Risk factors of Cerebral Microbleeds in Patients with Symptomatic and Atherosclerotic Cerebral Small Vessel Disease

doi:10.3969/j.issn.1673-5765.2023.04.010

Abstract

Abstract: Objective To analyze the risk factors of cerebral microbleeds (CMBs) in patients with symptomatic and atherosclerotic cerebral small vessel disease (CSVD) , and differences in clinical characteristics of CMBs in different locations.
Method The clinical data of patients with symptomatic and atherosclerotic CSVD from Changji Traditional Chinese Medicine Hospital of Xinjiang between March 2017 and October 2018 were retrospectively analyzed. According to having CMBs diagnosed by SWI or not, the patiens were divided into CMBs group and non-CMBs group. Binary logistic regression analysis was used to determine the risk factors for CMBs, and the correlation of CMBs number classification and independent risk factors was analyzed. In addition, according to the location of CMBs, the differences of clinical characteristics in different location subgroups were compared: lobar and non-lobar region subgroups, deep white matter and non-deep white matter subgroups, infratentorial region and non-infratentorial region subgroups.
Results A total of 144 CSVD patients were included, with 42 patients (29.2%) with CMBs. CMBs were located in lobar region in 18 cases, deep brain region in 23 cases and infratentorial region in 9 cases. Logistic regression analysis showed that lower apolipoprotein B (OR 0.308, 95%CI 0.099-0.957, P=0.042) and higher fasting blood glucose level (OR 1.128, 95%CI 1.015-1.254, P=0.026) ,
low and middle grade of diastolic pressure, more lacunar cerebral infarcts and lacunar lesions of presumed vascular origin were independent risk factors for CMBs. The grade of CMBs was negatively correlated with the level of apolipoprotein B (r = ﹣0.212, P= 0.011) , positively correlated with the grade of lacunar cerebral infarcts (r = 0.378, P< 0.001) and the grade of lacunar lesions of presumed vascular origin (r = 0.411, P< 0.001) . Compared to the non-lobar region subgroup, lobar region subgroup had the higher BMI (24.4 vs. 23.5, P=0.045) , left ventricular ejection fraction (61.0% vs. 60.0%, P=0.012) and lower heart rate (75.0 beat per minute vs. 83.0 beat per minute, P=0.017) , and educational level distribution also had statistical difference between the two groups (P=0.004) . Compared to the non-deep white matter region subgroup, deep white matter region subgroup had a higher male proportion (78.3% vs. 47.4%, P=0.038) and more lacunar cerebral infarcts (P=0.002) .
Conclusion Low apolipoprotein B level and high fasting blood glucose level, low and middle level of diastolic pressure, more lacunar cerebral infarcts and lacunar lesions of presumed vascular origin were independent risk factors for CMBs. The grade of CMBs was negatively correlated with the level of apolipoprotein B, and positively correlated with lacunar cerebral infarcts number and the grade of lacunar lesions of presumed vascular origin. BMI, left ventricular ejection fraction, heart rate and educational level were correlated with lobar CMBs, while gender and lacunar cerebral infarcts number were correlated with deep white matter CMBs.

Key words: Cerebral small vessel disease; Cerebral microbleed; Magnetic resonance imaging; Risk factor

摘要： 目的应用头颅MRI 的SWI序列检测症状性小动脉硬化脑小血管病（cerebral small vessel disease，CSVD）患者脑微出血（cerebral microbleeds，CMBs）灶，分析不同部位CMBs的临床特征差异及CMBs的危险因素。
方法回顾性纳入2017年3月—2018年10月就诊于新疆昌吉州中医院神经内科的小动脉硬化的CSVD患者。根据有无微出血分为CMBs组与无CMBs组。应用二元logistic回归分析CMBs的独立危险因素；判断CMBs数量分级与独立危险因素的相关性。根据CMBs的位置分为脑叶区亚组、深部区亚组、幕下区亚组。比较脑叶区CMBs与非脑叶区CMBs、深部CMBs与非深部CMBs、幕下区CMBs与非幕下区CMBs亚组之间的临床特征差异。
结果共纳入144例CSVD患者，CMBs组42例（29.2%），无CMBs组102例（70.8%），其中脑叶区18例，深部白质区23例，幕下区9例。二元logistic回归分析显示，低载脂蛋白b水平（OR 0.308，95%CI 0.099～0.957，P=0.042）及高空腹血糖值（OR 1.128，95%CI 1.015～1.254，P=0.026）、舒张压、脑梗死灶及假定血管源性腔隙灶是CMBs的独立危险因素。CMBs分级与载脂蛋白b呈负相关（r=-0.212，P=0.011），与脑梗死灶分级（r=0.378，P＜0.001）、假定血管源性腔隙灶分级（r=0.411，P＜0.001）呈正相关。脑叶区CMBs与非脑叶区CMBs相比：脑叶区CMBs组BMI（24.4 kg/m2 vs. 23.5 kg/m2，P=0.045）、射血分数（61.0% vs. 60.0%，P=0.012）高于非脑叶CMBs组，心率（75.0次/分 vs. 83.0次/分，P=0.017）低于非脑叶CMBs组，文化程度分布组间差异有统计学意义（P=0.004）。深部CMBs组的男性比例（78.3% vs. 47.4%，P=0.038）高于非深部CMBs组，梗死灶（P=0.002）数量多于非深部CMBs组。
结论低载脂蛋白b水平及高空腹血糖值、舒张压、脑梗死灶及假定血管源性的腔隙灶是CMBs独立危险因素；CMBs分级与载脂蛋白b呈负相关，与脑梗死灶分级、假定血管源性腔隙灶分级呈正相关；BMI、射血分数、心率、文化程度与脑叶CMBs相关，性别、梗死灶分级与深部CMBs相关。

关键词: 脑小血管病; 脑微出血; 磁共振成像; 危险因素

LIU Yang, WANG Rui, ZHANG Xiang, SUN Huiling, MA Yinghu.

Risk factors of Cerebral Microbleeds in Patients with Symptomatic and Atherosclerotic Cerebral Small Vessel Disease

[J]. Chinese Journal of Stroke, 2023, 18(04): 440-449.

刘洋, 王蕊, 张祥, 孙慧玲, 马英虎. 症状性小动脉硬化脑小血管病患者脑微出血的危险因素分析[J]. 中国卒中杂志, 2023, 18(04): 440-449.

References

[1] CANNISTRARO R J，BADI M，EIDELMAN B H，et al. CNS small vessel disease：a clinical review[J]. Neurology，2019，92（24）：1146-1156.
[2] NANNONI STEFANIA，OHLMEIER LAURA，BROWN ROBIN B，et al. Cognitive impact of cerebral microbleeds in patients with symptomatic small vessel disease[J]. Int J Stroke，2022，17（4）：415-424.
[3] WILSON DUNCAN，AMBLER GARETH，LEE KEON JOO，et al. Cerebral microbleeds and stroke risk after ischaemic stroke or transient ischaemic attack：a pooled analysis of individual patient data from cohort studies[J]. Lancet Neurol，2019，18（7）：653-665.
[4] 王慧玲，郑连红，王萌. 脑微出血机制与危险因素的研究进展[J]. 临床荟萃，2021，36（8）：749-752.
[5] 胡文立，杨磊，李婷，等. 中国脑小血管病诊治专家共识2021[J]. 中国卒中杂志，2021，16（7）：716-726.
[6] WARDLAW J M，SMITH E E，BIESSELS G J，et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration[J]. Lancet Neurol，2013，12（8）：822-838.
[7] 李虹，梅锦荣．大学生压力量表的编制[J]．应用心理学，2002，8（1）：27-32.
[8] 王孟成，戴晓阳，姚树桥. 中国大五人格问卷的初步编制Ⅲ：简式版的制定及信效度检验[J]. 中国临床心理学杂志，2011，19（4）：454-457.
[9] GREGOIRE S M，CHAUDHARY U J，BROWN M M，et al. The microbleed anatomical rating scale（MARS）：reliability of a tool to map brain microbleeds[J]. Neurology，2009，73（21）：1759.
[10] LUO Q，TANG H D，XU X X，et al. The prevalence and risk factors of cerebral microbleeds：a community-based study in China[J/OL] . Ther Clin Risk Manag，2021，17：165-171[2022-09-01]. https://doi.org/10.2147/TCRM.S297708.
[11] HAJI S，PLANCHARD R，ZUBAIR A，et al. The clinical relevance of cerebral microbleeds in patients with cerebral ischemia and atrial fibrillation[J]. J Neurol，2016，263（2）：238-244.
[12] HOFMAN，ALBERT，LUGT V D，et al. Association of cerebral microbleeds with cognitive decline and dementia[J]. JAMA Neurol，2016，73（8）：934-943.
[13] TSAI HSIN-HSI，PASI MARCO，TSAI LI-KAI，et al. Superficial cerebellar microbleeds and cerebral amyloid angiopathy：a magnetic resonance imaging/positron emission tomography study[J]. Stroke，2020，51（1）：202-208.
[14] LEI C Y，ZHONG L M，LING Y F，et al. Blood glucose levels are associated with cerebral microbleeds in patients with acute ischaemic stroke[J]. Eur Neurol，2018，80（3/4）：187-192.
[15] KESAV PRAVEEN，MENON DEEPAK，VYSAKHA K V，et al. Differential distribution of cerebral microbleeds in subtypes of acute ischemic minor stroke and TIA as well as its association with vascular risk factors[J]. Neurol India，2020，68（5）：1139-1143.
[16] LYU L C，SHEN J Y，ZENG C L，et al. Cerebral microbleeds are associated with blood pressure levels in individuals with hypertension[J]. Clin Exp Hypertens，2020，42（4）：328-334.
[17] NI R H，CHU L，XU D F，et al. Risk factors of cerebral microbleeds in young and middle-aged patients with hypertension[J]. Neurol Res，2018，40（5）：413-418.
[18] CHENG Y J，WANG Y A，SONG Q H，et al. Use of anticoagulant therapy and cerebral microbleeds：a systematic review and meta-analysis[J]. J Neurol，2021，268（5）：1666-1679.
[19] FENG X，TANG Q Q，CHENG C，et al. Low serum lipid levels，use of statin and cerebral microbleeds：a systematic review and meta-analysis[J/OL]. J Clin Neurosci，2021，94：216-225[2022-09-01]. https://doi.org/10.1016/j.jocn. 2021.10.032.
[20] 陈歆，顾雨铖，邹君惠，等. 脑小血管病患者脑白质病变评分及体积与脑微出血的相关性[J]. 国际脑血管病杂志，2018，26（11）：819-825.
[21] 许衡衡，邵鹏飞，马俊怡，等. 脑微出血与脑小血管病患者腔隙性脑梗死的相关性[J]. 国际脑血管病杂志，2021，29（4）：258-264.
[22] 乔琦，王惠娟，曲珍珍，等. 脑血管病患者脑微出血的相关危险因素分析[J]. 中华神经医学杂志，2018，17（8）：802-807.
[23] 张定，牟奇猛，韩波，等. 脑腔隙性脑梗死与微出血的相关性研究[J]. 医学影像学杂志，2015，25（1）：5.
[24] LIANG C H，WANG J，FENG M M，et al. White matter changes，duration of hypertension，and age are associated with cerebral microbleeds in patients with different stages of hypertension[J]. Quant Imaging Med Surg，2022，12（1）：119-130.