sided lateralization of the Broca area, and a nidus near the Wernicke area mainly leads to right-sided lateralization of the Wernicke area.

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Xiaofeng Deng, Zihao Zhang, Yan Zhang, Dong Zhang, Rong Wang, Xun Ye, Long Xu, Bo Wang, Kai Wang and Jizong Zhao

OBJECT

The authors compared the image quality and diagnostic sensitivity and specificity of 7.0-T and 3.0-T MRI and time-of-flight (TOF) MR angiography (MRA) in patients with moyamoya disease (MMD).

METHODS

MR images of 15 patients with ischemic-type MMD (8 males, 7 females; age 13–48 years) and 13 healthy controls (7 males, 6 females; age 19–28 years) who underwent both 7.0-T and 3.0-T MRI and MRA were studied retrospectively. The main intracranial arteries were assessed by using the modified Houkin’s grading system (MRA score). Moyamoya vessels (MMVs) were evaluated by 2 grading systems: the MMV quality score and the MMV area score. Two diagnostic criteria for MMD were used: the T2 criteria, which used flow voids in the basal ganglion on T2-weighted images, and the TOF criteria, which used the high-intensity areas in the basal ganglion on source images from TOF MRA. All data were evaluated by 2 independent readers who were blinded to the strength field and presence or absence of MMD. Using conventional angiography as the gold standard, the sensitivity and specificity of 7.0-T and 3.0-T MRI/MRA in the diagnosis of MMD were calculated. The differences between 7.0-T and 3.0-T MRI and MRA were statistically compared.

RESULTS

No significant differences were observed between 7.0-T and 3.0-T MRA in MRA score (p = 0.317) or MRA grade (p = 0.317). There was a strong correlation between the Suzuki’s stage and MRA grade in both 3.0-T (rs = 0.930; p < 0.001) and 7.0-T (rs = 0.966; p < 0.001) MRA. However, MMVs were visualized significantly better on 7.0-T than on 3.0-T MRA, suggested by both the MMV quality score (p = 0.001) and the MMV area score (p = 0.001). The correlation between the Suzuki’s stage and the MMV area score was moderate in 3.0-T MRA (rs = 0.738; p = 0.002) and strong in 7.0-T MRA (rs = 0.908; p < 0.001). Moreover, 7.0-T MR images showed a greater capacity for detecting flow voids in the basal ganglion on both T2-weighted MR images (p < 0.001) and TOF source images (p < 0.001); 7.0-T MRA also revealed the subbranches of superficial temporal arteries much better. Receiver operating characteristic curve analysis showed that, according to the T2 criteria, 7.0-T MRI/MRA was more sensitive (sensitivity 1.000; specificity 0.933) than 3.0-T MRI/MRA (sensitivity 0.692; specificity 0.933) in diagnosing MMD; based on the TOF criteria, 7.0-T MRI/MRA was more sensitive (1.000 vs 0.733, respectively) and more specific (1.000 vs 0.923, respectively) than 3.0-T MRI/MRA.

CONCLUSIONS

Compared with 3.0-T MRI/MRA, 7.0-T MRI/MRA detected and delineated MMVs more clearly and provided higher diagnostic sensitivity and specificity, although it did not show significant improvement in depicting main intracranial arteries. The authors speculate that 7.0-T MRI/MRA is a promising technique in the diagnosis of MMD because it is noninvasive compared with conventional angiography and it is more sensitive than 3.0-T MRI/MRA.