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Article(id=1241522774867506002, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241522764012647140, articleNumber=null, orderNo=null, doi=10.20043/j.cnki.MPM.202306460, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1687363200000, receivedDateStr=2023-06-22, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1773931695906, onlineDateStr=2026-03-19, pubDate=1704816000000, pubDateStr=2024-01-10, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1773931695906, onlineIssueDateStr=2026-03-19, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1773931695906, creator=13701087609, updateTime=1773931695906, updator=13701087609, issue=Issue{id=1241522764012647140, tenantId=1146029695717560320, journalId=1227665162245664772, year='2024', volume='51', issue='1', pageStart='1', pageEnd='192', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1773931693318, creator=13701087609, updateTime=1773931808852, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1241523248643494379, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241522764012647140, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1241523248643494380, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1241522764012647140, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=8, endPage=14, ext={EN=ArticleExt(id=1241522775492457327, articleId=1241522774867506002, tenantId=1146029695717560320, journalId=1227665162245664772, language=EN, title=A two-sample Mendelian randomized study on rheumatoid arthritis and atherosclerosis, columnId=1240413921954295836, journalTitle=Modern Preventive Medicine, columnName=Epidemiology and Statistical Methods, runingTitle=null, highlight=null, articleAbstract=
Objective

To study the causal relationship between rheumatoid arthritis (RA) and atherosclerosis (AS) by two-sample Mendelian randomized analysis.

Methods

The whole genomes of RA and different subtypes of AS were obtained from IEU Open GWAS (https://gwas.mrcieu.ac.uk/) database. Two-sample Mendelian randomized analysis was carried out using the inverse-variance weighted (IVW) method, MR-Egger regression, simple mode, weighted mode, and weighted median (WM),and the results were verified by multiple sensitivity analyses.

Results

In total 86 single nucleotide polymorphisms (SNPs) strongly associated with RA were included as instrumental variables in this study. According to IVW, RA was associated with coronary atherosclerosis (OR=1.034, 95%CI: 1.010-1.058) and peripheral atherosclerosis (OR=1.083, 95%CI: 1.041-1.127, P=0.001). Heterogeneity test, horizontal multiple effect analysis, sensitivity analysis, and MR-PRESSO further clarified the causal relationship by Mendelian randomization analysis.

Conclusion

RA has positive causal correlations with coronary atherosclerosis and peripheral atherosclerosis, but there is no causal correlation between AS and RA by reverse MR analysis. RA increases the risk of coronary atherosclerosis and peripheral arteriosclerosis. It is suggested to actively control RA to reduce the risk of AS.

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目的

采用两样本孟德尔随机化分析方法研究类风湿关节炎（rheumatoid arthritis，RA）与动脉粥样硬化（atherosclerosis，AS）之间的因果关系。

方法

在IEU Open GWAS（https://gwas.mrcieu.ac.uk/）数据库中获取RA与AS不同亚型的全基因组进行关联研究（genome-wide association study，GWAS）。通过逆方差加权法（inverse-variance weighted，IVW）、MR-Egger回归、简单模式(simple mode)、加权模型(weighted mode)和加权中位数法（weighted median，WM）进行两样本孟德尔随机化分析，并对结果采用多种敏感性分析进行校验。

结果

本研究纳入86个与RA强相关的单核苷酸多态性（single nucleotic polymorphism，SNP）作为工具变量。冠状动脉粥样硬化IVW法显示(OR:1.034，95%CI: 1.010～1.058,P=0.005)；外周动脉粥样硬化IVW法结果（OR:1.083,95%CI:1.041～1.127，P=0.001）；对其结果进行异质性检验、水平多效性分析、敏感性分析和MR-PRESSO进一步明确孟德尔随机化分析的因果关系。

结论

RA与冠状动脉粥样硬化、外周动脉硬化之间存在因果关联，且呈正相关；反向MR分析未发现AS与RA存在因果关联；RA的存在使得冠状动脉粥样硬化、外周动脉硬化的发病风险升高，建议积极控制RA以降低AS的发生风险。

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于睿，E-mail:；
张欢，E-mail:
, copyrightStatement=本刊刊出的所有文章不代表中华预防医学会和本刊编委会的观点，除非特别声明。, copyrightOwner=中华预防医学会和四川大学华西公共卫生学院, extLink=null, articleAbsUrl=null, sourceXml=9ApPkqu16jsZ0RsIzEbfPQ==, magXml=8dn2ze/Zm1ut+ADTMMv+gQ==, pdfUrl=null, pdf=NCRugyE2cFr9sOBFheZvYg==, pdfFileSize=2686060, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=8rPTtqTDxbTfE7c8Z0zhPg==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=2nL6Z8Eu/UHOLWt/6oSsCw==, mapNumber=null, authorCompany=null, fund=null, authors=

段盈竹（1990—），女，博士在读，研究方向：中西医结合防治心血管疾病

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段盈竹（1990—），女，博士在读，研究方向：中西医结合防治心血管疾病

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段盈竹（1990—），女，博士在读，研究方向：中西医结合防治心血管疾病

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Scientific Reports, 2022, 12(1): 8807., articleTitle=Pinolenic acid exhibits anti- inflammatory and anti-atherogenic effects in peripheral blood-derived monocytes from patients with rheumatoid arthritis, refAbstract=null), Reference(id=1241677636217394079, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, doi=null, pmid=null, pmcid=null, year=2022, volume=59, issue=1, pageStart=54, pageEnd=null, url=null, language=null, rfNumber=[26], rfOrder=25, authorNames=Mahmoud NF, Allam NM, Omara II, journalName=Medicina (Kaunas, Lithuania), refType=null, unstructuredReference=Mahmoud NF, Allam NM, Omara II, et al. Efficacy of siwan traditional therapy on erythrocyte sedimentation rate, lipid profile, and atherogenic index as cardiac risk factors related to rheumatoid arthritis[J]. Medicina (Kaunas, Lithuania), 2022, 59(1): 54., articleTitle=Efficacy of siwan traditional therapy on erythrocyte sedimentation rate, lipid profile, and atherogenic index as cardiac risk factors related to rheumatoid arthritis, refAbstract=null), Reference(id=1241677636322251681, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, doi=null, pmid=null, pmcid=null, year=2021, volume=1, issue=12, pageStart=null, pageEnd=null, url=null, language=null, rfNumber=[27], rfOrder=26, authorNames=Rasooly D, Peloso GM, journalName=Curr Protoc, refType=null, unstructuredReference=Rasooly D, Peloso GM. Two-Sample multivariable mendelian randomization analysis using R[J]. Curr Protoc, 2021, 1(12): e335., articleTitle=Two-Sample multivariable mendelian randomization analysis using R, refAbstract=null)], funds=[Fund(id=1241677631884677987, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, awardId=82274494, language=CN, fundingSource=国家自然科学基金(82274494), fundOrder=null, country=null), Fund(id=1241677631972758373, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, awardId=2020JH1/10100022, language=CN, fundingSource=辽宁省科学技术计划项目工业重大专项(2020JH1/10100022), fundOrder=null, country=null), Fund(id=1241677632039867240, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, awardId=2023JH2/101600030, language=CN, fundingSource=辽宁省科学技术计划项目(2023JH2/101600030), fundOrder=null, country=null), Fund(id=1241677632132141931, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, awardId=LJKFR20220255, language=CN, fundingSource=辽宁省教育厅基本科研项目(LJKFR20220255), fundOrder=null, country=null)], companyList=[AuthorCompany(id=1241677621570884129, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, xref=null, ext=[AuthorCompanyExt(id=1241677621579272740, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, companyId=1241677621570884129, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=Liaoning University of Traditional Chinese Medicine, Shenyang, Liaoning 110847, China), AuthorCompanyExt(id=1241677621587661348, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, companyId=1241677621570884129, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=辽宁中医药大学，辽宁 沈阳 110847)])], figs=[ArticleFig(id=1241677628336296744, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, language=EN, label=Figure 1, caption=Forest plot, figureFileSmall=PnnfQ8ZH3D4cu5qhrjSszA==, figureFileBig=8BALE2Tb+l6auJ14KAxoOQ==, tableContent=null), ArticleFig(id=1241677629842051886, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, language=CN, label=图1, caption=森林图

注：图A、B分别为RA与冠状动脉粥样硬化、RA与外周动脉粥样硬化森林图。

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注：图C、D分别为RA与冠状动脉粥样硬化、RA与外周动脉粥样硬化散点图。

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注：图E、F分别为RA与冠状动脉粥样硬化、RA与外周动脉粥样硬化漏斗图。

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注：图G、H分别为RA与冠状动脉粥样硬化、RA与外周动脉粥样硬化leave-one-out法结果图。

, figureFileSmall=DKaKUITT/YRy/jVothtg3w==, figureFileBig=sWfvu2ljjGHTtl7tZz3cGQ==, tableContent=null), ArticleFig(id=1241677630727050061, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, language=EN, label=Table 1, caption=

The basic information of study sample

, figureFileSmall=null, figureFileBig=null, tableContent=
疾病GWAS ID年份（年）人口样本量病例数对照数SNPs数量
类风湿性关节炎ebi-a-GCST900135342020欧洲人58 28414 36143 92313 108 512
冠状动脉粥样硬化finn-b-I9_CORATHER2021欧洲人211 20316 761194 44216 380 402
外周动脉粥样硬化finn-b-DM_PERIPHATHERO2021欧洲人168 8326 631162 20116 380 247
), ArticleFig(id=1241677630873850704, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, language=CN, label=表1, caption=

研究样本基本信息

, figureFileSmall=null, figureFileBig=null, tableContent=
疾病GWAS ID年份（年）人口样本量病例数对照数SNPs数量
类风湿性关节炎ebi-a-GCST900135342020欧洲人58 28414 36143 92313 108 512
冠状动脉粥样硬化finn-b-I9_CORATHER2021欧洲人211 20316 761194 44216 380 402
外周动脉粥样硬化finn-b-DM_PERIPHATHERO2021欧洲人168 8326 631162 20116 380 247
), ArticleFig(id=1241677630987096917, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, language=EN, label=Table 2, caption=

Instrumental variables

, figureFileSmall=null, figureFileBig=null, tableContent=
效应等位基因非效应等位基因P值效应值(β)
TG9.73×10-11-0.078
TC2.36×10-8-0.085
CT2.01×10-18-0.099
TC3.82×10-240.191
AG1.82×10-280.488
CA1.29×10-1030.788
AG9.92×10-150.115
TC2.45×10-190.381
CT1.88×10-12-0.136
TC4.32×10-300.147
AG1.01×10-10-0.075
GA1.90×10-90.080
TC1.59×10-110.103
TC1.35×10-110.138
TC3.04×10-80.087
TC4.29×10-140.099
GA6.77×10-120.082
GA8.68×10-600.383
AG3.29×10-22-0.438
TC4.42×10-90.067
TC4.13×10-40-0.154
TA2.29×10-110.084
AG4.54×10-19-0.117
AT1.14×10-14-0.101
CT1.13×10-160.105
CA1.48×10-13-0.098
TC1.02×10-130.107
AG1.69×10-200.130
CT1.47×10-80.103
GA6.20×10-11-0.089
AG6.66×10-130.106
TC6.49×10-260.196
AG6.04×10-14-0.092
AG2.51×10-9-0.073
AG3.75×10-26-0.128
GT6.04×10-10-0.089
TC1.66×10-110.091
CA1.71×10-190.162
AT7.86×10-9-0.123
GA2.65×10-140.090
CT4.62×10-80.067
GC2.91×10-30-0.253
AG3.32×10-24-0.126
AG1.98×10-150.099
AG7.17×10-170.142
AG1.07×10-9-0.085
CG1.08×10-15-0.380
CT1.87×10-190.124
TC9.64×10-110.074
GA3.94×10-110.086
GA3.96×10-10-0.091
GA1.28×10-80.087
CT7.85×10-90.098
GA1.76×10-100.075
TC2.21×10-120.088
CA9.52×10-130.249
TC5.86×10-100.074
AG3.75×10-80.086
TG1.00×10-2000.652
CT6.17×10-100.083
AG1.36×10-100.089
GT4.79×10-9-0.079
TC3.19×10-10-0.107
TC6.33×10-9-0.202
TC3.57×10-90.104
CT5.57×10-140.134
CG3.01×10-110.120
AG1.11×10-9-0.107
AC1.41×10-1450.591
AG1.42×10-12-0.085
TC3.13×10-250.149
AG1.11×10-670.699
TC6.11×10-180.137
TG4.14×10-90.070
AG5.37×10-9-0.078
TC6.83×10-150.160
AG1.94×10-26-0.196
AG3.47×10-290.284
CT4.47×10-240.124
CT1.81×10-9-0.082
GT1.00×10-2000.489
AG9.26×10-11-0.089
CT1.94×10-190.114
AG1.50×10-180.113
GC2.30×10-110.091
TC2.70×10-100.083
), ArticleFig(id=1241677631188423512, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, language=CN, label=表2, caption=

工具变量信息

, figureFileSmall=null, figureFileBig=null, tableContent=
效应等位基因非效应等位基因P值效应值(β)
TG9.73×10-11-0.078
TC2.36×10-8-0.085
CT2.01×10-18-0.099
TC3.82×10-240.191
AG1.82×10-280.488
CA1.29×10-1030.788
AG9.92×10-150.115
TC2.45×10-190.381
CT1.88×10-12-0.136
TC4.32×10-300.147
AG1.01×10-10-0.075
GA1.90×10-90.080
TC1.59×10-110.103
TC1.35×10-110.138
TC3.04×10-80.087
TC4.29×10-140.099
GA6.77×10-120.082
GA8.68×10-600.383
AG3.29×10-22-0.438
TC4.42×10-90.067
TC4.13×10-40-0.154
TA2.29×10-110.084
AG4.54×10-19-0.117
AT1.14×10-14-0.101
CT1.13×10-160.105
CA1.48×10-13-0.098
TC1.02×10-130.107
AG1.69×10-200.130
CT1.47×10-80.103
GA6.20×10-11-0.089
AG6.66×10-130.106
TC6.49×10-260.196
AG6.04×10-14-0.092
AG2.51×10-9-0.073
AG3.75×10-26-0.128
GT6.04×10-10-0.089
TC1.66×10-110.091
CA1.71×10-190.162
AT7.86×10-9-0.123
GA2.65×10-140.090
CT4.62×10-80.067
GC2.91×10-30-0.253
AG3.32×10-24-0.126
AG1.98×10-150.099
AG7.17×10-170.142
AG1.07×10-9-0.085
CG1.08×10-15-0.380
CT1.87×10-190.124
TC9.64×10-110.074
GA3.94×10-110.086
GA3.96×10-10-0.091
GA1.28×10-80.087
CT7.85×10-90.098
GA1.76×10-100.075
TC2.21×10-120.088
CA9.52×10-130.249
TC5.86×10-100.074
AG3.75×10-80.086
TG1.00×10-2000.652
CT6.17×10-100.083
AG1.36×10-100.089
GT4.79×10-9-0.079
TC3.19×10-10-0.107
TC6.33×10-9-0.202
TC3.57×10-90.104
CT5.57×10-140.134
CG3.01×10-110.120
AG1.11×10-9-0.107
AC1.41×10-1450.591
AG1.42×10-12-0.085
TC3.13×10-250.149
AG1.11×10-670.699
TC6.11×10-180.137
TG4.14×10-90.070
AG5.37×10-9-0.078
TC6.83×10-150.160
AG1.94×10-26-0.196
AG3.47×10-290.284
CT4.47×10-240.124
CT1.81×10-9-0.082
GT1.00×10-2000.489
AG9.26×10-11-0.089
CT1.94×10-190.114
AG1.50×10-180.113
GC2.30×10-110.091
TC2.70×10-100.083
), ArticleFig(id=1241677631301669722, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, language=EN, label=Table 3, caption=

MR analysis results of RA and coronary arteriosclerosis

, figureFileSmall=null, figureFileBig=null, tableContent=
MR方法OR值（95%CI）b P值
MR Egger1.048（1.012～1.086）0.0470.0180.010
weighted median1.040（1.008～1.073）0.0390.0160.013
inverse variance weighted1.034（1.010～1.058）0.0330.0120.005
simple mode1.015（0.945～1.090）0.0150.0360.682
weighted mode1.046（1.018～1.075）0.0450.0140.002
), ArticleFig(id=1241677631398138715, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, language=CN, label=表3, caption=

RA和冠状动脉粥样硬化MR结果

, figureFileSmall=null, figureFileBig=null, tableContent=
MR方法OR值（95%CI）b P值
MR Egger1.048（1.012～1.086）0.0470.0180.010
weighted median1.040（1.008～1.073）0.0390.0160.013
inverse variance weighted1.034（1.010～1.058）0.0330.0120.005
simple mode1.015（0.945～1.090）0.0150.0360.682
weighted mode1.046（1.018～1.075）0.0450.0140.002
), ArticleFig(id=1241677631528162143, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, language=EN, label=Table 4, caption=

MR analysis results of RA and peripheral atherosclerosis

, figureFileSmall=null, figureFileBig=null, tableContent=
methodOR值（95%CI）b P值
MR Egger1.110（1.045～1.180）0.1050.0311.16×10-3
weighted median1.110（1.050～1.174）0.1040.0292.56×10-4
inverse variance weighted1.083（1.041～1.127）0.0800.0208.38×10-5
simple mode1.034（0.916～1.168）0.0340.0625.89×10-1
weighted mode1.111（1.059～0.105）0.1050.0255.45×10-5
), ArticleFig(id=1241677631670768484, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1241522774867506002, language=CN, label=表4, caption=

RA和外周动脉粥样硬化MR结果

, figureFileSmall=null, figureFileBig=null, tableContent=
methodOR值（95%CI）b P值
MR Egger1.110（1.045～1.180）0.1050.0311.16×10-3
weighted median1.110（1.050～1.174）0.1040.0292.56×10-4
inverse variance weighted1.083（1.041～1.127）0.0800.0208.38×10-5
simple mode1.034（0.916～1.168）0.0340.0625.89×10-1
weighted mode1.111（1.059～0.105）0.1050.0255.45×10-5
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类风湿关节炎与动脉粥样硬化的两样本孟德尔随机化研究
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段盈竹 , 马海钧 , 倪萍 , 梁健 , 张颖 , 张欢 , 于游 , 于睿
现代预防医学 | 流行病与统计方法 2024,51(1): 8-14
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现代预防医学 | 流行病与统计方法 2024, 51(1): 8-14
类风湿关节炎与动脉粥样硬化的两样本孟德尔随机化研究
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段盈竹, 马海钧, 倪萍, 梁健, 张颖, 张欢 , 于游, 于睿
作者信息
  • 辽宁中医药大学，辽宁 沈阳 110847

    • 段盈竹（1990—），女，博士在读，研究方向：中西医结合防治心血管疾病

通讯作者:

于睿，E-mail:；
张欢，E-mail:
A two-sample Mendelian randomized study on rheumatoid arthritis and atherosclerosis
Ying-zhu DUAN, Hai-jun MA, Ping NI, Jian LIANG, Ying ZHANG, Huan ZHANG , You YU, Rui YU
Affiliations
  • Liaoning University of Traditional Chinese Medicine, Shenyang, Liaoning 110847, China
出版时间: 2024-01-10 doi: 10.20043/j.cnki.MPM.202306460
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摘要
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目的

采用两样本孟德尔随机化分析方法研究类风湿关节炎（rheumatoid arthritis，RA）与动脉粥样硬化（atherosclerosis，AS）之间的因果关系。

方法

在IEU Open GWAS（https://gwas.mrcieu.ac.uk/）数据库中获取RA与AS不同亚型的全基因组进行关联研究（genome-wide association study，GWAS）。通过逆方差加权法（inverse-variance weighted，IVW）、MR-Egger回归、简单模式(simple mode)、加权模型(weighted mode)和加权中位数法（weighted median，WM）进行两样本孟德尔随机化分析，并对结果采用多种敏感性分析进行校验。

结果

本研究纳入86个与RA强相关的单核苷酸多态性（single nucleotic polymorphism，SNP）作为工具变量。冠状动脉粥样硬化IVW法显示(OR:1.034，95%CI: 1.010～1.058,P=0.005)；外周动脉粥样硬化IVW法结果（OR:1.083,95%CI:1.041～1.127，P=0.001）；对其结果进行异质性检验、水平多效性分析、敏感性分析和MR-PRESSO进一步明确孟德尔随机化分析的因果关系。

结论

RA与冠状动脉粥样硬化、外周动脉硬化之间存在因果关联，且呈正相关；反向MR分析未发现AS与RA存在因果关联；RA的存在使得冠状动脉粥样硬化、外周动脉硬化的发病风险升高，建议积极控制RA以降低AS的发生风险。

孟德尔随机化  /  类风湿关节炎  /  动脉粥样硬化  /  冠状动脉粥样硬化  /  外周动脉硬化
Objective

To study the causal relationship between rheumatoid arthritis (RA) and atherosclerosis (AS) by two-sample Mendelian randomized analysis.

Methods

The whole genomes of RA and different subtypes of AS were obtained from IEU Open GWAS (https://gwas.mrcieu.ac.uk/) database. Two-sample Mendelian randomized analysis was carried out using the inverse-variance weighted (IVW) method, MR-Egger regression, simple mode, weighted mode, and weighted median (WM),and the results were verified by multiple sensitivity analyses.

Results

In total 86 single nucleotide polymorphisms (SNPs) strongly associated with RA were included as instrumental variables in this study. According to IVW, RA was associated with coronary atherosclerosis (OR=1.034, 95%CI: 1.010-1.058) and peripheral atherosclerosis (OR=1.083, 95%CI: 1.041-1.127, P=0.001). Heterogeneity test, horizontal multiple effect analysis, sensitivity analysis, and MR-PRESSO further clarified the causal relationship by Mendelian randomization analysis.

Conclusion

RA has positive causal correlations with coronary atherosclerosis and peripheral atherosclerosis, but there is no causal correlation between AS and RA by reverse MR analysis. RA increases the risk of coronary atherosclerosis and peripheral arteriosclerosis. It is suggested to actively control RA to reduce the risk of AS.

Mendelian randomization  /  Rheumatoid arthritis  /  Atherosclerosis  /  Coronary atherosclerosis  /  Peripheral arteriosclerosis
段盈竹, 马海钧, 倪萍, 梁健, 张颖, 张欢, 于游, 于睿. 类风湿关节炎与动脉粥样硬化的两样本孟德尔随机化研究. 现代预防医学, 2024 , 51 (1) : 8 -14 . DOI: 10.20043/j.cnki.MPM.202306460
Ying-zhu DUAN, Hai-jun MA, Ping NI, Jian LIANG, Ying ZHANG, Huan ZHANG, You YU, Rui YU. A two-sample Mendelian randomized study on rheumatoid arthritis and atherosclerosis[J]. Modern Preventive Medicine, 2024 , 51 (1) : 8 -14 . DOI: 10.20043/j.cnki.MPM.202306460
正文
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类风湿关节炎（rheumatoid arthritis，RA）是一种病因不明的多因素自身免疫性疾病、是最常见的慢性炎症性疾病之一[1]。主要累及关节亦可损害关节外器官，包括心脏、肾脏、肺、消化系统、眼睛、皮肤和神经系统以及全身合并症[2]。RA不仅是一种医学特征，而且是一个公共卫生问题，其并发症和合并症会使患者的预期寿命缩短几年[3]。
动脉粥样硬化（atherosclerosis，AS）是一种慢性动脉疾病，是动脉壁上沉积了一层像小米粥样的脂类,使动脉弹性减低、管腔变窄的慢性低级别炎症性病变[4]。它可以刺激先天和适应性免疫反应，是发达国家和发展中国家血管性死亡的主要原因[5]，根据世界卫生组织的报告，估计每年有1 790万人死于心血管疾病，占所有死亡人数的32%[6]。
近年来，国内外诸多学者在临床研究中发现RA患者易合并AS，前期针对两种疾病进行大量的文献检索与分析，结果呈现两种疾病间多数基于传统的观察性研究，并且存在观察的样本量较少、选择性偏倚等诸多问题，导致暴露与结局的研究结果受多因素影响，没有一定的可靠性[7-8]本研究主要探讨RA能否增加患AS的风险，同时是否具有反向因果关联。
孟德尔随机化（Mendelian randomization，MR）是利用与暴露密切相关的遗传变异来产生更为可靠证据的研究方法[9]。MR使用单核苷酸多态性（single nucleotic polymorphism，SNP）作为工具变量（IV），以此来验证暴露因素与结局之间的因果关系，且能够最小化混杂因素和反向因果关系的偏差，是一种新型的天然随机对照试验[10]。MR对结果运用多种敏感性分析进行校验，使结果更具可靠性[11]。这种生物信息学方法比传统的观察性研究更具优势，也更加具有成本效益。本研究利用MR明确RA和AS是否存在关联且有因果关系，为RA合并AS发病机制研究提供新的可靠性生物信息学依据,为临床疾病的预防、诊疗提供新思路。
1　材料和方法
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1.1　研究设计
本研究采用两样本孟德尔随机化法（two sample Mendelian randomization，TSMR）探究RA与AS之间的因果关系，以RA为暴露因素，AS为结局。MR必须遵循三大核心假设：（1）IV与暴露因素RA显著相关；（2）IV与任何潜在的混杂因素无关；（3）IV仅通过暴露因素RA一种途径影响结局AS。结局选取了AS的不同亚型，主要包括冠状动脉粥样硬化、脑动脉粥样硬化和外周动脉粥样硬化。本研究还进行了一项反向MR，即以AS为暴露，RA为结局，以探究AS与RA之间是否存在因果关联。
IV的筛选的参数设置为：选择与RA相关的显著性P<5×10-8的SNP，设置连锁不平衡参数（r2= 0.001），物理遗传距离（kb=10 000）。F检验挑选F>10的工具变量，以排除弱工具变量偏倚[12]。F值计算公式如下：
其中N表示全基因组关联分析（genome-wide association studies，GWAS）中的样本量，k表示工具变量的个数，R2表示工具变量解释暴露因素的程度。
其中MAF表示等位基因的频率（minor allele frequency）, β表示SNP对暴露因素的效应值。
1.2　数据来源
本研究使用获取的数据均为公开的全基因组关联研究（genome - wide association study，GWAS）数据库网站IEU Open GWAS（https://gwas.mrcieu.ac.uk/）中的统计结果。对于RA的遗传数据我们使用了European Study最近发表的GWAS中与RA相关的已发表遗传变异。该GWAS包括58 284人，病例组14 361人，对照组43 923人，SNP：13 108 512。AS不同亚型的遗传数据基于Finn Gen数据库相关的研究中获取，其中冠状动脉粥样硬化样本量211 203人，其中病例组16 761人，对照组194 442人；外周动脉粥样硬化的样本量168 832人，病例组6 631人，对照组162 201人。所用数据集的GWAS ID及其他信息见表1。
1.3　研究方法
1.3.1　MR分析
本研究TSMR中运用逆方差加权法（inverse-variance weighted，IVW）、MR-Egger回归、简单模式(simple mode)、加权模型(weighted mode)和加权中位数法（weight median）等五种方法以推断因果关系[13]。在判定暴露与结局的因果关联中，五种方法主要以IVW法分析的结果为主，剩余四种方法作为辅助补充。IVW法当P<0.05时，差异具有统计学意义，认为本研究暴露与结局之间存在因果关系；当OR>1时，认定暴露与结局之间呈正相关[14]。
1.3.2　异质性检验、敏感性分析、水平多效性分析
异质性检验主要是检验IV之间是否存在较大差异，同时运用Cochran Q检验来判断IVW模型和MR-Egger回归模型的异质性[15]。当P<0.05时，存在异质性，对MR结果存在一定的影响。敏感性分析使用留一法（leave-one-out）是逐个剔除SNP后发现是否有非特异性的SNP影响主效应识别离群值。水平多效性分析为了检验遗传变异是否通过核心假设以外的途径影响结局，主要方法使用Egger-intercept法，当P<0.05时，代表存在水平多效性[16]。
1.3.3　MR-PRESSO分析
全局的多效性残差和异质性分析使用MR-PRESSO分析，评估离群值对于暴露与结局之间关联的影响同时校正剔除离群值[17]。
1.3.4　反向MR分析
为了使研究信息更全面、研究结果更可靠，本研究进一步对AS与RA是否有关联且存在因果关系，进行了反向MR分析。同样运用上述五种分析方法和多种敏感性分析，暴露因素选取AS两种亚型，RA作为结局进行分析。IV的选择和MR分析运用的R4.2.2版本以及TSMR和MRPRESSO软件包[18]。
2　结果
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2.1　工具变量的选择及F值检验
本次从数据集ebi-a-GCST90013534筛选到与暴露RA强相关的工具变量共有86个，总F统计量均大于10，不存在弱工具变量。SNPs信息见表2。
2.2　孟德尔随机化分析结果
本文使用了五种MR探究RA与AS不同亚型的因果关系，见表3、4。其中RA与冠状动脉粥样硬化、外周动脉硬化存在因果关系，外周动脉粥样硬化IVW法结果（OR:1.083,95%CI: 1.0401～1.127，P=0.001）。冠状动脉粥样硬化IVW法结果(OR:1.034, 95%CI:1.010～1.058，P=0.005); RA和冠状动脉硬化分析结果：IVW法、weighted mode法及MR-Egger法具有统计学意义，simple mode法和weighted median法结果不具有统计学意义；RA和外周动脉硬化分析结果均有统计学意义。本研究最主要根据IVW法的结果来判定，其他四种分析方法总体效应与IVW法效应方向一致[19]。因此我们可以说明RA与冠状动脉粥样硬化、外周动脉硬化呈正相关为风险因素。阳性结果的IVW法和MR-Egger法森林图如图1所示、散点图见图2、漏斗图见图3。
2.3　异质性检验、敏感性分析、水平多效性分析结果
根据MR分析结果，对RA和冠状动脉粥样硬化的因果关联进行检验。基于异质性结果，IVW法的Cochran Q检验值（冠状）=121.353（P=0.480），MR-Egger法的Cochran Q检验值（冠状）=119.723（P=0.480），RA和外周动脉粥样硬化的因果关联进行检验。基于异质性结果，IVW法的Cochran Q检验值（外周）=83.883（P=0.483），MR-Egger法的Cochran Q检验值（外周）=80.326（P=0.563），P均>0.05表明结果未受到异质性的影响。敏感性分析采用“leave-one-out”法,发现逐个剔除SNP后，所得结果均P<0.05，表明不存在会对因果关系估计结果产生影响的非特异性SNP，可视化结果见图4“leave-one-out”法结果森林图。水平多效性分析结果显示使用Egger-intercept法P（冠状）=0.291>0.05；Egger-intercept法P（外周）=0.063>0.05，Egger截距与0无统计学差异，表明水平多效性不会对因果关系结果造成偏倚。以上三种敏感性分析均使得RA是冠状动脉粥样硬化的风险因素这一结果更加稳健可靠。
2.4　MR-PRESSO分析结果
最后对RA和冠状动脉粥样硬化、外周动脉硬化因果关系进行MR-PRESSO分析，结果分别为P（冠状）=0.983>0.05,P（外周）=0.435>0.05全局分析结果一致，不存在离群值变量。充分肯定了暴露因素RA与结局冠状动脉粥样硬化之间的关联是严谨可靠的。
2.5　反向MR分析结果
利用上述方法，筛选得到与暴露冠状动脉粥样硬化强相关SNPs共31个，6个跟外周动脉粥样硬化相关的SNP，未筛选到与脑动脉粥样硬化相关的SNP。根据反向MR随机化结果显示两种不同亚型的AS不与RA构成因果关系。
3　讨论
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本研究的目的是判断RA对于AS的发病是否存在因果关系，因此笔者运用GWAS数据库开展了针对RA与AS的TSMR，结果表明RA会增加AS的发病其风险增高。因而在基因遗传学角度阐明AS发病的危险因素提供了证据，为后续开展分子生物学研究提供依据，对RA患者并发AS的预防及治疗具有重大意义[20]。
MR分析是一种研究两种疾病相关联的流行病学研究方法，基本原理是运用遗传变异估计因受其影响表型的健康情况，通过遗传变异来推断暴露因素与结局指标之间的因果效应[21]。本研究前期经过严格筛选共纳入符合条件的86个与RA相关的SNPs且均满足三大核心假设、F>10,也不存在弱工具变量偏倚。本研究结果主要以IVW法为主，此方法特点是利用结局方差的倒数作为权重来进行拟合，同时不考虑截距项是否为0，产生的偏倚相对最小[22]。RA与冠状动脉粥样硬化、外周动脉粥样硬化存在因果关系，能增加冠状动脉粥样硬化、外周动脉粥样硬化风险；本研究除了IVW法以外同时运用了多种敏感性分析进行校正，结果均无统计学意义。反向MR也未发现AS与RA存在因果关系。
研究表明心血管疾病尤其是AS占RA患者死亡率的比例最大。在一项样本量超15万例患者的大型荟萃分析中，发现与一般人群相比，RA诱发心血管事件风险增加48%、相关死亡率高50%。一项对RA患者外周血单个核细胞的横断面分析发现，细胞亚群与冠状动脉钙化密切相关[23]。胶原诱导关节炎(CIA)动物模型具有促动脉粥样硬化的脂质特征，HDL较低，LDL较高，RA的炎症改变了脂质组成，增强了清道夫受体的表达，放大了胆固醇的内流和泡沫细胞的形成，促进了AS的发生[24]。
RA与AS这两种疾病之间潜在的共享途径、共同发病机制包括炎症、免疫、氧化应激及内皮功能障碍等[25]。越来越多的研究证据表明，在两种疾病中起着核心作用的是免疫系统，RA中涉及的促炎细胞因子通过先天和适应性免疫反应促进了AS的发生，其中促炎细胞因子IL-18和IL-33起关键作用[26]。
本研究运用TSMR与传统观察性研究相比，能够避免反向因果关系、减少临床伦理道德问题、排除混杂因素节约时间，同时进行了多变量的MR研究，使研究结果更加可靠[27]。但本研究还存在一定的局限性，首先，获得的可供分析的SNPs数量并不多，研究人群较单一仅为欧洲人群，虽然一定程度上能够减少人口分层引起的偏倚，但无法证明本研究结果在其他人群中的适用性。其次，本研究中暴露和结局为二分类变量，一些研究指出以二分类变量作为暴露和结局指标的MR研究不足以解释存在的因果关系。最后，与其他MR研究一样，本研究尚不能解决未观察到的多效性，对研究结果可能产生一定影响。
本研究的优点和创新性：首次使用MR探讨RA与AS两种亚型之间的因果关系并证明了RA是冠状动脉粥样硬化、外周动脉粥样硬化风险因素。采用研究的思路及得到的因果关系是临床预防、诊疗研究两者关联的一个重要补充。RA患者要注意预防冠状动脉粥样硬化、外周动脉粥样硬化的发生，降低心血管事件的发生及死亡率，起到未病先防的作用。
综上所述本研究利用MR探究RA与AS的因果关系，结果表明RA与冠状动脉粥样硬化、外周动脉粥样硬化存在因果关系且呈正相关；反向MR分析表明AS和RA之间不存在因果效应。本结论还需要接受大量生物信息学及分子机制的研究进一步验证。对于患有RA的患者，临床医师还应对患者进行冠状动脉粥样硬化、外周动脉粥样硬化的筛查，全面积极治疗，防止患者病情加重，提高患者生存质量。
基金
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  • 国家自然科学基金(82274494)
  • 辽宁省科学技术计划项目工业重大专项(2020JH1/10100022)
  • 辽宁省科学技术计划项目(2023JH2/101600030)
  • 辽宁省教育厅基本科研项目(LJKFR20220255)
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2024年第51卷第1期
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文章信息
doi: 10.20043/j.cnki.MPM.202306460
  • 接收时间：2023-06-22
  • 首发时间：2026-03-19
  • 出版时间：2024-01-10
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  • 收稿日期：2023-06-22
基金
国家自然科学基金(82274494)
辽宁省科学技术计划项目工业重大专项(2020JH1/10100022)
辽宁省科学技术计划项目(2023JH2/101600030)
辽宁省教育厅基本科研项目(LJKFR20220255)
作者信息
    辽宁中医药大学，辽宁 沈阳 110847

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species		 占总种数比例
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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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