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Article(id=1199334728051552341, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1199334721185477563, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.0351.2023.0901, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1678118400000, receivedDateStr=2023-03-07, revisedDate=null, revisedDateStr=null, acceptedDate=1680710400000, acceptedDateStr=2023-04-06, onlineDate=1763873281728, onlineDateStr=2025-11-23, pubDate=1714233600000, pubDateStr=2024-04-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1763873281728, onlineIssueDateStr=2025-11-23, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1763873281728, creator=13701087609, updateTime=1763873281728, updator=13701087609, issue=Issue{id=1199334721185477563, tenantId=1146029695717560320, journalId=1189873630562394117, year='2024', volume='49', issue='4', pageStart='367', pageEnd='488', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1763873280092, creator=13701087609, updateTime=1763874025072, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1199337845925183534, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1199334721185477563, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1199337845925183535, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1199334721185477563, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=426, endPage=431, ext={EN=ArticleExt(id=1199334728374513772, articleId=1199334728051552341, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=The changes of serum NGB levels after aSAH and its clinical value in prediction of delayed cerebral ischemia, columnId=1190310109000602400, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Clinical Research, runingTitle=null, highlight=null, articleAbstract=

Objective To investigate the changes of serum neuroglobulin (NGB) levels in patients with aneurysmal subarachnoid hemorrhage (aSAH) and its clinical value in predicting of delayed cerebral ischemia (DCI). Methods A total of 217 patients with aSAH who were diagnosed and treated in the Department of Neurology of Wuwei People's Hospital from October 2019 to October 2022 were selected. They were divided into DCI group and non-DCI group according to the occurrence of DCI after aSAH. The clinical data, and serum NGB levels on day 1 and day 3 after admission were compared between the two groups, and the value of serum NGB in prediction of DCI was evaluated by ROC curve. Logistic regression was used to analyze the risk factors to DCI in aSAH patients. Results DCI occurred in 43 of 217 patients with aSAH (19.8%). Hunt-Hess grade and modified Fisher grade in DCI group were higher than those in non-DCI group (P<0.05). The level of serum NGB in DCI group was higher than that in non-DCI group on day 1 and day 3 after admission (P<0.05), and the levels of serum NGB on day 3 after admission were lower than that on day 1 in two groups (P<0.05). The decrease of serum NGB level in DCI group was lower than that in non-DCI group (P<0.05). ROC curves showed that serum NGB at 3 d after admission predicted a greater AUC for DCI (0.838) than serum NGB at 1 d after admission (0.706)(Z=2.139, P<0.05), with an optimal cutoff of 10.19 ng/ml of serum NGB, the sensitivity and specificity were 74.4% and 86.8% respectively. Logistic regression analysis showed that the risk factors of DCI in patients with aSAH were modified Fisher Grade Ⅲ-Ⅳ (OR=3.790, 95%CI 1.531-9.382), Hunt-Hess grade Ⅲ-Ⅴ(OR=2.448, 95%CI 1.023-5.858) and increased serum NGB at 3 d after admission (OR=1.835, 95%CI 1.496-2.251). Conclusions The serum NGB level is relatively high in patients with DCI after aSAH in the early stage. The serum NGB level, modified Fisher grade, and Hunt-Hess grade are related to the development of DCI after aSAH, and the serum NGB level on 3 d after admission has high predictive value.

, correspAuthors=Li-Shan Ma, authorNote=null, correspAuthorsNote=
E-mail:
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目的 探究动脉瘤性蛛网膜下腔出血(aSAH)患者发病后血清神经球蛋白(NGB)水平变化及其预测迟发性脑缺血(DCI)的临床价值。方法 选取2019年10月-2022年10月武威市人民医院神经科诊治的217例aSAH患者；根据aSAH后是否发生DCI分为DCI组(n=43)与非DCI组(n=174)。比较两组患者临床资料及入院后1 d、3 d的血清NGB水平；采用ROC曲线评估血清NGB水平预测DCI发生的价值；采用logistic回归分析aSAH患者发生DCI的影响因素。结果 217例aSAH患者中发生DCI 43例(19.8%)。DCI组患者Hunt-Hess分级、改良Fisher分级均高于非DCI组(P<0.05)。DCI组患者入院后1 d、3 d血清NGB水平均高于非DCI组(P<0.001)；两组入院后3 d血清NGB水平均较1 d时降低(P<0.001)，且DCI组下降程度低于非DCI组(P<0.001)。ROC曲线分析显示，入院后3 d血清NGB水平预测DCI的AUC(0.838)大于入院后1 d血清NGB(0.706)(Z=2.139，P<0.05)，其最佳临界值为10.19 ng/ml，敏感度为74.4%、特异度为86.8%。logistic回归分析显示，改良Fisher分级Ⅲ-Ⅳ级(OR=3.790，95%CI 1.531~9.382)、Hunt-Hess分级Ⅲ-Ⅴ级(OR=2.448，95%CI 1.023~5.858)、入院后3 d血清NGB水平增高(OR=1.835，95%CI 1.496~2.251)是aSAH患者发生DCI的危险因素(P<0.05)。结论 aSAH后发生DCI的患者早期血清NGB呈相对高水平。血清NGB水平、改良Fisher分级、Hunt-Hess分级均与aSAH后DCI的发生有关，且入院后3 d血清NGB水平对DCI的预测价值较高。

, correspAuthors=马立山, authorNote=null, correspAuthorsNote=
马立山，E-mail：
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李瑾，副主任医师，主要从事神经系统疾病诊治方面的研究

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李瑾，副主任医师，主要从事神经系统疾病诊治方面的研究

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李瑾，副主任医师，主要从事神经系统疾病诊治方面的研究

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Sci Rep, 2019, 9(1): 18799., articleTitle=Effects of exogenous neuroglobin (Ngb) on retinal inflammatory chemokines and microglia in a rat model of transient hypoxia, refAbstract=null), Reference(id=1199334736041701894, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, doi=null, pmid=null, pmcid=null, year=2018, volume=47, issue=4, pageStart=125, pageEnd=129, url=null, language=null, rfNumber=[16], rfOrder=15, authorNames=蒋瑞冲, 王琦伟, 徐敉, journalName=医学研究杂志, refType=null, unstructuredReference=蒋瑞冲, 王琦伟, 徐敉, 等. 急性缺血性脑卒中发病早期血清脑红蛋白和HIF-1α水平变化及意义[J]. 医学研究杂志, 2018, 47(4): 125-129., articleTitle=急性缺血性脑卒中发病早期血清脑红蛋白和HIF-1α水平变化及意义, refAbstract=null), Reference(id=1199334736167531018, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, doi=null, pmid=null, pmcid=null, year=2020, volume=17, issue=1, pageStart=17, pageEnd=25, url=null, language=null, rfNumber=[17], rfOrder=16, authorNames=段婉莹, 刘丽萍, 杨中华, journalName=中国脑血管病杂志, refType=null, unstructuredReference=段婉莹, 刘丽萍, 杨中华, 等. 动脉瘤性蛛网膜下腔出血后迟发性脑缺血的早期凝血及纤溶生物标志物变化[J]. 中国脑血管病杂志, 2020, 17(1): 17-25., articleTitle=动脉瘤性蛛网膜下腔出血后迟发性脑缺血的早期凝血及纤溶生物标志物变化, refAbstract=null), Reference(id=1199334736310137358, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, doi=null, pmid=null, pmcid=null, year=2018, volume=116, issue=null, pageStart=e258, pageEnd=e265, url=null, language=null, rfNumber=[18], rfOrder=17, authorNames=Cai H, Zheng S, Cai B, journalName=World Neurosurg, refType=null, unstructuredReference=Cai H, Zheng S, Cai B, et al. Neuroglobin as a novel biomarker for predicting poor outcomes in aneurysmal subarachnoid hemorrhage[J]. World Neurosurg, 2018, 116: e258-e265., articleTitle=Neuroglobin as a novel biomarker for predicting poor outcomes in aneurysmal subarachnoid hemorrhage, refAbstract=null), Reference(id=1199334736368857617, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, doi=null, pmid=null, pmcid=null, year=2018, volume=9, issue=2, pageStart=163, pageEnd=null, url=null, language=null, rfNumber=[19], rfOrder=18, authorNames=Xiong XX, Pan F, Chen RQ, journalName=Cell Death Dis, refType=null, unstructuredReference=Xiong XX, Pan F, Chen RQ, et al. Neuroglobin boosts axon regeneration during ischemic reperfusion via p38 binding and activation depending on oxygen signal[J]. Cell Death Dis, 2018, 9(2): 163., articleTitle=Neuroglobin boosts axon regeneration during ischemic reperfusion via p38 binding and activation depending on oxygen signal, refAbstract=null), Reference(id=1199334736465326613, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, doi=null, pmid=null, pmcid=null, year=2018, volume=45, issue=4, pageStart=61, pageEnd=64, url=null, language=null, rfNumber=[20], rfOrder=19, authorNames=李涵, 郝东宁, journalName=国际神经病学神经外科学杂志, refType=null, unstructuredReference=李涵, 郝东宁. 眼跳潜伏期预测动脉瘤性蛛网膜下腔出血后迟发性脑缺血的研究[J]. 国际神经病学神经外科学杂志, 2018, 45(4): 61-64., articleTitle=眼跳潜伏期预测动脉瘤性蛛网膜下腔出血后迟发性脑缺血的研究, refAbstract=null), Reference(id=1199334736666653209, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, doi=null, pmid=null, pmcid=null, year=2020, volume=17, issue=4, pageStart=174, pageEnd=180, url=null, language=null, rfNumber=[21], rfOrder=20, authorNames=陈刘炜, 沈睿, 张翔, journalName=中国脑血管病杂志, refType=null, unstructuredReference=陈刘炜, 沈睿, 张翔, 等. 高红细胞分布宽度水平对动脉瘤性蛛网膜下腔出血不良预后的预测价值[J]. 中国脑血管病杂志, 2020, 17(4): 174-180., articleTitle=高红细胞分布宽度水平对动脉瘤性蛛网膜下腔出血不良预后的预测价值, refAbstract=null), Reference(id=1199334736834425375, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, doi=null, pmid=null, pmcid=null, year=2020, volume=42, issue=14, pageStart=1485, pageEnd=1488, url=null, language=null, rfNumber=[22], rfOrder=21, authorNames=陈素云, 赵志新, 杨仙鸿, journalName=浙江医学, refType=null, unstructuredReference=陈素云, 赵志新, 杨仙鸿, 等. NLR和AFR与动脉瘤性蛛网膜下腔出血患者迟发性脑缺血的关系研究[J]. 浙江医学, 2020, 42(14): 1485-1488., articleTitle=NLR和AFR与动脉瘤性蛛网膜下腔出血患者迟发性脑缺血的关系研究, refAbstract=null)], funds=[Fund(id=1199334733323792832, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, awardId=WW2101149, language=EN, fundingSource=Project of Wuwei Science and Technology Plan(WW2101149), fundOrder=null, country=null), Fund(id=1199334733411873221, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, awardId=WW2101149, language=CN, fundingSource=武威市科技计划项目(WW2101149), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1199334729582473415, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, xref=1, ext=[AuthorCompanyExt(id=1199334729595056331, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, companyId=1199334729582473415, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1Department of Neurology, Wuwei, Gansu 733000, China), AuthorCompanyExt(id=1199334729603444940, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, companyId=1199334729582473415, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1武威市人民医院神经内科，甘肃武威 733000)]), AuthorCompany(id=1199334729729274071, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, xref=2, ext=[AuthorCompanyExt(id=1199334729737662681, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, companyId=1199334729729274071, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2Department of Neurosurgery, Wuwei People's Hospital, Wuwei, Gansu 733000, China), AuthorCompanyExt(id=1199334729746051289, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, companyId=1199334729729274071, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2武威市人民医院神经外科，甘肃武威 733000)])], figs=[ArticleFig(id=1199334731910312294, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=EN, label=Fig.1, caption=The ROC curve of the serum level of NGB on prediction of DCI in aSAH patients, figureFileSmall=1TTzeqWdZ1Pq+TJENjZk9A==, figureFileBig=FdInK8VzZMA8txHy2/gWrQ==, tableContent=null), ArticleFig(id=1199334732031947118, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=CN, label=图1, caption=不同时间点血清NGB水平预测aSAH患者发生DCI的ROC曲线

NGB. 神经球蛋白；aSAH. 动脉瘤性蛛网膜下腔出血；DCI. 迟发性脑缺血

, figureFileSmall=1TTzeqWdZ1Pq+TJENjZk9A==, figureFileBig=FdInK8VzZMA8txHy2/gWrQ==, tableContent=null), ArticleFig(id=1199334732266828160, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=EN, label=Fig.2, caption=Visualize forest map of influencing factors of DCI in aSAH patients, figureFileSmall=DoToXCKSimrJKtLx+qKbYw==, figureFileBig=Hku8hDIQAXyXtKdCZ/ZSvA==, tableContent=null), ArticleFig(id=1199334732350714245, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=CN, label=图2, caption=aSAH患者发生DCI的影响因素可视化森林图

aSAH. 动脉瘤性蛛网膜下腔出血；DCI. 迟发性脑缺血；NGB. 神经球蛋白

, figureFileSmall=DoToXCKSimrJKtLx+qKbYw==, figureFileBig=Hku8hDIQAXyXtKdCZ/ZSvA==, tableContent=null), ArticleFig(id=1199334732455571854, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=EN, label=Tab.1, caption=

Comparison of clinical data between aSAH parients in two groups

, figureFileSmall=null, figureFileBig=null, tableContent=
项目

DCI组
(n=43)

非DCI组
(n=174)

t/χ2/ZP
性别[例(%)]0.0700.791
男19(44.2)73(42.0)
女24(55.8)101(58.1)
年龄(岁, $\bar{x}±s$)58.2±12.857.3±11.20.4450.657

发病至入院时间[h,

M(Q1, Q3)]

18(14, 22)17(12, 21)0.4320.666
基础疾病史[例(%)]
高血压病21(48.8)63(36.2)2.3180.128
糖尿病6(14.0)18(10.3)0.4560.499
高脂血症4(9.3)13(7.5)0.1600.689
吸烟[例(%)]16(37.2)57(32.8)0.3060.580
饮酒[例(%)]15(34.9)58(33.3)0.0370.847
责任动脉瘤部位[例(%)]0.0950.758
前循环动脉29(67.4)113(64.9)
后循环动脉14(32.6)61(35.1)
多发性动脉瘤[例(%)]12(27.9)41(23.6)0.3520.553
动脉瘤最大直径[例(%)]1.0450.593
<5 mm15(34.9)67(38.5)
5~10 mm20(46.5)85(48.9)
>10 mm8(18.6)22(12.6)
治疗方式[例(%)]0.6900.708
开颅夹闭15(34.9)51(29.3)
血管内栓塞25(58.1)113(64.9)
非手术治疗3(7.0)10(5.8)
Hunt-Hess分级[例(%)]6.3720.012
Ⅰ-Ⅱ级16(37.2)102(58.6)
Ⅲ-Ⅴ级27(62.8)72(41.4)
改良Fisher分级[例(%)]8.1840.004
Ⅰ-Ⅱ级14(32.6)99(56.9)
Ⅲ-Ⅳ级29(67.4)75(43.1)
脑积水[例(%)]4(9.3)8(4.6)1.4610.227
脑血管痉挛[例(%)]8(18.6)17(9.8)2.6400.104
颅内大动脉狭窄[例(%)]11(25.6)39(22.4)0.1950.659
再出血[例(%)]4(9.3)6(3.5)2.6880.101
), ArticleFig(id=1199334732564623764, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=CN, label=表1, caption=

两组aSAH患者临床资料比较

, figureFileSmall=null, figureFileBig=null, tableContent=
项目

DCI组
(n=43)

非DCI组
(n=174)

t/χ2/ZP
性别[例(%)]0.0700.791
男19(44.2)73(42.0)
女24(55.8)101(58.1)
年龄(岁, $\bar{x}±s$)58.2±12.857.3±11.20.4450.657

发病至入院时间[h,

M(Q1, Q3)]

18(14, 22)17(12, 21)0.4320.666
基础疾病史[例(%)]
高血压病21(48.8)63(36.2)2.3180.128
糖尿病6(14.0)18(10.3)0.4560.499
高脂血症4(9.3)13(7.5)0.1600.689
吸烟[例(%)]16(37.2)57(32.8)0.3060.580
饮酒[例(%)]15(34.9)58(33.3)0.0370.847
责任动脉瘤部位[例(%)]0.0950.758
前循环动脉29(67.4)113(64.9)
后循环动脉14(32.6)61(35.1)
多发性动脉瘤[例(%)]12(27.9)41(23.6)0.3520.553
动脉瘤最大直径[例(%)]1.0450.593
<5 mm15(34.9)67(38.5)
5~10 mm20(46.5)85(48.9)
>10 mm8(18.6)22(12.6)
治疗方式[例(%)]0.6900.708
开颅夹闭15(34.9)51(29.3)
血管内栓塞25(58.1)113(64.9)
非手术治疗3(7.0)10(5.8)
Hunt-Hess分级[例(%)]6.3720.012
Ⅰ-Ⅱ级16(37.2)102(58.6)
Ⅲ-Ⅴ级27(62.8)72(41.4)
改良Fisher分级[例(%)]8.1840.004
Ⅰ-Ⅱ级14(32.6)99(56.9)
Ⅲ-Ⅳ级29(67.4)75(43.1)
脑积水[例(%)]4(9.3)8(4.6)1.4610.227
脑血管痉挛[例(%)]8(18.6)17(9.8)2.6400.104
颅内大动脉狭窄[例(%)]11(25.6)39(22.4)0.1950.659
再出血[例(%)]4(9.3)6(3.5)2.6880.101
), ArticleFig(id=1199334732686258591, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=EN, label=Tab.2, caption=

Comparison of the serum level of NGB between aSAH parients in two groups (ng/ml, $\bar{x}±s$)

, figureFileSmall=null, figureFileBig=null, tableContent=
组别入院后1 d入院后3 dtP
DCI组(n=43)14.41±3.5612.15±3.844.872<0.001
非DCI组(n=174)11.94±2.937.95±2.1232.072<0.001
t4.7356.917
P<0.001<0.001
), ArticleFig(id=1199334732786921893, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=CN, label=表2, caption=

两组aSAH患者血清NGB水平比较(ng/ml， $\bar{x}±s$)

, figureFileSmall=null, figureFileBig=null, tableContent=
组别入院后1 d入院后3 dtP
DCI组(n=43)14.41±3.5612.15±3.844.872<0.001
非DCI组(n=174)11.94±2.937.95±2.1232.072<0.001
t4.7356.917
P<0.001<0.001
), ArticleFig(id=1199334732912751017, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=EN, label=Tab.3, caption=

The ROC curve of the serum level of NGB on prediction of DCI in aSAH patients

, figureFileSmall=null, figureFileBig=null, tableContent=
指标AUC标准误P95%CI最佳临界值(ng/ml)敏感度(%)特异度(%)约登指数
入院后1 d血清NGB0.7060.047<0.0010.613~0.79913.8965.175.30.404
入院后3 d血清NGB0.8380.040<0.0010.758~0.91710.1974.486.80.612
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血清NGB水平预测aSAH患者发生DCI的ROC曲线结果

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指标AUC标准误P95%CI最佳临界值(ng/ml)敏感度(%)特异度(%)约登指数
入院后1 d血清NGB0.7060.047<0.0010.613~0.79913.8965.175.30.404
入院后3 d血清NGB0.8380.040<0.0010.758~0.91710.1974.486.80.612
), ArticleFig(id=1199334733109883317, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=EN, label=Tab.4, caption=

The result of multivariate logistic regression analysis of DCI in aSAH patients

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因素BSEWald自由度POR95%CI
入院后3 d血清NGB0.6070.10433.8911<0.0011.8351.496~2.251
改良Fisher分级Ⅲ-Ⅳ级1.3320.4628.30210.0043.7901.531~9.382
Hunt-Hess分级Ⅲ-Ⅴ级0.8950.4454.04110.0442.4481.023~5.858
), ArticleFig(id=1199334733214740922, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1199334728051552341, language=CN, label=表4, caption=

aSAH患者发生DCI的多因素logistic回归分析结果

, figureFileSmall=null, figureFileBig=null, tableContent=
因素BSEWald自由度POR95%CI
入院后3 d血清NGB0.6070.10433.8911<0.0011.8351.496~2.251
改良Fisher分级Ⅲ-Ⅳ级1.3320.4628.30210.0043.7901.531~9.382
Hunt-Hess分级Ⅲ-Ⅴ级0.8950.4454.04110.0442.4481.023~5.858
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aSAH患者血清神经球蛋白水平变化及其预测迟发性脑缺血的临床价值
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李瑾 1 , 马立山 2, *
解放军医学杂志 | 临床研究 2024,49(4): 426-431
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解放军医学杂志 | 临床研究 2024, 49(4): 426-431
aSAH患者血清神经球蛋白水平变化及其预测迟发性脑缺血的临床价值
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李瑾1, 马立山2, *
作者信息
  • 1武威市人民医院神经内科，甘肃武威 733000
  • 2武威市人民医院神经外科，甘肃武威 733000

    • 李瑾，副主任医师，主要从事神经系统疾病诊治方面的研究

通讯作者:

马立山，E-mail：
The changes of serum NGB levels after aSAH and its clinical value in prediction of delayed cerebral ischemia
Jin Li1, Li-Shan Ma2, *
Affiliations
  • 1Department of Neurology, Wuwei, Gansu 733000, China
  • 2Department of Neurosurgery, Wuwei People's Hospital, Wuwei, Gansu 733000, China
出版时间: 2024-04-28 doi: 10.11855/j.issn.0577-7402.0351.2023.0901
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摘要
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目的 探究动脉瘤性蛛网膜下腔出血(aSAH)患者发病后血清神经球蛋白(NGB)水平变化及其预测迟发性脑缺血(DCI)的临床价值。方法 选取2019年10月-2022年10月武威市人民医院神经科诊治的217例aSAH患者；根据aSAH后是否发生DCI分为DCI组(n=43)与非DCI组(n=174)。比较两组患者临床资料及入院后1 d、3 d的血清NGB水平；采用ROC曲线评估血清NGB水平预测DCI发生的价值；采用logistic回归分析aSAH患者发生DCI的影响因素。结果 217例aSAH患者中发生DCI 43例(19.8%)。DCI组患者Hunt-Hess分级、改良Fisher分级均高于非DCI组(P<0.05)。DCI组患者入院后1 d、3 d血清NGB水平均高于非DCI组(P<0.001)；两组入院后3 d血清NGB水平均较1 d时降低(P<0.001)，且DCI组下降程度低于非DCI组(P<0.001)。ROC曲线分析显示，入院后3 d血清NGB水平预测DCI的AUC(0.838)大于入院后1 d血清NGB(0.706)(Z=2.139，P<0.05)，其最佳临界值为10.19 ng/ml，敏感度为74.4%、特异度为86.8%。logistic回归分析显示，改良Fisher分级Ⅲ-Ⅳ级(OR=3.790，95%CI 1.531~9.382)、Hunt-Hess分级Ⅲ-Ⅴ级(OR=2.448，95%CI 1.023~5.858)、入院后3 d血清NGB水平增高(OR=1.835，95%CI 1.496~2.251)是aSAH患者发生DCI的危险因素(P<0.05)。结论 aSAH后发生DCI的患者早期血清NGB呈相对高水平。血清NGB水平、改良Fisher分级、Hunt-Hess分级均与aSAH后DCI的发生有关，且入院后3 d血清NGB水平对DCI的预测价值较高。

动脉瘤性蛛网膜下腔出血  /  迟发性脑缺血  /  神经球蛋白  /  预测

Objective To investigate the changes of serum neuroglobulin (NGB) levels in patients with aneurysmal subarachnoid hemorrhage (aSAH) and its clinical value in predicting of delayed cerebral ischemia (DCI). Methods A total of 217 patients with aSAH who were diagnosed and treated in the Department of Neurology of Wuwei People's Hospital from October 2019 to October 2022 were selected. They were divided into DCI group and non-DCI group according to the occurrence of DCI after aSAH. The clinical data, and serum NGB levels on day 1 and day 3 after admission were compared between the two groups, and the value of serum NGB in prediction of DCI was evaluated by ROC curve. Logistic regression was used to analyze the risk factors to DCI in aSAH patients. Results DCI occurred in 43 of 217 patients with aSAH (19.8%). Hunt-Hess grade and modified Fisher grade in DCI group were higher than those in non-DCI group (P<0.05). The level of serum NGB in DCI group was higher than that in non-DCI group on day 1 and day 3 after admission (P<0.05), and the levels of serum NGB on day 3 after admission were lower than that on day 1 in two groups (P<0.05). The decrease of serum NGB level in DCI group was lower than that in non-DCI group (P<0.05). ROC curves showed that serum NGB at 3 d after admission predicted a greater AUC for DCI (0.838) than serum NGB at 1 d after admission (0.706)(Z=2.139, P<0.05), with an optimal cutoff of 10.19 ng/ml of serum NGB, the sensitivity and specificity were 74.4% and 86.8% respectively. Logistic regression analysis showed that the risk factors of DCI in patients with aSAH were modified Fisher Grade Ⅲ-Ⅳ (OR=3.790, 95%CI 1.531-9.382), Hunt-Hess grade Ⅲ-Ⅴ(OR=2.448, 95%CI 1.023-5.858) and increased serum NGB at 3 d after admission (OR=1.835, 95%CI 1.496-2.251). Conclusions The serum NGB level is relatively high in patients with DCI after aSAH in the early stage. The serum NGB level, modified Fisher grade, and Hunt-Hess grade are related to the development of DCI after aSAH, and the serum NGB level on 3 d after admission has high predictive value.

aneurysmal subarachnoid hemorrhage  /  delayed cerebral ischemia  /  neuroglobulin  /  prediction
李瑾, 马立山. aSAH患者血清神经球蛋白水平变化及其预测迟发性脑缺血的临床价值. 解放军医学杂志, 2024 , 49 (4) : 426 -431 . DOI: 10.11855/j.issn.0577-7402.0351.2023.0901
Jin Li, Li-Shan Ma. The changes of serum NGB levels after aSAH and its clinical value in prediction of delayed cerebral ischemia[J]. Medical Journal of Chinese People’s Liberation Army, 2024 , 49 (4) : 426 -431 . DOI: 10.11855/j.issn.0577-7402.0351.2023.0901
正文
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蛛网膜下腔出血(subarachnoid hemorrhage，SAH)约占卒中的10%，其中动脉瘤性SAH(aneurysmal SAH，aSAH)占比>80%[1-2]。迟发性脑缺血(delayed cerebral ischemia，DCI)是aSAH发病后的常见并发症，多数发生于aSAH后14 d内，可造成不可逆脑损伤，被认为是aSAH致残、致死的重要原因[3]。我国一项全国性、多中心、前瞻性研究显示，aSAH后的DCI可导致功能预后变差和出院时及出院后3、6、12个月的病死率增高[4]。因此，早期预测及防治至关重要。但DCI发病机制、病理生理过程复杂，常规判断可能存在滞后性，因而探寻早期、客观的标志物辅助早期预测成为研究热点。相关研究显示，缺氧缺血性损伤引起的血栓、微血管功能障碍等可影响DCI的发生与进展[5]。神经球蛋白(neuroglobin，NGB)是以单体形式存在于神经细胞的携氧蛋白，在缺氧缺血性损伤时水平增高。有研究显示NGB与缺血性卒中病情、aSAH患者功能及预后有关[6-7]，但关于DCI的研究尚少。本研究探讨aSAH患者血清NGB水平变化及其预测DCI的价值，旨在为相关的临床应用及DCI的防治提供依据。
1 资料与方法
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1.1 研究对象
选取2019年10月-2022年10月武威市人民医院神经科诊治的aSAH患者217例。纳入标准：(1)aSAH诊断符合《中国动脉瘤性蛛网膜下腔出血诊疗指导规范》[8]中的标准，且经CT血管造影(CT angiography，CTA)或数字减影血管造影(digital subtraction angiography，DSA)检查确诊；(2)首次发病；(3)发病至入院时间<48 h；(4)年龄>18岁。排除标准：(1)其他病因导致的SAH，如动静脉畸形、外伤出血等；(2)入院时影像学证据和(或)临床症状提示已发生或疑似DCI，或入院3 d内疑似或确定发生DCI；(3)发病时间不明确；(4)合并心、肝、肾等原发性脏器疾病；(5)感染性疾病，其他恶性肿瘤及血液、免疫系统疾病；(6)行两种手术治疗；(7)入院7 d内死亡；(8)近1个月使用过抗血小板、抗凝药物或免疫抑制药。217例患者中，男92例，女125例；年龄28~83(57.5±11.5)岁；发病至入院时间4~36 h，中位数为17(12，21) h；责任动脉瘤部位为前循环动脉142例，后循环动脉75例；多发性动脉瘤53例；接受血管内栓塞治疗138例，开颅夹闭治疗66例，非手术治疗13例。本研究经武威市人民医院伦理道德委员会批准(WW2101149)，患者或其家属签署知情同意书。
1.2 方法
1.2.1 资料收集
患者入院后24 h内收集其人口学信息(性别、年龄等)、基础疾病史(高血压病、糖尿病、高脂血症等)、个人行为(吸烟、饮酒等)、神经系统状态(Hunt-Hess分级、改良Fisher分级等)、动脉瘤情况(责任动脉瘤部位、多发性动脉瘤、动脉瘤最大直径等)、治疗方式(开颅夹闭、血管内栓塞、非手术治疗等，均由神经外科、神经内科、神经介入科等多学科评估讨论决定)，并统计发病至入院时间；跟踪统计颅内大动脉狭窄、脑积水、脑血管痉挛、再出血等情况。
1.2.2 血清NGB检测
分别在患者入院后1 d、3 d抽取外周肘静脉血2 ml于乙二胺四乙酸试管中，室温下离心15 min(1000×g)，收集上清-80 °C存储；6 h内采用酶联免疫吸附试验(ELISA)测定血清NGB水平，试剂购自武汉巴菲尔生物技术公司。
1.3 DCI诊断及分组
随访患者直至发生DCI或aSAH后1个月。DCI诊断标准[9]：(1)新发局灶性神经功能受损(失语、偏盲、偏瘫等)和(或)意识水平降低 [格拉斯哥昏迷评分(Glasgow coma scale，GCS)单项或总分下降≥2分] 且持续>1 h(并非术后立即发生)；(2)动态复查头部CT报告新发梗死病灶，与临床症状及体征对应，且对比确证新发病灶在发病后首次CT及术后CT复查中并未出现；(3)排除了导致恶化或低密度灶的其他原因(脑实质出血、脑积水、感染、癫痫等)。由患者住院期间的主治医师及神经功能监护组完成DCI的诊断。根据有无发生DCI将患者分为DCI组(n=43)与非DCI组(n=174)。
1.4 统计学处理
采用SPSS 22.0软件进行统计分析。计数资料以例(%)表示，两组间比较采用χ2检验；计量资料服从正态分布者以$\bar{x}±s$表示，两组间比较采用t检验，非正态分布者以M(Q1，Q3)表示，两组间比较采用非参数检验。采用多因素logistic回归分析aSAH患者发生DCI的影响因素；采用受试者工作特征曲线(receiver operator characteristic curve，ROC)评估血清NGB水平预测DCI发生的价值，曲线下面积(area under curve，AUC)为0.7~0.9提示有一定预测准确度，AUC比较采用De-long检验。P<0.05为差异有统计学意义。
2 结果
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2.1 aSAH后DCI发生情况
aSAH患者217例中，发生DCI 43例(19.8%)，未发生DCI 174例(80.2%)。DCI发生时间为aSAH发病后5~17(8.81±2.61) d。
2.2 两组临床资料比较
DCI组患者Hunt-Hess分级、改良Fisher分级明显高于非DCI组(P<0.05)；两组性别、年龄、发病至入院时间、基础疾病史、吸烟、饮酒、责任动脉瘤部位、多发性动脉瘤、动脉瘤最大直径、治疗方式、脑积水、脑血管痉挛、颅内大动脉狭窄、再出血情况等比较差异均无统计学意义(P>0.05，表1)。
2.3 两组血清NGB水平比较
DCI组患者入院后1 d、3 d血清NGB水平均明显高于非DCI组(P<0.001)；两组入院后3 d血清NGB水平均较1 d时降低(P<0.001)，且DCI组血清NGB水平下降程度低于非DCI组[(2.26±3.04) ng/ml vs. (3.99±1.64) ng/ml，t=3.605，P<0.01](表2)。
2.4 血清NGB水平预测aSAH患者发生DCI的ROC曲线分析
ROC曲线分析显示，入院后3 d血清NGB水平预测DCI的AUC(0.838)大于入院后1 d血清NGB(0.706)(Z=2.139，P=0.032)；入院后3 d血清NGB水平预测的最佳临界值为10.19 ng/ml，敏感度为74.4%、特异度为86.8%，预测价值更高(图1，表3)。
2.5 aSAH患者发生DCI的多因素logistic回归分析
以有无发生DCI为因变量(赋值：DCI=1，非DCI=0)，以表1中P<0.05的变量和入院后3 d血清NGB为自变量(改良Fisher分级赋值：Ⅲ-Ⅳ级=1，Ⅰ-Ⅱ级=0；Hunt-Hess分级赋值：Ⅲ-Ⅴ级=1，Ⅰ-Ⅱ级=0)，纳入多因素logistic回归分析。结果显示，改良Fisher分级Ⅲ-Ⅳ级、Hunt-Hess分级Ⅲ-Ⅴ级、入院后3 d血清NGB水平增高是aSAH患者发生DCI的危险因素(P<0.05，图2，表4)。
3 讨论
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DCI是影响aSAH患者预后的重要并发症。Olsen等[10]的回顾性队列研究显示，492例aSAH患者的DCI发生率为23%，未发生DCI的aSAH患者具有更好的功能结局，DCI与长期病死率相关。本研究217例aSAH患者中发生DCI 43例(19.8%)，与上述报道接近；但低于张魁等[11]的结果(47.5%)，考虑与病例入选范围、病情程度、个体差异等有关。DCI的发病机制复杂，尚未完全明确。现代医学研究认为，导致DCI的关键过程之一在于缺氧缺血性脑损伤，其由微血管血栓、微循环障碍、脑血管痉挛等血管事件引起[12]。aSAH后脑血管中一氧化氮水平下降，抑制了一氧化氮合酶的活性，进而促进血小板聚集，引起血管痉挛；微血管痉挛程度加重，导致相应的脑血流量下降，继而诱发凝血级联反应，造成微血栓，加之脑微循环灌注不足，从而发生脑缺血[13-14]。由于DCI发生时间尚不明确，因此，早期预测是及时防治DCI和逆转损伤的关键。
NGB是具有较高氧亲和力的脑特异性血蛋白，在缺氧缺血性脑损伤中起神经保护作用。动物体内模型实验结果显示，在急性缺血缺氧时NGB水平升高，干预调节后其水平呈下降趋势[15]。蒋瑞冲等[16]发现，NGB水平在发病24 h后明显升高，与缺血性卒中评分及预后有关。在脑组织缺氧缺血时，神经细胞需产生更多的NGB帮助神经组织摄取、运输氧，清除活性氮、活性氧，维持细胞稳态，抵抗缺血缺氧损害[17]。故NGB水平升高也间接提示需要对抗的缺血缺氧损害程度较重，这也是本研究中DCI组血清NGB水平高于非DCI组的可能原因。Cai等[18]研究也显示，aSAH后血清NGB水平升高，在第2天达峰值后逐渐下降；NGB水平预测6个月不良结局的AUC为0.818，是独立预测因子(OR=1.919，95%CI 1.158~3.180)；提示NGB水平对aSAH预后有一定预测价值。本研究结果显示，aSAH患者入院后3 d血清NGB水平预测DCI的AUC(0.838)大于入院后1 d血清NGB(0.706)，其最佳临界值为10.19 ng/ml，敏感度为74.4%，特异度为86.8%。即当入院后3 d的NGB≥10.19 ng/ml时，aSAH患者发生DCI的危险性较高。除与上述原因有关外，考虑还与促轴突再生有关。Xiong等[19]发现，NGB在缺血/再灌注期间可通过O2-Ngb-p38-GAP43信号转导促进轴突再生，对治疗应用具有潜在价值。
既往多项研究显示，Fisher分级、Hunt-Hess分级与aSAH后DCI的发生有关，本研究结果与之一致[20-21]。本研究中logistic回归分析结果显示，改良Fisher分级Ⅲ-Ⅳ级(OR=3.790，95%CI 1.531~9.382)、Hunt-Hess分级Ⅲ-Ⅴ级(OR=2.448，95%CI 1.023~5.858)、血清NGB水平增高(OR=1.835，95%CI 1.496~2.251)是aSAH患者发生DCI的危险因素，提示临床应加强早期评估与监测。陈素云等[22]研究显示，年龄在有无DCI组中存在差异；本研究结果未检出该项差异，考虑与患者个体差异、病例入选年龄差距等有关。
综上所述，aSAH后发生DCI的患者早期血清NGB呈相对高水平，NGB、改良Fisher分级、Hunt-Hess分级均与aSAH后DCI的发生有关，且入院后3 d血清NGB对DCI具有较高的预测价值，可在临床推荐应用。因本研究为单中心研究，病例入选范围受限，可能导致结果的偏倚；同时为减轻患者的应激反应，仅在患者入院后1 d、3 d采集血样检测，未观察密集时点的血清NGB动态变化，故相关研究结论有待进一步扩大病例入选范围，进行多中心、多时点的检验和验证。
基金
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  • 武威市科技计划项目(WW2101149)
文献
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2024年第49卷第4期
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doi: 10.11855/j.issn.0577-7402.0351.2023.0901
  • 接收时间：2023-03-07
  • 首发时间：2025-11-23
  • 出版时间：2024-04-28
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  • 收稿日期：2023-03-07
  • 录用日期：2023-04-06
基金
Project of Wuwei Science and Technology Plan(WW2101149)
武威市科技计划项目(WW2101149)
作者信息
    1武威市人民医院神经内科，甘肃武威 733000
    2武威市人民医院神经外科，甘肃武威 733000

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鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
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