Effect of type 2 diabetes mellitus on leptomeningeal collateral
circulation in patients with acute cerebral infarction

doi:10.3760/cma.j.issn.1007-1245.2022.07.004

International Medicine and Health Guidance News ›› 2022, Vol. 28 ›› Issue (7): 902-907.DOI: 10.3760/cma.j.issn.1007-1245.2022.07.004

• Scientific Research • Previous Articles Next Articles

Effect of type 2 diabetes mellitus on leptomeningeal collateral circulation in patients with acute cerebral infarction

Chen Jianjun¹, Chen Qiaoqiong², Mei Zhizhong¹, Huang Xiaoyun¹, Yu Yingli¹, Lin Han¹, Huang Yihong¹, Liao Wang³

¹Department of Neurology, Houjie Hospital, Dongguan 523945, China; ²Department of Endocrinology, Binhaiwan Hospital, Dongguan 523905, China; ³Department of Neurology, Second Hospital, Guangzhou Medical University, Guangzhou 510250, China

Received:2022-01-24 Online:2022-04-01 Published:2022-05-06
Contact: Liao Wang, Email: liaowang@gzhmu.edu.cn
Supported by:
Project of Youth Scientific Foundation of National Natural Science Foundation (82101271);

Project of Youth Foundation and Area Combination Foundation of Basic and Basic Application Research Foundation in Guangdong (2020A1515110317);

Project of Natural Science Foundation in Guangdong (2021A1515010705);

General Project of Social Science and Technology Development in Dongguan (202050715023717)

2型糖尿病对急性脑梗死患者软脑膜侧支循环的影响

陈建军¹ 陈巧琼² 梅志忠¹ 黄晓芸¹ 余映丽¹ 林菡¹ 黄益洪¹ 廖旺³

¹东莞市厚街医院神经科，东莞　523945； ²东莞市滨海湾中心医院内分泌科，东莞　523905； ³广州医科大学附属第二医院神经科，广州　510250

通讯作者: 廖旺，Email：liaowang@gzhmu.edu.cn
基金资助:
国家自然科学基金青年科学基金项目（82101271）；

广东省基础与应用基础研究基金区域联合基金-青年基金项目（2020A1515110317）；

广东省自然科学基金面上项目（2021A1515010705）；

2020东莞市社会科技发展（一般）项目（202050715023717）

Abstract

Abstract: Objective　To investigate the effect of type 2 diabetes mellitus on leptomeningeal collateral circulation in patients with acute cerebral infarction. Methods　Ninety-four type 2 diabetes patients with acute ischemic cerebral infarction and occlusion or over 85% stenosis of anterior cerebral artery, middle cerebral artery, and internal carotid artery treated at Houjie Hospital from March 1, 2020 to June 30, 2021 were selected as a diabetes and cerebral infarction group, including 51 males and 43 females, and they were (65.02±14.15) years old. Ninety-four patients with acute ischemic cerebral infarction of similar occlusion or stenosis and of similar age were selected as a control group, including 48 males and 46 females, and they were (68.20±12.63) years old. Regional leptomeningeal collateral (rLMC) score was used as an indicator to evaluate the leptomeningeal collateral circulation. The scores of National Institute of Health Stroke Scale (NIHSS) and Alberta Stroke Program Early CT Score (ASPECTS) of the two groups were evaluated. The related factors, such as the age of onset, blood pressure, blood glucose, cholesterol, low-density lipoprotein cholesterol (LDL-C), smoking history, drinking history, and histories of cerebral infarction and coronary heart disease, were compared and analyzed. The correlation regression analysis was carried out. Results　The rLMC score, NIHSS score at admission, and ASPECTS score were (11.55±5.22), (11.99±8.57), and (5.26±2.45) in the diabetes and cerebral infarction group, and were (14.02±4.88), (10.03±8.75), and (6.27±2.53) in the control group, with statistical differences (P=0.001, 0.123, and 0.006). There were statistical differences in blood glucose, smoking history, and drinking history but not in the other indicators at admission between the two groups. Spearman correlation analysis of rLMC score showed that rLMC was significantly correlated with NIHSS score (r=-5.790, P<0.001) and ASPECTS score (r=0.556, P<0.001). Systolic pressure (r=0.207, P=0.045) and diastolic pressure (r=0.213, P=0.040), cholesterol (r=0.244, P=0.018), and LDL-C (r=0.215, P=0.037) were all statistically significant. Age (r=-0.089, P=0.392) and blood glucose (r=-0.292, P=0.120) were not statistically significant. Multiple regression showed that only ASPECTS and NIHSS scores were statistically associated with rLMC. Conclusions　Type 2 diabetes not only significantly affects the establishment of leptomeningeal collateral circulation in patients with acute ischemic cerebral infarction, but also affects the volume of cerebral infarction and the disease severity. In addition to the effects of type 2 diabetes on leptomeningeal collaterals, it is possible that arterial blood pressure (systolic and diastolic pressures), cholesterol, and LDL-C are associated with perfusion of leptomeningeal collateral circulation.

Key words: Type , 2 , diabetes, Leptomeningeal collateral circulation, Acute cerebral infarction, rLMC

摘要： 目的　探讨2型糖尿病对急性脑梗死患者软脑膜侧支循环的影响。方法　选取2020年3月1日至2021年6月30日东莞市厚街医院收治的2型糖尿病合并急性缺血性脑梗死（大脑前动脉、大脑中动脉及颈内动脉颅内段闭塞或狭窄程度大于85%）患者作为研究对象（糖尿病脑梗死组），共94例，其中男51例，女43例，年龄（65.02±14.15）岁。配对选取94例脑血管闭塞或狭窄部位、程度相似、年龄相近的非糖尿病急性缺血性脑梗死患者作为对照组，其中男48例，女46例，年龄（68.20±12.63）岁。采用局部软脑膜侧支循环评分（rLMC）作为评价软脑膜侧支循环指标，对两组患者采用美国国立卫生研究院卒中量表（NIHSS）评分、Alberta卒中项目早期CT评分（ASPECTS），相关因素如患者发病年龄、入院时的血压、血糖、胆固醇、低密度脂蛋白胆固醇（LDL-C）、吸烟史、饮酒史、既往脑梗死病史和冠心病等进行对比分析、相关回归分析等。结果　糖尿病脑梗死组和对照组的rLMC分别为（11.55±5.22）分和（14.02±4.88）分，差异有统计学意义（P=0.001）；入院时NIHSS评分分别为（11.99±8.57）分和（10.03±8.75）分，差异无统计学意义（P=0.123）；ASPECTS分别为（5.26±2.45）分和（6.27±2.53），差异有统计学意义（P=0.006）。入院时血糖和饮酒史有差异外，其余与对照组相比差异均无统计学意义。rLMCS评分的Spearman相关性分析显示：rLMC与NIHSS评分（r=-5.790，P<0.001）和ASPECTS评分（r=0.556，P<0.001）显著相关。收缩压（r=0.207，P=0.045）和舒张压（r=0.213，P=0.040）、胆固醇（r=0.244，P=0.018）、LDL-C（r=0.215，P=0.037），差异均有统计学意义。年龄（r=-0.089，P=0.392）和血糖（r=-0.292，P=0.120）差异均无统计学意义。多元回归显示只有ASPECTS和NIHSS评分跟rLMC有显著相关。结论　2型糖尿病不仅显著影响急性缺血性脑梗死软脑膜侧支循环的建立，而且还影响脑梗死体积和疾病的严重程度。除了2型糖尿病对软脑膜侧支循环的影响外，可能动脉血压（收缩压和舒张压）、胆固醇和LDL-C与软脑膜侧支循环的灌注相关。

关键词: 2型糖尿病, 软脑膜侧支循环, 急性脑梗死, rLMC

Chen Jianjun, Chen Qiaoqiong, Mei Zhizhong, Huang Xiaoyun, Yu Yingli, Lin Han, Huang Yihong, Liao Wang. Effect of type 2 diabetes mellitus on leptomeningeal collateral circulation in patients with acute cerebral infarction[J]. International Medicine and Health Guidance News, 2022, 28(7): 902-907.

陈建军, 陈巧琼, 梅志忠, 黄晓芸, 余映丽, 林菡, 黄益洪, 廖旺. 2型糖尿病对急性脑梗死患者软脑膜侧支循环的影响[J]. 国际医药卫生导报, 2022, 28(7): 902-907.

References

[1] Raymond SB, Schaefer PW. Imaging brain collaterals: quantification, scoring, and potential significance[J]. Top Magn Reson Imaging, 2017,26(2):67-75. DOI: 10.1097/RMR.0000000000000123.

[2] Nishijima Y, Akamatsu Y, Yang SY, et al. Impaired collateral flow compensation during chronic cerebral hypoperfusion in the type 2 diabetic mice[J]. Stroke, 2016,47(12):3014-3021. DOI: 10.1161/STROKEAHA. 116. 014882.

[3] Akamatsu Y, Nishijima Y, Lee CC, et al. Impaired leptomeningeal collateral flow contributes to the poor outcome following experimental stroke in the type 2 diabetic mice[J]. J Neurosci, 2015,35(9):3851-3864. DOI: 10.1523/JNEUROSCI.3838-14.2015.

[4] Sundaram S, Kannoth S, Thomas B, et al. Collateral assessment by CT angiography as a predictor of outcome in symptomatic cervical internal carotid artery occlusion[J]. AJNR Am J Neuroradiol, 2017,38(1):52-57. DOI: 10.3174/ajnr.A4957.

[5] Maurer CJ, Egger K, Dempfle AK, et al. Facing the time window in acute ischemic stroke: the infarct core[J]. Clin Neuroradiol, 2016,26(2):153-158. DOI: 10.1007/s00062- 016-0501-8.

[6] Gersing AS, Schwaiger BJ, Kleine JF, et al. Clinical outcome predicted by collaterals depends on technical success of mechanical thrombectomy in middle cerebral artery occlusion[J]. J Stroke Cerebrovasc Dis, 2017,26(4):801-808. DOI: 10.1016/j.jstrokecerebrovasdis. 2016. 10.020.

[7] Gerber JC, Petrova M, Krukowski P, et al. Collateral state and the effect of endovascular reperfusion therapy on clinical outcome in ischemic stroke patients[J]. Brain Behav, 2016,6(9):e00513. DOI: 10.1002/brb3.513.

[8] Ichijo M, Iwasawa E, Numasawa Y, et al. Significance of development and reversion of collaterals on MRI in early neurologic improvement and long-term functional outcome after intravenous thrombolysis for ischemic stroke[J]. AJNR Am J Neuroradiol, 2015,36(10):1839-1845. DOI: 10.3174/ajnr.A4384.

[9] Kibel A, Selthofer-Relatic K, Drenjancevic I, et al. Coronary microvascular dysfunction in diabetes mellitus[J]. J Int Med Res, 2017,45(6):1901-1929. DOI: 10.1177/0300060516675504.

[10] Sasor A, Ohlsson B. Microangiopathy is common in submucosal vessels of the colon in patients with diabetes mellitus[J]. Rev Diabet Stud, 2014,11(2):175-180. DOI: 10.1900/RDS.2014.11.175.

[11] Sun B, Li X, Liu X, et al. Association between carotid plaque characteristics and acute cerebral infarction determined by MRI in patients with type 2 diabetes mellitus[J]. Cardiovasc Diabetol, 2017,16(1):111. DOI: 10.1186/s12933-017-0592-9.

[12] Karapanayiotides T, Piechowski-Jozwiak B, van Melle G, et al. Stroke patterns, etiology, and prognosis in patients with diabetes mellitus[J]. Neurology, 2004,62(9):1558-1562. DOI: 10.1212/01.wnl.0000123252.55688.05.

[13] Adams HP, del Zoppo G, Alberts MJ, et al.Guidelines for the early management of adults with ischemic stroke: a guideline from the American Heart Association/American Stroke Association Stroke Council, Clinical Cardiology Council, Cardiovascular Radiology and Intervention Council, and the Atherosclerotic Peripheral Vascular Disease and Quality of Care Outcomes in Research Interdisciplinary Working Groups: the American Academy of Neurology affirms the value of this guideline as an educational tool for neurologists[J]. Stroke, 2007,38(5):1655-1711. DOI: 10.1161/STROKEAHA.107. 181486.

[14] Kohner EM, Aldington SJ, Stratton IM, et al. United kingdom prospective diabetes study, 30: diabetic retinopathy at diagnosis of non-insulin-dependent diabetes mellitus and associated risk factors[J]. Arch Ophthalmol, 1998,116(3):297-303. DOI: 10.1001/archopht.116.3.297.

[15] Barber PA, Demchuk AM, Zhang J, et al. Validity and reliability of a quantitative computed tomography score in predicting outcome of hyperacute stroke before thrombolytic therapy. ASPECTS study group. alberta stroke programme early CT score[J]. Lancet, 2000,355(9216):1670-1674. DOI: 10.1016/s0140-6736(00)02237-6.

[16] Menon BK, Smith EE, Modi J, et al. Regional leptomeningeal score on CT angiography predicts clinical and imaging outcomes in patients with acute anterior circulation occlusions[J]. AJNR Am J Neuroradiol, 2011,32(9):1640-1645. DOI: 10.3174/ajnr.A2564.

[17] Zhu S, McClure LA, Lau H, et al. Recurrent vascular events in lacunar stroke patients with metabolic syndrome and/or diabetes[J]. Neurology, 2015,85(11):935-941. DOI: 10.1212/WNL.0000000000001933.

[18] Shah AD, Langenberg C, Rapsomaniki E, et al. Type 2 diabetes and incidence of cardiovascular diseases: a cohort study in 1·9 million people[J]. Lancet Diabetes Endocrinol, 2015,3(2):105-113. DOI: 10.1016/S2213- 8587(14)70219-0.

[19] Kibel A, Selthofer-Relatic K, Drenjancevic I, et al. Coronary microvascular dysfunction in diabetes mellitus[J]. J Int Med Res, 2017,45(6):1901-1929. DOI: 10.1177/0300060516675504.

[20] Shou J, Zhou L, Zhu S, et al. Diabetes is an independent risk factor for stroke recurrence in stroke patients: a meta-analysis[J]. J Stroke Cerebrovasc Dis, 2015,24(9):1961-1968. DOI: 10.1016/j.jstrokecerebrovasdis. 2015. 04.004..

[21] Capes SE, Hunt D, Malmberg K, et al. Stress hyperglycemia and prognosis of stroke in nondiabetic and diabetic patients: a systematic overview[J]. Stroke, 2001,32(10):2426-2432. DOI: 10.1161/hs1001.096194.

[22] Jiang B, Churilov L, Kanesan L, et al. Blood pressure may be associated with arterial collateralization in anterior circulation ischemic stroke before acute reperfusion therapy[J]. J Stroke, 2017,19(2):222-228. DOI: 10.5853/jos.2016.01739.

[23] Tun NN, Arunagirinathan G, Munshi SK, et al. Diabetes mellitus and stroke: a clinical update[J]. World J Diabetes, 2017,8(6):235-248. DOI: 10.4239/wjd.v8.i6.235.

[24] Arsava EM, Vural A, Akpinar E, et al. The detrimental effect of aging on leptomeningeal collaterals in ischemic stroke[J]. J Stroke Cerebrovasc Dis, 2014,23(3):421-426. DOI: 10.1016/j.jstrokecerebrovasdis.2013.03.014.

[25] Menon BK, Smith EE, Coutts SB, et al. Leptomeningeal collaterals are associated with modifiable metabolic risk factors[J]. Ann Neurol, 2013,74(2):241-248. DOI: 10.1002/ana.23906.

Effect of type 2 diabetes mellitus on leptomeningeal collateral circulation in patients with acute cerebral infarction

2型糖尿病对急性脑梗死患者软脑膜侧支循环的影响

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