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Table of Contents    
ORIGINAL ARTICLE
Year : 2020  |  Volume : 68  |  Issue : 6  |  Page : 1409-1413

Neurocognitive Outcomes in Adult Quasi -Moyamoya Disease: A Prospective Analysis of Consecutive Cases


1 Department of Neurosurgery, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei Province, People's Republic of China
2 School of Basic Medical Sciences and Forensic Medicine, Hangzhou Medical College, Hangzhou, Zhejiang Province, People's Republic of China
3 Department of Obstetrics and Gynecology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei Province, People's Republic of China
4 Department of Neurosurgery, West China Hospital, West China School of Medicine, Sichuan University, Chengdu, Sichuan Province, People's Republic of China

Date of Web Publication19-Dec-2020

Correspondence Address:
Dr. Dongsheng Guo
Department of Neurosurgery, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei Province
People's Republic of China
Junjuan Wang
School of Basic Medical Sciences and Forensic Medicine, Hangzhou Medical College, Hangzhou, Zhejiang Province
People's Republic of China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.304116

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 » Abstract 


Background: This study aimed to evaluate and compare the neurocognitive outcomes of adult quasi-moyamoya disease (quasi-MMD) patients with autoimmune diseases (AIDs) to help better manage these patients.
Methods: We performed a structured battery of neurocognitive tests to analyze and compare the neurocognitive outcomes of adult quasi-MMD patients with AID in our hospital from October 2000 to September 2015.
Results: Overall, 27.3% of the neuropsychological test comparisons indicated a significant improvement in cognition, and a significant decline was found in 6%. In 47.4% of comparisons, the observed difference did significantly change the reliable change indices (RCI) before and after anti-autoimmune treatment. We found that the number of patients showing significant improvements, and no change in cognitive outcomes did differ between quasi-MMD and MMD (31.8% vs 14.9% with p = 0.006 and 50.0% vs 66.8% with p = 0.031, respectively; Chi-squared test). The incidence of cognitive decline in quasi-MMD patients (18.2%) did not significantly differ from that in MMD patients (18.3%) (p = 0.982). After adjusting for covariates, including sex, age, type 2 diabetes mellitus, risk factors, other comorbidities, and AID, multiple logistic regression analysis suggested that AID was more likely to aggravate the neurocognitive outcome of quasi-MMD patients (p = 0.042, odds ratio (OR) 6.78, 95% confidence interval (CI) 1.31–62.71).
Conclusions: AID was more likely to aggravate the neurocognitive outcome of quasi-MMD patients, and anti-autoimmune treatment could improve long-term neurocognitive outcomes. These findings indicated that AID seemed to be an independent risk factor for the pathological and physiological mechanisms of quasi-MMD.


Keywords: Autoimmune diseases, neurocognitive outcome, quasimoyamoya disease
Key Messages: Quasi-MMD is relatively less common in the asian population compared to the classical MMD. This study included Quasi MMD associated with autoimmune etiology. The occurence of severe cognitive deficits was positively correlated with the existence of AID, which promptly responds to anti-autoimmune therapy.


How to cite this article:
Chen J, Wang J, Zheng X, Liu Y, Guo D. Neurocognitive Outcomes in Adult Quasi -Moyamoya Disease: A Prospective Analysis of Consecutive Cases. Neurol India 2020;68:1409-13

How to cite this URL:
Chen J, Wang J, Zheng X, Liu Y, Guo D. Neurocognitive Outcomes in Adult Quasi -Moyamoya Disease: A Prospective Analysis of Consecutive Cases. Neurol India [serial online] 2020 [cited 2021 Jan 21];68:1409-13. Available from: https://www.neurologyindia.com/text.asp?2020/68/6/1409/304116




Quasi-moyamoya disease (quasi-MMD) is characterized by moyamoya vasculopathy (MMV) and well-recognized comorbidities, including autoimmune disease (AID), atherosclerosis, meningitis, brain tumors, Down syndrome, and cranial irradiation.[1],[2],[3],[4] Immunological basis has increasingly noted that quasi-MMD and AIDs often coexist in one individual.[2],[3],[4],[5],[6],[7] The majority of previous studies have rarely focused on the neuropsychological aspects of patients.[8],[9],[10],[11],[12],[13],[14],[15],[16],[17] However, the incidence and severity of cognitive outcomes in quasi-MMD patients associated with AID are yet to be systematically evaluated.[6],[10],[12],[17] We prospectively explored the long-term cognitive outcomes in quasi-MMD patients associated with AID.


 » Methods Top


Patients selection

This prospective study was performed on patients seen from October 2000 to September 2015 at West China Hospital of Sichuan University. Patients were identified for potential inclusion based on the International Classification of Diseases 9th Revision (ICD-9) code 4375 (MMD) and the latest Japanese guidelines. To qualify for inclusion in the study, patients had to have angiographically identified bilateral MMV. Patients with intracranial atherosclerosis with angiographic evidence, reversible vasoconstriction syndrome, intracranial dissection, systemic vasculitis, meningitis, head injury, previous cranial base radiation therapy, or undefined inflammatory processes were excluded. This study was approved by the Sichuan University ethics committee. Each participant signed an informed consent form. All individuals were diagnosed with quasi-MMD based on the guidelines set by the Research Committee on MMD of the Japanese Ministry of Health and Welfare.[18] This study was carried out in accordance with the Code of Ethics of the World Medical Association (Declaration of Helsinki). AID in each quasi-MMD patient was assessed by medical testing, and specific diagnoses were performed according to the ICD-10. All of the following AIDs were considered in the study: Autoimmune thyroid diseases, including Graves' disease (GD) and Hashimoto thyroiditis (HT); autoimmune Type 1 diabetes mellitus; autoimmune gastritis (AIG); systemic lupus erythematosus (SLE); antiphospholipid antibody syndrome (APAS); autoimmune polyendocrine syndrome (APS); and primary biliary cirrhosis (PBC).

Patients were excluded for the following reasons: Age <18 years, Wechsler Adult Intelligence Scale-Third Edition Vocabulary score <7, presence of major psychopathology (psychosis, major depression, or substance abuse), presence of a motor deficit that precluded the administration of some tests, presence of neurological comorbidity (congenital malformations or traumatic brain injury), major surgical complication (stroke or hemorrhage), or low intelligence (full-scale intelligent quotient (IQ) <70).

Treatment of autoimmune disease

All AID patients were treated by a relevant diplomate who had extensive clinical experience according to the management guidelines. During the follow-up period, patients' autoimmune symptoms were well controlled after anti-autoimmune therapy.

Neuropsychological assessment

Basic cognitive ability and intelligence were evaluated with the Wechsler Adult Intelligence Scale-Third Edition (WAIS-III).[19] Memory was assessed using the California Verbal Learning Test-Second Edition and the Wechsler Memory Test-Revised, specifically the Visual Reproduction Immediate and Delayed components.[20] The Trail Making Test Part B (TMT-B), and the Letter and Category Fluency Tests were used to assess executive ability.[21] Sensorimotor function was assessed with the Grooved Pegboard Test.[22] The Trail Making Test Part A assessed the speed of information processing, and expressive language was measured with the Boston Naming Test.[23],[24] The Beck Depression Inventory-II was used as a self-report measure of depression.[22] Each test was completed by the patient and by a family member or other informant familiar with the patient.

The neuropsychological tests were administered to all patients in accordance with manual instructions. Patients were evaluated in a single 3-hour session. Just before the initiation of cognitive testing, each patient was asked to rate his or her current experience of pain, fatigue, depression, and anxiety on a 0 to 10 analog scale, with 10 being maximal. Patients were tested just before anti-autoimmune treatment and again approximately 6 months posttreatment. The mean test–retest interval was 6.5 ± 1.4 (standard deviation (SD)) months. The mean follow-up period was 7.1 ± 3.5 (SD) years.

Data analysis

Continuous variables were expressed as a percentage or as the mean ± SD. Differences were considered to be statistically significant if the P value was < 0.05. To discriminate and compare whether there was a significant change in cognitive performance between pre- and postsurgical neuropsychological assessments, reliable change indices (RCIs) were obtained for each test from previously published reports.[22],[23],[24],[25],[26],[27] The RCI is an indicator used to determine whether a change in an individual's test score with the repeated administration of a test is large enough to indicate a true change in the test score, as opposed to test–retest variability, measurement error, or practice effects. As applied, the RCI is a significance test of the statistical probability that the observed difference between 2 sequential scores can be attributed to variability/error/practice (i.e., the null hypothesis). Statistical analyses were performed with Statistical Package for the Social Sciences (SPSS) 18.0 (SPSS Inc.). Differences were considered to be significant with a P value < 0.05.


 » Results Top


Clinical characteristics of quasi-MMD patients

A total of 44 quasi-MMD patients were included in this study. The gender of the patients was predominantly female (68.2%, n = 30). The average age of the patients was 37.8 years ± 13.1 (SD). Their mean education duration was 12.8 ± 3.2 years. The AID types in quasi-MMD patients included the following: GD (25 patients), HT (8 patients), AIG (4 patients), SLE (3 patients), APAS (2 patients), APS (1 patient), and PBC (1 patient).

Cognitive outcome of quasi-MMD patients with AID

Neuropsychological assessments demonstrated total memory improvement in 9 (20.5%) cases, no change in 32 (72.7%) cases, and decline in 5 (11.4%) cases. Nine of the 44 (20.5%) patients showed executive improvement, whereas no change was seen in 25 (56.8%) patients, and a decline was seen in 10 (22.7%) patients. Eight of the 44 (18.2%) patients showed sensorimotor function improvement, whereas no change was seen in 32 (72.7%) patients, and a decline was seen in 5 (11.4%) patients. Ten of the 44 (22.7%) patients showed information processing improvement, whereas no change was seen in 31 (70.5%) patients, and a decline was seen in 3 patients (6.8%). One of the 44 (2.3%) patients showed expressive language improvement, whereas no change was seen in 39 (88.6%) patients, and a decline was seen in 5 (11.4%) patients. On the Beck Depression Inventory-II, 10 (22.7%) patients showed significantly improved depression, and 4 (9.1%) patients showed significantly worsened depression, with 30 (68.2%) patients remaining unchanged. Overall, 27.3% of the neuropsychological test comparisons indicated a significant improvement in cognition, and a significant decline was found in 6%. In 47.4% of comparisons, the observed difference did not change the RCI before and after anti-autoimmune treatment. In addition, we found that patients in whom the AID condition was poorly controlled exhibited a decline in cognition. However, other patients who had an AID condition that was well controlled exhibited a lower decline.

Cognitive outcome comparison between quasi-MMD with AID and MMD

Patient characteristics are summarized in [Table 1]. There were no significant differences in age (P = 0.105) and sex (P = 0.19) between quasi-MMD and MMD. The quasi-MMD patients were further analyzed to determine whether there was a difference between those patients who underwent anti-autoimmune treatment. The neuropsychological outcomes are presented in [Table 2]. We found that the number of patients showing significant improvementand no change in cognitive outcomes did differ between quasi-MMD and MMD (31.8% vs 14.9% with p = 0.006 and 50.0% vs 66.8% with p = 0.031, respectively; Chi-squared test). These outcomes suggested that neurocognitive function was more substantially impacted in AID patients and that controlling the morbid state of AID and maintaining long-term clinical health could significantly improve patients' cognitive outcomes. To determine whether the effect on cognition in patients with AID was significant, patients that exhibited no changes were analyzed. As a result, the incidence of cognitive decline in quasi-MMD patients (18.2%) did not significantly differ from that seen in MMD patients (18.3%) (P = 0.982).
Table 1: Comparison of neuropsychological test measures after anti-autoimmune therapy in quasi-MMD patients with AID during the follow-up period

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Table 2: Patients (and %) with quasi-MMD with AID or MMD in whom neurocognition declined, remained unchanged, or improved after relevant anti-autoimmune treatment

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The abovementioned results demonstrated that controlling AID is beneficial for long-term neurocognitive outcomes. However, these results also suggested that AID may negatively influence the neurocognitive outcomes of quasi-MMD patients. The scores of cognitive outcomes, including performance intelligence quotient (IQ), comprehension, full-sale IQ, bender gestalt test recall, and CVLT-II total words recalled were significantly different.

Independent predictor of cognitive outcomes

The effects of various clinical factors on cognitive outcomes in quasi-MMD and MMD patients were compared. After univariate analysis, no significant correlations were observed with respect to patient age, history of stroke, and disease type between the 2 groups. After adjusting for covariates such as sex, age at disease onset, type 2 diabetes mellitus, risk factors, disease type, AID, surgery and cerebrovascular strokes, multiple logistic regression analysis was conducted to further evaluate the neurocognitive effect of AID on quasi-MMD patients. It was found that AID was more likely to aggravate neurocognitive outcomes in quasi-MMD patients (p = 0.042, odds ratio (OR) 6.78, 95% confidence interval (CI) 1.31–62.71).


 » Discussion Top


Cognitive outcomes of MMD have previously been outlined in a number of studies.[8],[9],[10] The incidence rate of quasi-MMD has been increasingly reported in recent years. Previous studies have shown that there is an increased incidence of cognitive impairment in adult MMD patients.[1],[2],[3] However, the cognitive outcomes of patients with quasi-MMD associated with AID patients remained unclear. In this study, we administered objective tests to assess the overall effect of AID on cognitive function in these individuals. As a result, cognitive dysfunction was found in tests of digit span, memory, verbal fluency, sensorimotor function, processing speed, and executive function, whereas attention and verbal reasoning were not affected. Our findings demonstrate cognitive dysfunction in adult moyamoya patients and show that adult patients with neurocognitive dysfunction are affected by AID.[10],[11]

This study is the first to prospectively focus on cognitive outcomes in a large population of patients with concurrent quasi-MMD and AID. Our findings indicate that the incidence of patients' cognitive improvement shows a significant change in quasi-MMD patients with AID after anti-autoimmune treatment [Table 1] and [Table 2]. The incidence of cognitive decline in patients shows a significant change in quasi-MMD patients with AID that is poorly controlled [Table 1] and [Table 2]. Attention, memory, conceptualization, mental flexibility, and inhibitory control were impaired almost equally in quasi-MMD and MMD patients. The results suggest that AID may aggravate cognitive function in quasi-MMD patients and maybe an independent factor in quasi-MMD patients with AID cognitive dysfunction.

Previous studies demonstrated that immune and inflammatory responses may give rise to immune complex deposition in the brain.[28],[29],[30],[31] Autoimmune cerebral vasculitis is attributed to the deposition of immune complexes deposition and is related to cerebral moyamoya-like vascular changes.[28] Presumably, the abovementioned physiological changes may aggravate hypoxic cerebral ischemic injury in brain tissue. We also found positive correlations between specific neurocognitive functions and perfusion in relevant brain regions, even after a long time. This finding suggests that long-standing hypoperfusion in specific regions can cause related neurocognitive dysfunctions in adult MMD patients. Several studies have shown that an increased incidence of cognitive impairment in adult MMD represents a manifestation of hypoxic–ischemic injury in the brain or a manifestation of ongoing hypoperfusion.[5],,[7],[8],[9],[10] Therefore, this study indicates that AID may impair the cognitive outcome in quasi-MMD patients. Previous studies concluded that autoimmune mechanisms may play an important role in the onset of MMD and are associated with stenosis or occlusion of the internal carotid artery.[3],[4] Theoretically, the beneficial effect of anti-AID therapy on some neurocognitive improvements could be anticipated. In this study, patients with MMD after anti-AID therapy experienced significantly more neurocognitive improvement than neurocognitive impairment. The results of this study indicate that anti-AID therapy could be valuable for cognitive function improvement. Previous studies have suggested that specific neurocognitive functions are positively correlated with brain region perfusion.[8],[9],[10],[11],[12],[13] We suggest that the recovery of an autoimmune abnormality, consequently preventing the immune response, may also play an important role in improving cognitive function in MMD patients. Consistent with previous reports, impaired executive function/attention and working memory were observed in patients with MMD, who have brain regions that are vulnerable to chronic ischemia.[15],[16] Immune complex deposition may consume more cerebral blood flow and glucose than other brain lesions.[28],[29],[30],[31] Therefore, anti-AID treatment may be considered to prevent further ischemic injury and to correct hypoperfusion. Previous studies have suggested that long-standing hypoperfusion in specific regions can cause related neurocognitive dysfunctions in adults with MMD.[8],[9],[10],[11],[12],[13],[16]

To better understand the observed outcomes, we prospectively analyzed and compared the neurocognitive outcomes of patients with quasi-MMD with AID and those with MMD. We found that outcomes showing significant improvement and no change in cognitive outcomes did statistically differ between patients with quasi-MMD with AID and those with MMD. These outcomes suggested that neurocognitive function was more substantially impacted in AID and that controlling the morbid state of AID and maintaining long-term clinical health could significantly improve patients' cognitive outcomes. Multiple logistic regression analysis demonstrated that AID was more likely to aggravate the neurocognitive outcomes of quasi-MMD patients with AID.

There were some limitations to our study. First, we used the ICD-9 code to identify patients; therefore, selection bias could have occurred if this code was incorrectly applied. This was a prospective study, but we tried our best to ensure accuracy in the clinical diagnoses of quasi-MMD, MMD, and AID identification. We acknowledge that selection bias, which often occurs in prospective studies, may have also influenced the interpretation of our results. Second, the sample size was relatively small. However, this study mainly explored the neurocognitive outcomes of patients with quasi-MMD with AID, which is a rare disease. The sample size may help to complete research objectives.


 » Conclusions Top


Neurocognitive dysfunction in adult quasi-MMD patients with AID was higher than that in MMD patients. AID was more likely to aggravate neurocognitive outcomes of quasi-MMD patients, and anti-autoimmune treatment could improve long-term neurocognitive outcomes. These findings indicated that AID may be an independent risk factor for the pathological and physiological mechanisms of quasi-MMD. These findings should be taken into consideration when deciding the treatment strategies.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

This work was supported by Research on Public Welfare Technology Application Projects of Zhejiang Province (Grant No. LGF19H060009).

Conflicts of interest

There are no conflicts of interest.



 
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