Long-Term Study on Cognitive Function in
Adult Patients with Moyamoya Disease

doi:10.3969/j.issn.1673-5765.2024.07.006

Abstract

Abstract:

Objective To assess the cognitive function of adult patients with Moyamoya disease (MMD) and the changes during long-term follow-up, and to explore the influencing factors of cognitive decline in adult patients with MMD.

Methods A prospective cohort study was used to continuously include 64 adult patients with MMD admitted to the First Affiliated Hospital of Naval Medical University from January 2015 to June 2016, of whom 42 patients underwent revascularization (16 patients underwent combined revascularization and 26 patients underwent indirect revascularization), and 22 patients did not receive surgical treatment. Baseline characteristics of all patients were collected, and cognitive function was assessed by the MoCA at baseline, short-term [(6±1) months] follow-up, and long-term [(10±1) years] follow-up. Emotional status was assessed by patient health questionnaire-9 (PHQ-9) and generalized anxiety disorder-7-item (GAD-7). The changes in cognitive function and emotional status were analyzed in all patients, as well as in patients receiving different treatment approaches, during short- and long-term follow-ups. The reliable change index (RCI) was used to determine whether there was a decline in function with the following formula: RCIMoCA= (X2-X1) /standard deviation (SD). It was defined as cognitive decline when RCIMoCA＜-1. The binary logistic regression model was used to explore the independent influencing factors of long-term cognitive decline in adult patients with MMD.

Results A total of 53 patients completed the long-term follow-up, including 13 patients who underwent combined revascularization, 22 patients who underwent indirect revascularization, and 18 patients who did not undergo surgery. The MoCA scores of the overall population tended to stabilize during the long-term follow-up period (P=0.694). Patients who underwent combined revascularization [21 (18-25) points vs. 19 (17-24) points, P=0.035] and indirect revascularization [20 (17-22) points vs. 19 (16-22) points, P=0.047] showed improvement in MoCA scores at short-term follow-up, but tended to stabilize relative to baseline at long-term follow-up. There was no significant decrease in MoCA scores in patients who did not undergo surgery at short-term follow-up, but there was a decrease in MoCA scores compared with baseline at long-term follow-up [15 (11-24) points vs. 18 (14-26) points, P=0.039]. Over time, the cognitive function of adult patients with MMD tended to worsen, while the anxiety and depression status tended to improve. There was a significant difference in the proportion of surgical treatment between the two groups with and without cognitive decline during the long-term follow-up (P=0.037), but logistic regression did not find it as an independent influencing factor (P>0.05).

Conclusions During long-term follow-up, the cognitive function of adult patients with MMD generally remain stable, and the anxiety and depression status tends to improve. Revascularization may have a positive effect on maintaining long-term cognitive stability, and future studies with larger sample sizes are needed.

Key words: Moyamoya disease; Cognitive function; Neuropsychology; Revascularization

摘要：

目的评估成人烟雾病患者的认知水平及其在长期随访中的变化，并探讨成人烟雾病患者认知功能下降的影响因素。

方法采用前瞻性队列研究设计，连续纳入2015年1月—2016年6月海军军医大学第一附属医院脑血管病中心收治的成人烟雾病患者64例，其中42例接受血流重建术（联合血流重建术16例、间接血流重建术26例）治疗，22例未接受手术治疗。收集所有患者的基线资料，并使用MoCA评估患者基线、短期[（6±1）个月]随访、长期[（10±1）年]随访时的认知功能，采用9条目患者健康问卷（patient health questionnaire-9，PHQ-9）和7条目广泛性焦虑障碍（generalized anxiety disorder-7-item，GAD-7）量表评估患者的情绪状态。分析所有患者以及接受不同治疗患者在短期随访和长期随访中的认知功能和情绪状态变化。采用可靠变化指数（reliable change index，RCI）判断是否存在功能下降，计算公式为RCIMoCA=（X2-X1）/标准差（standard deviation，SD），将RCIMoCA＜-1定义为认知功能下降。采用二元logistic回归模型探讨成人烟雾病患者长期认知功能下降的独立影响因素。

结果共53例患者完成长期随访，其中接受联合血流重建术治疗患者13例，接受间接血流重建术治疗患者22例，未接受手术者18例。整体人群3个随访时期MoCA评分趋于稳定（P=0.694）：接受联合血流重建术[21（18～25）分 vs. 19（17～24）分，P=0.035]和间接血流重建术[20（17～22）分 vs. 19（16～22）分，P=0.047]治疗的患者短期随访MoCA评分有改善，但长期随访相对基线趋于稳定；未手术患者短期随访MoCA评分无明显下降，长期随访较基线有下降[（15（11～24）分 vs. 18（14～26）分，P=0.039]。随着时间的延长，成人烟雾病患者的认知功能恶化有加重趋势，而焦虑、抑郁状态有好转趋势。长期随访认知功能下降组与未下降组之间的手术治疗比例差异有统计学意义（P=0.037），但logistic回归分析未发现手术治疗是其独立影响因素（P＞0.05）。

结论在长期随访中，成人烟雾病患者认知功能大致保持稳定，焦虑、抑郁状态趋于好转。血流重建术可能对维持长期认知稳定有积极作用，但仍需扩大样本量进一步明确。

关键词: 烟雾病; 认知功能; 神经心理; 血流重建术

CLC Number:

YAO Yang, FU Kaikai, ZHU Junrong, ZHAO Ming, CHEN Lei, HAN Yi, LI Qiang, ZHANG Ping.

Long-Term Study on Cognitive Function in Adult Patients with Moyamoya Disease [J]. Chinese Journal of Stroke, 2024, 19(7): 769-776.

姚阳, 傅锴锴, 朱俊蓉, 赵明, 陈蕾, 韩易, 李强, 张萍 .

成人烟雾病患者认知功能的长期研究 [J]. 中国卒中杂志, 2024, 19(7): 769-776.

References

[1] SUN J，SHI Z Y，YU L B，et al. Predictors of preoperative cognitive dysfunction in adults with Moyamoya disease：a preliminary research[J/OL]. BMC Neurol，2022，22（1）：12[2024-05-22]. https://doi.org/10.1186/s12883-021-02511-2.

[2] KRONENBURG A，VAN DEN BERG E，VAN SCHOONEVELD M M，et al. Cognitive functions in children and adults with Moyamoya vasculopathy：a systematic review and meta-analysis[J]. J Stroke，2018，20（3）：332-341.

[3] NAKAGAWARA J，OSATO T，KAMIYAMA K，et al. Diagnostic imaging of higher brain dysfunction in patients with adult Moyamoya disease using statistical imaging analysis for 123I iomazenil single photon emission computed tomography[J]. Neurol Med Chir（Tokyo），2012，52（5）：318-326.

[4] WILLIAMS T S，WESTMACOTT R，DLAMINI N，et al. Intellectual ability and executive function in pediatric Moyamoya vasculopathy[J]. Dev Med Child Neurol，2012，54（1）：30-37.

[5] NASREDDINE Z S，PHILLIPS N A，BéDIRIAN V，et al. The montreal cognitive assessment，MoCA：a brief screening tool for mild cognitive impairment[J]. J Am Geriatr Soc，2005，53（4）：695-699.

[6] KROENKE K，SPITZER R L，WILLIAMS J B. The PHQ-9：validity of a brief depression severity measure[J]. J Gen Intern Med，2001，16（9）：606-613.

[7] LÖWE B，DECKER O，MüLLER S，et al. Validation and standardization of the generalized anxiety disorder screener（GAD-7）in the general population[J]. Med Care，2008，46（3）：266-274.

[8] FESTA J R，SCHWARZ L R，PLISKIN N，et al. Neurocognitive dysfunction in adult Moyamoya disease[J]. J Neurol，2010，257（5）：806-815.

[9] CALVIERE L，CATALAA I，MARLATS F，et al. Correlation between cognitive impairment and cerebral hemodynamic disturbances on perfusion magnetic resonance imaging in European adults with Moyamoya disease[J]. J Neurosurg，2010，113（4）：753-759.

[10] SU S H，HAI J，ZHANG L，et al. Assessment of cognitive function in adult patients with hemorrhagic Moyamoya disease who received no surgical revascularization[J]. Eur J Neurol，2013，20（7）：1081-1087.

[11] CHAN E，GAL A M，VAN HARSKAMP N，et al. Long-term study of the cognitive profile of Moyamoya disease in adults[J/OL]. J Stroke Cerebrovasc Dis，2023，32（6）：107064[2024-05-22]. https://doi.org/10.1016/j.jstrokecerebrovasdis.2023.107064.

[12] ZEIFERT P D，KARZMARK P，BELL-STEPHENS T E，et al. Neurocognitive performance after cerebral revascularization in adult Moyamoya disease[J]. Stroke，2017，48（6）：1514-1517.

[13] KARZMARK P，ZEIFERT P D，TAN S，et al. Effect of Moyamoya disease on neuropsychological functioning in adults[J]. Neurosurgery，2008，62（5）：1048-1051.

[14] KAZUMATA K，THA K K，TOKAIRIN K，et al. Brain structure，connectivity，and cognitive changes following revascularization surgery in adult Moyamoya disease[J/OL]. Neurosurgery，2019，85（5）：e943-e952[2024-05-22]. https://doi.org/10.1093/neuros/nyz176.

[15] UCHIDA S，KUBO Y，OOMORI D，et al. Long-term cognitive changes after revascularization surgery in adult patients with ischemic Moyamoya disease[J]. Cerebrovasc Dis Extra，2021，11（3）：145-154.

[16] YANAGIHARA W，CHIDA K，KOBAYASHI M，et al. Impact of cerebral blood flow changes due to arterial bypass surgery on cognitive function in adult patients with symptomatic ischemic Moyamoya disease[J]. J Neurosurg，2018，131（6）：1716-1724.

[17] FRERICHS R J，TUOKKO H A. A comparison of methods for measuring cognitive change in older adults[J]. Arch Clin Neuropsychol，2005，20（3）：321-333.

[18] NAKAMIZO A，AMANO T，MATSUO S，et al. Five-year changes in cognitive function and their predictor in adult Moyamoya disease[J/OL]. World Neurosurg，2022，165：e346-e351[2024-05-22]. https://doi.org/10.1016/j.wneu.2022.06.055.

[19] AMEN D G，KRISHNAMANI P，MEYSAMI S，et al. Classification of depression，cognitive disorders，and co-morbid depression and cognitive disorders with perfusion SPECT neuroimaging[J]. J Alzheimers Dis，2017，57（1）：253-266.

[20] LEI Y，LI Y J，GUO Q H，et al. Postoperative executive function in adult Moyamoya disease：a preliminary study of its functional anatomy and behavioral correlates[J]. J Neurosurg，2017，126（2）：527-536.

[21] 张萍，方亦斌，陈蕾，等. 血流重建术对成人烟雾病患者抑郁焦虑状态的影响[J]. 第二军医大学学报，2021，42（3）：275-280.

ZHANG P，FANG Y B，CHEN L，et al. Effect of revascularization on depression and anxiety of adult patients with Moyamoya disease[J]. Academic Journal of Second Military Medical University，2021，42（3）：275-280.

[22] HE S H，DUAN R，LIU Z Q，et al. Characteristics of cognitive impairment in adult asymptomatic Moyamoya disease[J/OL]. BMC Neurol，2020，20（1）：322[2024-05-22]. https://doi.org/10.1186/s12883-020-01898-8.

[23] KARZMARK P，ZEIFERT P D，BELL-STEPHENS T E，et al. Neurocognitive impairment in adults with Moyamoya disease without stroke[J]. Neurosurgery，2012，70（3）：634-638.

[24] FESTA J R，SCHWARZ L R，PLISKIN N，et al. Neurocognitive dysfunction in adult Moyamoya disease[J]. J Neurol，2010，257（5）：806-815.

[25] SHEN X X，ZHANG H D，FU H G，et al. Association of cognitive function and hypoperfusion in Moyamoya disease patients without stroke[J]. J Cereb Blood Flow Metab，2023，43（4）：542-551.

[26] SU S H，HAI J，ZHANG L，et al. Quality of life and psychological impact in adult patients with hemorrhagic Moyamoya disease who received no surgical revascularization[J]. J Neurol Sci，2013，328（1/2）：32-36.

[27] TIAN B，XU B，LIU Q，et al. Adult Moyamoya disease：320-multidetector row CT for evaluation of revascularization in STA-MCA bypasses surgery[J]. Eur J Radiol，2013，82（12）：2342-2347.

[28] TAYLOR W D，SCHULTZ S K，PANAITE V，et al. Perspectives on the management of vascular depression[J]. Am J Psychiatry，2018，175（12）：1169-1175.

Long-Term Study on Cognitive Function in Adult Patients with Moyamoya Disease

成人烟雾病患者认知功能的长期研究

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