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Article(id=1209198310695506107, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1209198303988813828, articleNumber=null, orderNo=null, doi=10.11855/j.issn.0577-7402.2021.06.02, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1612454400000, receivedDateStr=2021-02-05, revisedDate=1620489600000, revisedDateStr=2021-05-09, acceptedDate=null, acceptedDateStr=null, onlineDate=1766224943087, onlineDateStr=2025-12-20, pubDate=1624809600000, pubDateStr=2021-06-28, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1766224943087, onlineIssueDateStr=2025-12-20, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1766224943087, creator=13701087609, updateTime=1766224943087, updator=13701087609, issue=Issue{id=1209198303988813828, tenantId=1146029695717560320, journalId=1189873630562394117, year='2021', volume='46', issue='6', pageStart='531', pageEnd='636', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1766224941489, creator=13701087609, updateTime=1766225124231, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1209199070531424860, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1209198303988813828, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1209199070531424861, tenantId=1146029695717560320, journalId=1189873630562394117, issueId=1209198303988813828, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=538, endPage=544, ext={EN=ArticleExt(id=1209198310972330193, articleId=1209198310695506107, tenantId=1146029695717560320, journalId=1189873630562394117, language=EN, title=Effect of resveratrol on vascular repair after carotid balloon injury in rats, columnId=1190310110212751762, journalTitle=Medical Journal of Chinese People’s Liberation Army, columnName=Basic Research, runingTitle=null, highlight=null, articleAbstract=

Objective To understand the effect of resveratrol (RSV) on vascular repair after the common carotid balloon injury in rats. Methods Forty SD rats were randomized into four groups (n=10): sham group, model group, solvent control group(DSMO group) and RSV group. After establishing the carotid artery balloon injury model, the rats in model group had no special treatment, while the rats in DMSO group and RSV group were given the same dose of DMSO or RSV respectively at the outside of the adventitia of carotid balloon injury segments. The rats in sham group received external carotid artery ligation. Fourteen days after the surgery, excessive anesthesia was applied to rats. The injured segments of the carotid arteries were collected, followed by HE staining to observe the degree of vascular intimal hyperplasia and stenosis. The expression of CD31 using immunohistochemical staining was detected to evaluate the degree of the re-endothelialization, and Western blotting was used to detect the expression levels of vascular endothelial growth factor (VEGF) in the arterial tissues. Results HE staining results showed that there was no significant difference in EEL circumference, EEL area and IEL area between groups (P>0.05); compared with sham group and DMSO group, the lumen area of RSV group decreased significantly (P<0.05). Compared with sham group, the degree of intimal hyperplasia increased in model group and RSV group (P<0.05); compared with model group, the degree of intimal hyperplasia decreased in DMSO group (P<0.05); compared with DMSO group, the degree of intimal hyperplasia increased in RSV group(P<0.05). Compared with sham group, the degree of stenosis in model group and RSV group were significantly higher (P<0.05); compared with model group, the degree of stenosis in DMSO group decreased significantly (P<0.05); compared with DMSO group, the degree of stenosis in RSV group was significantly higher (P<0.05). CD31 immunohistochemical staining results showed that the expression of CD31 in model group was significantly lower than that in sham group (P<0.05), and the expression of CD31 in RSV group was significantly higher than that in model group (P<0.05). Western blotting results showed that the expression of VEGF in model group significantly decreased than that in sham group (P<0.05); compared with model group and DMSO group, the expression of VEGF in RSV group significantly enhanced (P<0.05). Conclusion RSV can promote vascular repair and intimal hyperplasia, and enhance re-endothelialization after the common carotid balloon injury in rats, and the mechanism may be related to the proliferation and migration of adjacent resident endothelial cells and the recruitment of bone marrow endothelial cells or circulating endothelial cells.

, correspAuthors=Jian-Juan Ke, authorNote=null, correspAuthorsNote=
*E-mail:
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目的 探讨白藜芦醇(RSV)对颈总动脉球囊损伤术后大鼠血管的修复作用。方法 将40只SD大鼠随机分为假手术组、模型组、溶剂对照组(DSMO组)与RSV组，每组10只。制备左颈总动脉球囊损伤模型后，模型组不给药，DMSO组和RSV组在颈总动脉球囊损伤段外周分别给予相同剂量的溶剂DMSO和RSV。假手术组仅结扎颈外动脉。14 d后过量麻醉处死大鼠，取颈总动脉损伤段组织，HE染色观察血管内膜增生程度和管腔狭窄程度，CD31免疫组织化学染色评估血管再内皮化程度，Western blotting检测动脉组织中血管内皮生长因子(VEGF)的表达水平。结果 HE染色结果显示，各组外膜以内区(EEL)周长、EEL面积以及内膜及内区(IEL)面积差异无统计学意义(P>0.05)；与假手术组和DMSO组相比，RSV组管腔面积明显减小(P<0.05)。与假手术组相比，模型组和RSV组的内膜增生程度加重(P<0.05)；与模型组相比，DMSO组内膜增生程度减轻(P<0.05)；与DMSO组相比，RSV组内膜增生程度加重(P<0.05)。与假手术组相比，模型组和RSV组管腔狭窄程度加重(P<0.05)；与模型组相比，DMSO组管腔狭窄程度减轻(P<0.05)；与DMSO组相比，RSV组管腔狭窄程度加重(P<0.05)。CD31免疫组织化学染色结果显示，与假手术组相比，模型组CD31表达减弱(P<0.05)；与模型组相比，RSV组CD31表达明显增强(P<0.05)。Western blotting检测结果显示，与假手术组相比，模型组动脉组织中VEGF表达水平明显降低(P<0.05)；与模型组和DMSO组相比，RSV组动脉组织中VEGF表达水平明显增高(P<0.05)。结论 RSV在大鼠颈总动脉球囊损伤术后短期内可促进血管新生、内膜再生及增强再内皮化程度，其机制可能与邻近驻留内皮细胞的增殖、迁移，骨髓内皮细胞或循环内皮细胞的募集有关。

, correspAuthors=柯剑娟, authorNote=null, correspAuthorsNote=
柯剑娟，E-mail：
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罗兰，医学硕士，主要从事血管介入术后再狭窄方面的研究

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罗兰，医学硕士，主要从事血管介入术后再狭窄方面的研究

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罗兰，医学硕士，主要从事血管介入术后再狭窄方面的研究

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A. 各组大鼠颈总动脉横切面HE染色(×40)；B. EEL周长；C. EEL面积；D. IEL面积；E. 管腔面积；F. 内膜增生程度；G. 管腔狭窄程度；RSV. 白藜芦醇；EEL. 外膜以内区；IEL. 内膜及内区；与假手术组比较，(1)P<0.05；与模型组比较，(2)P<0.05；与DMSO组比较，(3)P<0.05。

, figureFileSmall=NeMYZSNEq9JFWo81NjlwLQ==, figureFileBig=cSYor5yLS/U8JZSw2DAM9A==, tableContent=null), ArticleFig(id=1209198317997789672, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1209198310695506107, language=EN, label=Fig.2, caption=Effect of RSV on vascular reendothelialization in rats with common carotid artery balloon injury (n=3), figureFileSmall=oyAB9LxCoXZAxdxSsD/Y/A==, figureFileBig=1cmW3m1to6k22THVGQ+xgw==, tableContent=null), ArticleFig(id=1209198318069092844, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1209198310695506107, language=CN, label=图2, caption=RSV对颈总动脉球囊损伤模型大鼠血管再内皮化的影响(n=3)

A. 各组大鼠颈总动脉横切面CD31免疫组织化学染色(×40)；B. Barnes评分；RSV. 白藜芦醇；与假手术组比较，(1)P<0.05；与模型组比较，(2)P<0.05。

, figureFileSmall=oyAB9LxCoXZAxdxSsD/Y/A==, figureFileBig=1cmW3m1to6k22THVGQ+xgw==, tableContent=null), ArticleFig(id=1209198318165561841, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1209198310695506107, language=EN, label=Fig.3, caption=Comparison of the relative expression level of VEGF protein in common carotid artery tissues (Western blotting, n=6), figureFileSmall=wPirAi+hqA1ONXkfTy85ZQ==, figureFileBig=k2x0MSNk5Df9+CrMDaj1rg==, tableContent=null), ArticleFig(id=1209198318249447922, tenantId=1146029695717560320, journalId=1189873630562394117, articleId=1209198310695506107, language=CN, label=图3, caption=各组颈总动脉组织中VEGF蛋白相对表达量比较(Western blotting，n=6)

与假手术组比较，(1)P<0.05；与模型组比较，(2)P<0.05；与DMSO组比较，(3)P<0.05。

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白藜芦醇对颈总动脉球囊损伤术后大鼠血管的修复作用
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罗兰 , 熊颖 , 国奥 , 陈春意 , 夏韵 , 李靖凡 , 卢清 , 柯剑娟 *
解放军医学杂志 | 基础研究 2021,46(6): 538-544
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解放军医学杂志 | 基础研究 2021, 46(6): 538-544
白藜芦醇对颈总动脉球囊损伤术后大鼠血管的修复作用
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罗兰, 熊颖, 国奥, 陈春意, 夏韵, 李靖凡, 卢清, 柯剑娟*
作者信息
  • 武汉大学中南医院麻醉科，武汉 430071

    • 罗兰，医学硕士，主要从事血管介入术后再狭窄方面的研究

通讯作者:

柯剑娟，E-mail：
Effect of resveratrol on vascular repair after carotid balloon injury in rats
Lan Luo, Ying Xiong, Ao Guo, Chun-Yi Chen, Yun Xia, Jing-Fan Li, Qing Lu, Jian-Juan Ke*
Affiliations
  • Department of Anesthesiology, Zhongnan Hospital of Wuhan University, Wuhan 430071, China
出版时间: 2021-06-28 doi: 10.11855/j.issn.0577-7402.2021.06.02
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摘要
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目的 探讨白藜芦醇(RSV)对颈总动脉球囊损伤术后大鼠血管的修复作用。方法 将40只SD大鼠随机分为假手术组、模型组、溶剂对照组(DSMO组)与RSV组，每组10只。制备左颈总动脉球囊损伤模型后，模型组不给药，DMSO组和RSV组在颈总动脉球囊损伤段外周分别给予相同剂量的溶剂DMSO和RSV。假手术组仅结扎颈外动脉。14 d后过量麻醉处死大鼠，取颈总动脉损伤段组织，HE染色观察血管内膜增生程度和管腔狭窄程度，CD31免疫组织化学染色评估血管再内皮化程度，Western blotting检测动脉组织中血管内皮生长因子(VEGF)的表达水平。结果 HE染色结果显示，各组外膜以内区(EEL)周长、EEL面积以及内膜及内区(IEL)面积差异无统计学意义(P>0.05)；与假手术组和DMSO组相比，RSV组管腔面积明显减小(P<0.05)。与假手术组相比，模型组和RSV组的内膜增生程度加重(P<0.05)；与模型组相比，DMSO组内膜增生程度减轻(P<0.05)；与DMSO组相比，RSV组内膜增生程度加重(P<0.05)。与假手术组相比，模型组和RSV组管腔狭窄程度加重(P<0.05)；与模型组相比，DMSO组管腔狭窄程度减轻(P<0.05)；与DMSO组相比，RSV组管腔狭窄程度加重(P<0.05)。CD31免疫组织化学染色结果显示，与假手术组相比，模型组CD31表达减弱(P<0.05)；与模型组相比，RSV组CD31表达明显增强(P<0.05)。Western blotting检测结果显示，与假手术组相比，模型组动脉组织中VEGF表达水平明显降低(P<0.05)；与模型组和DMSO组相比，RSV组动脉组织中VEGF表达水平明显增高(P<0.05)。结论 RSV在大鼠颈总动脉球囊损伤术后短期内可促进血管新生、内膜再生及增强再内皮化程度，其机制可能与邻近驻留内皮细胞的增殖、迁移，骨髓内皮细胞或循环内皮细胞的募集有关。

内膜增生  /  白藜芦醇  /  再狭窄  /  血管修复  /  再内皮化

Objective To understand the effect of resveratrol (RSV) on vascular repair after the common carotid balloon injury in rats. Methods Forty SD rats were randomized into four groups (n=10): sham group, model group, solvent control group(DSMO group) and RSV group. After establishing the carotid artery balloon injury model, the rats in model group had no special treatment, while the rats in DMSO group and RSV group were given the same dose of DMSO or RSV respectively at the outside of the adventitia of carotid balloon injury segments. The rats in sham group received external carotid artery ligation. Fourteen days after the surgery, excessive anesthesia was applied to rats. The injured segments of the carotid arteries were collected, followed by HE staining to observe the degree of vascular intimal hyperplasia and stenosis. The expression of CD31 using immunohistochemical staining was detected to evaluate the degree of the re-endothelialization, and Western blotting was used to detect the expression levels of vascular endothelial growth factor (VEGF) in the arterial tissues. Results HE staining results showed that there was no significant difference in EEL circumference, EEL area and IEL area between groups (P>0.05); compared with sham group and DMSO group, the lumen area of RSV group decreased significantly (P<0.05). Compared with sham group, the degree of intimal hyperplasia increased in model group and RSV group (P<0.05); compared with model group, the degree of intimal hyperplasia decreased in DMSO group (P<0.05); compared with DMSO group, the degree of intimal hyperplasia increased in RSV group(P<0.05). Compared with sham group, the degree of stenosis in model group and RSV group were significantly higher (P<0.05); compared with model group, the degree of stenosis in DMSO group decreased significantly (P<0.05); compared with DMSO group, the degree of stenosis in RSV group was significantly higher (P<0.05). CD31 immunohistochemical staining results showed that the expression of CD31 in model group was significantly lower than that in sham group (P<0.05), and the expression of CD31 in RSV group was significantly higher than that in model group (P<0.05). Western blotting results showed that the expression of VEGF in model group significantly decreased than that in sham group (P<0.05); compared with model group and DMSO group, the expression of VEGF in RSV group significantly enhanced (P<0.05). Conclusion RSV can promote vascular repair and intimal hyperplasia, and enhance re-endothelialization after the common carotid balloon injury in rats, and the mechanism may be related to the proliferation and migration of adjacent resident endothelial cells and the recruitment of bone marrow endothelial cells or circulating endothelial cells.

intimal hyperplasia  /  resveratrol  /  restenosis  /  vascular repair  /  re-endothelialization
罗兰, 熊颖, 国奥, 陈春意, 夏韵, 李靖凡, 卢清, 柯剑娟. 白藜芦醇对颈总动脉球囊损伤术后大鼠血管的修复作用. 解放军医学杂志, 2021 , 46 (6) : 538 -544 . DOI: 10.11855/j.issn.0577-7402.2021.06.02
Lan Luo, Ying Xiong, Ao Guo, Chun-Yi Chen, Yun Xia, Jing-Fan Li, Qing Lu, Jian-Juan Ke. Effect of resveratrol on vascular repair after carotid balloon injury in rats[J]. Medical Journal of Chinese People’s Liberation Army, 2021 , 46 (6) : 538 -544 . DOI: 10.11855/j.issn.0577-7402.2021.06.02
正文
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过去十年，由于药物洗脱支架技术的进展[1]，短期内血管内再狭窄发生率逐年下降，但继发的支架内再狭窄发生率上升[2]。有研究发现，药物洗脱支架破坏了内皮的功能和完整性，不利于内皮再生，从而造成内皮持续性炎症、内皮化不完全、动脉愈合延迟，形成继发的血栓相关血管内狭窄[3-4]。血管内膜增生过度亦可限制管腔血流，导致血管再狭窄[5]。白藜芦醇(resveratrol，RSV)是一种天然的植物多酚，具有抗癌、抗氧化、抗炎和抗过敏等多种有益特性[6-9]。RSV可将细胞阻滞在G1~S期，以剂量依赖的方式抑制平滑肌细胞(smooth muscle cell，SMC)增殖[10]，加速SMC凋亡[11]，最终减轻血管壁增厚引起的再狭窄。有研究报道，RSV在体外培养的人主动脉和肺动脉内皮细胞中可以时间和剂量依赖的方式抑制内皮细胞的增殖[12]，但关于其对受损血管内皮的修复作用研究较少。本研究采用颈总动脉球囊损伤大鼠模型，通过损伤段局部给药的方式观察体内环境下RSV对内皮及整个血管的修复作用。
1 材料与方法
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1.1 主要试剂及仪器
RSV(纯度≥99.8%)、F-127 Pluronic固体凝胶、DMSO溶液、4%多聚甲醛缓冲液购自上海碧云天生物技术有限公司；苏木精染液、BCA蛋白质浓度测定试剂盒(Ba1086)购自武汉百仟度生物科技有限公司；DAB显色试剂盒购自江苏世泰实验器材有限公司；小鼠抗CD31一抗(ab24590)购自英国Abcam公司；HRP标记的山羊抗小鼠二抗(5220-0341)购自美国SeraCare公司；兔抗人血管内皮生长因子(vascular endothelial growth factor，VEGF)单克隆抗体(19003-1-AP)购自美国Proteintech公司；HRP标记的山羊抗兔IgG(074-1506)购自美国KPL公司。2F球囊导管购自日本泰尔茂有限公司；全自动数字玻片扫描与分析系统(型号Aperio VERSA8)购自上海徕卡生物系统有限公司；病理切片机(型号RM2016)购自上海徕卡仪器有限公司。
1.2 实验动物及分组
40只健康雄性Sprague-Dawley大鼠购自北京斯贝福生物技术有限公司[实验动物生产许可证号：SYXK(京)2016-0001]，体重200~250 g，SPF级屏障环境下饲养于通风良好的武汉大学中南医院动物实验中心大鼠房内[相对湿度50%~60%、温度(22±2)℃]，自由饮食。适应性饲养2 d后，随机分为假手术组、模型组、溶剂对照组(DSMO组)与RSV组，每组10只。大鼠所有手术均在1%戊巴比妥钠(45 mg/kg)腹腔麻醉下进行，实验结束后，用1%戊巴比妥钠(100 mg/kg)过量麻醉实施安乐死。动物实验流程经武汉大学中南医院动物实验中心审核和批准(WP2020-08121)。
1.3 颈总动脉球囊损伤大鼠模型制备
根据文献[13]、[14]的方法制备颈总动脉球囊损伤大鼠模型。大鼠术前禁食禁水12 h后称重，腹腔注射1%戊巴比妥钠(45 mg/kg)麻醉，颈部备皮消毒，正中纵向做3 cm左右切口，钝性分离皮下组织，于左侧斜方肌上方钝性分离出颈总动脉，将其与伴行的迷走神经和交感神经分离，动脉夹夹闭近心端，继续向颈总动脉远心端分离，直至颈内动脉及颈外动脉的分叉处远心端约5 mm，结扎颈外动脉远心端。在颈外动脉线结近心端横向剪一小开口，将2F球囊导管从小口插入颈总动脉2.0~2.5 cm，向球囊内注气约0.25 ml，并向外抽动球囊导管3次。在距颈总动脉分叉处约2 mm位置结扎颈外动脉近心端，使颈总动脉及颈内动脉恢复充盈搏动，即造模成功。
1.4 颈总动脉外膜给药
参照文献[14]，使用Pluronic凝胶方法进行颈总动脉给药。将500 μg RSV溶于30 μl 10% DMSO中，然后与270 μl 25% F-127 Pluronic凝胶混合冰育。为避免RSV光异构化，将RSV、DMSO与F-127 Pluronic凝胶的混合物保存于铝箔包裹的密封Eppendorf管中。
RSV组：在颈总动脉进行球囊血管成形术后，将含RSV的凝胶均匀涂在颈总动脉损伤段的外周，使其固化。DSMO组：将30 μl 10% DMSO与270 μl 25% F-127 Pluronic凝胶混合冰育，均匀涂在颈总动脉损伤段的外周，使其固化。给药结束后，逐层缝合关闭术野。假手术组仅结扎颈外动脉，模型组仅行颈总动脉球囊损伤术，均不给药。术后单独饲养，常规饮食，自由饮水至第14天，用1%戊巴比妥钠(100 mg/kg)过量麻醉处死，取颈总动脉损伤段动脉组织，进行后续检测。
1.5 HE染色观察血管内膜增生程度和管腔狭窄程度
每组随机挑选3只大鼠处死，取颈总动脉损伤段动脉组织，固定24 h、脱水、石蜡包埋。蜡块以5 μm厚度做横切面，置于60℃恒温箱内烘干，常规脱蜡至水，苏木精染色1 min，冲洗返蓝，伊红染色1 min，清洗后脱水、透明、封片，使用全自动数字玻片扫描与分析系统进行拍照。在横截面切片上测量外膜以内区(EEL)面积及周长、内膜及内区(IEL)面积、管腔面积，内膜面积=(IEL面积—管腔面积)，中膜面积=(EEL面积—IEL面积)，使用ImageScope软件进行分析。每个样本取3个横截面，取平均值。内膜增生程度由内膜面积与中膜面积的比值判定，比值越大表明内膜增生程度越重；管腔狭窄程度由管腔面积与IEL面积的比值判定，比值越小表明管腔狭窄程度越重。
1.6 CD31免疫组织化学染色评估血管再内皮化程度
石蜡切片常规脱蜡至水，修复抗原，洗涤，滴加BSA孵育30 min；加入小鼠抗CD31一抗(1:200)，4℃孵育过夜，PBS溶液(pH 7.4)洗涤；滴加HRP标记的山羊抗小鼠二抗(1:100)，室温避光孵育50 min，PBS溶液(pH 7.4)洗涤；滴加DAB显色剂，显微镜下控制显色反应。显色完全后，苏木精复染，盐酸乙醇分化，氨水返蓝，脱水，封片，使用全自动数字玻片扫描与分析系统拍照，使用Barnes法进行评分，具体评分细则如下。A(细胞显色有无及深浅评分)：0分(不着色)、1分(浅黄色)、2分(棕黄色)、3分(棕褐色)；B(显色细胞比例评分)：1分(1%~10%)、2分(11%~50%)、3分(51%~80%)、4分(>80%)。Barnes评分(分)=A×B。评分越高表明CD31表达水平越高。
1.7 Western blotting检测颈总动脉组织中VEGF的表达水平
取大鼠颈总动脉损伤段组织，PBS漂洗后剪成小块置于匀浆器中，加入RIPA总蛋白裂解液，冰浴彻底匀浆，4℃下13 000 r/min离心5 min，取上清。使用BCA蛋白浓度测定试剂盒测定总蛋白浓度，上样40 μg，行10%十二烷基硫酸钠-聚丙烯酰胺凝胶电泳，将蛋白转移到PVDF膜上，5%脱脂奶粉室温封闭1 h；加入兔抗人VEGF单克隆抗体(1:1000)4℃孵育过夜，洗涤后加入HRP标记的山羊抗兔IgG(1:50 000)，室温孵育30 min；加入ECL混合溶液，曝光、显影、定影。使用全自动数码凝胶图像分析系统对胶片进行拍照，用ImageJ软件处理系统分析目标条带的光密度值。
1.8 统计学处理
采用SPSS 22.0软件进行统计分析。正态分布的计量资料以$\bar{x}±s$表示，组间比较采用单因素方差分析，进一步两两比较采用LSD-t检验。P<0.05为差异有统计学意义。
2 结果
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2.1 RSV对颈总动脉球囊损伤模型大鼠血管内膜增生和管腔再狭窄的影响
HE染色结果显示，假手术组、模型组、DMSO组和RSV组EEL周长依次为(2776±104) μm、(2808±96) μm、(2794±61) μm、(2737±108) μm，EEL面积依次为(401 723±110 235) μm2、(427 645±51 249) μm2、(428 551±24 924) μm2、(409 668±155 414) μm2，IEL面积依次为(297 989±104 605) μm2、(299 906±38 691) μm2、(305 250±31 223) μm2、(280 259±153 262) μm2，管腔面积依次为(290 240±104 463) μm2、(230 440±44 012) μm2、(288 568±35 384) μm2、(137 545±64 629) μm2，内膜增生程度依次为0.075±0.003、0.559±0.119、0.135±0.031、1.092±0.360，管腔狭窄程度依次为0.964±0.011、0.764±0.049、0.944±0.020、0.532±0.189。各组EEL周长、EEL面积及IEL面积比较差异无统计学意义(P>0.05)。与假手术组和DMSO组相比，RSV组管腔面积减小(P<0.05)。与假手术组相比，模型组和RSV组血管内膜增生程度加重(P<0.05)；与模型组相比，DMSO组血管内膜增生程度明显减轻(P<0.05)；与DMSO组相比，RSV组血管内膜增生程度加重(P<0.05)。与假手术组相比，模型组和RSV组管腔狭窄程度加重(P<0.05)；与模型组相比，DMSO组管腔狭窄程度减轻(P<0.05)；与DMSO组相比，RSV组管腔狭窄程度加重(P<0.05)(图1)。
2.2 RSV对颈总动脉球囊损伤模型大鼠血管再内皮化的影响
CD31免疫组化阳性产物位于内皮细胞表面，呈棕褐色，代表血管内皮化的程度。如图2A所示，假手术组内皮细胞连续性最好且均染为棕褐色；模型组内皮细胞连续性较差且70%的内皮细胞染色为棕黄色；DMSO组内皮细胞连续性较差，约80%的内皮细胞染色为棕黄色；RSV组内皮细胞连续性较好且90%的内皮细胞染色为棕褐色。Barnes评分结果显示，假手术组、模型组、DMSO组和RSV组动脉组织Barnes评分依次为(12.00±0.00)分、(7.33±1.16)分、(8.67±3.06)分、(11.00±1.70)分。与假手术组相比，模型组动脉组织Barnes评分降低(P<0.05)；与模型组相比，RSV组动脉组织Barnes评分明显增高(P<0.05，图2B)。
2.3 RSV对颈总动脉球囊损伤模型大鼠动脉组织中VEGF表达的影响
Western blotting检测结果显示，假手术组、模型组、DMSO组和RSV组动脉组织中VEGF的表达水平依次为0.72±0.13、0.31±0.12、0.38±0.18、0.67±0.18。与假手术组相比，模型组动脉组织中VEGF表达水平明显降低(P<0.05)；与模型组和DMSO组相比，RSV组动脉组织中VEGF表达水平明显增高(P<0.05)(图3)。
3 讨论
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经皮冠状动脉介入治疗引起血管损伤的过程较复杂，包括内皮剥脱、各种生长因子和细胞因子的释放、血小板活化，以及平滑肌细胞增殖和迁移到内皮下间隙形成新内膜增生等[15-16]，最终导致靶血管再狭窄。相较裸金属支架，药物洗脱支架显著降低了再狭窄发生率，但晚期(置入后>1年)血栓形成再狭窄的发生率却有所增高[17]。涂覆在支架上抑制血管平滑肌细胞增殖的药物也可抑制内皮细胞的增殖，延迟内皮的修复。药物洗脱支架可在局部递送高浓度的药物，累积的药物在血管支架内停留，延长了药物抗增殖作用的时间，从而影响内皮的恢复和功能[18]。研究发现，血管内皮细胞为减少血栓形成、脂质吸收及减轻炎症提供了有效的屏障[19]。内皮细胞功能丧失导致血小板的反应性增加，同时激活有丝分裂原，增加黏附分子和组织因子的表达，并减少血栓调节蛋白的产生，从而促进血栓形成，导致经皮冠状动脉介入治疗后的内皮功能障碍和炎症[20-22]。内皮再生是一种修复机制，用于维持正常血管功能的内皮单层完整性。在支架置入后，再生的内皮细胞可能在屏障完整性、细胞-细胞连接、血管通透性，以及抗氧化和抗血栓分子的表达等方面减弱[23-25]，而不成熟和无效的内皮细胞更容易发生血栓，从而导致管腔狭窄[26]。
本研究结果显示，处理14 d，RSV使损伤的血管内膜增生，管腔狭窄明显，再内皮化程度较其他处理组增强，未发生收缩性重构。相较假手术组，其余各组均有不同程度的内膜增生和管壁变厚，假手术组因未行球囊损伤术损伤内皮细胞，内皮最为完整，CD31免疫组织化学染色呈棕褐色且连续性最强。相较其他处理组，RSV处理过的血管损伤段CD31表达增加，表明RSV可增强受损血管的再内皮化程度。VEGF具有促进血管再生的能力，VEGF家族及其受体系统已被证实是血管新生细胞信号转导中的基本调节剂[27]，VEGF表达增加表明RSV能增强内膜的再生能力和血管的新生能力。由此可见，短期内血管内膜增生、管腔狭窄并非病理性血管重构引起的狭窄，而是由RSV对血管内膜再生和再内皮化的修复作用造成的。值得注意的是，相较传统的RSV给药方式如腹腔注射和灌胃等，本研究采用经颈总动脉外膜给药，可使药物精准高效地作用于颈总动脉损伤段，因此在两周内即可观察到明显的效应，表明RSV在短期内确实能够促进血管新生、内膜再生以及增强内皮化程度。再内皮化是修复受损血管的第一步，能加速受损区域内膜的恢复和预防血栓形成等并发症，是预防远期再狭窄的前提。
内膜损伤后，邻近内皮剥脱区域驻留内皮细胞的增殖、迁移和源自骨髓的内皮祖细胞(endothelial progenitor cell，EPC)的募集可使内皮剥脱区域再内皮化[16]。驻留的内皮细胞增殖并从邻近的完整节段迁移到受损节段，从而修复内皮屏障。循环内皮细胞(circulating endothelial cell，CEC)是一种成熟的细胞，在血管损伤后从血管壁脱落进入循环，到达内皮受损节段修复内皮[28-29]。正常情况下，CEC的数量非常低，但介入术后明显增多，表明血管内支架诱导了内皮化[30]。EPC是骨髓中造血细胞的一种，为多能干细胞，在血流中循环，可分化成内皮谱系细胞[31]，在受伤的内膜处可发挥内皮再生的作用[32]。当EPC被动员到血管损伤部位时可形成一个循环细胞池，这些细胞可以填补内皮不连续的部位，修复受损的内皮[33]，加速再内皮化进程。由此推测，RSV修复血管的始动机制可能为促进邻近驻留内皮细胞的迁移，或者增强对骨髓内皮细胞或循环内皮细胞的募集。
本研究存在以下不足：(1)未对动脉组织的炎症反应进行评估，HE染色、CD31免疫组织化学染色的样本量偏小。(2)侧重于RSV对血管形态学、再内皮化指标和血管再生指标的研究，忽略了血管炎症相关指标；后续研究需关注炎症指标，扩大样本量，减小误差。(3)仅进行了短期实验，未能阐述RSV对内膜损伤血管修复的具体机制及RSV对血管的长期作用，后续需进行长期的体内和体外实验以分析可能的机制，为预防介入术后再狭窄提供新思路。
综上所述，RSV可使大鼠颈总动脉球囊损伤术后血管CD31和VEGF的表达增强，短期内血管壁增厚，再内皮化程度增强，具有修复血管内皮的作用，其机制可能是促进邻近驻留内皮细胞的增殖、迁移以及骨髓内皮细胞或循环内皮细胞的募集。
基金
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  • 国家自然科学基金(81471858)
  • 武汉大学中南医院科技创新培育基金(ZNPY2018103)
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2021年第46卷第6期
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doi: 10.11855/j.issn.0577-7402.2021.06.02
  • 接收时间：2021-02-05
  • 首发时间：2025-12-20
  • 出版时间：2021-06-28
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  • 收稿日期：2021-02-05
  • 修回日期：2021-05-09
基金
National Natural Science Foundation of China(81471858)
国家自然科学基金(81471858)
Science and Technology Innovation Fund of Zhongnan Hospital of Wuhan University(ZNPY2018103)
武汉大学中南医院科技创新培育基金(ZNPY2018103)
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    武汉大学中南医院麻醉科，武汉 430071

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genus		 种数
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species		 占总种数比例
Percentage of
total species (%)		 属
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Number of
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鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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