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Article(id=1322190384151769760, tenantId=1146029695717560320, journalId=1319373162502258839, issueId=1322190316019499694, articleNumber=null, orderNo=null, doi=10.16016/j.2097-0927.202505029, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1747065600000, receivedDateStr=2025-05-13, revisedDate=1753113600000, revisedDateStr=2025-07-22, acceptedDate=null, acceptedDateStr=null, onlineDate=1793164352690, onlineDateStr=2026-10-28, pubDate=1756483200000, pubDateStr=2025-08-30, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1793164352690, onlineIssueDateStr=2026-10-28, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1793164352690, creator=13701087609, updateTime=1793164352690, updator=13701087609, issue=Issue{id=1322190316019499694, tenantId=1146029695717560320, journalId=1319373162502258839, year='2025', volume='47', issue='16', pageStart='1825', pageEnd='1980', issueExtLink='null', onlineDate='null', pubDate='1756483200000', pubDateStr='2025-08-30', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=0, createTime=1793164336447, creator='13701087609', updateTime=1793164553187, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1322191225206198613, tenantId=1146029695717560320, journalId=1319373162502258839, issueId=1322190316019499694, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1322191225206198614, tenantId=1146029695717560320, journalId=1319373162502258839, issueId=1322190316019499694, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=1962, endPage=1969, ext={EN=ArticleExt(id=1322190384361484961, articleId=1322190384151769760, tenantId=1146029695717560320, journalId=1319373162502258839, language=EN, title=Causal effects between different sub-phenotypes of endometriosis and female infertility: a bidirectional Mendelian randomization study, columnId=1320435174995772212, journalTitle=Journal of Army Medical University, columnName=Clinical Medicine, runingTitle=null, highlight=null, articleAbstract=
Objective‍

To investigate the bidirectional causal relationship between different subtypes of endometriosis and female infertility using Mendelian randomization (MR).

Methods‍

A two-sample MR analysis was performed on the data sourced from publicly available genome-wide association study (GWAS) of endometriosis and infertility. For each subtype of endometriosis, instrumental variables (IVs) satisfying MR assumptions were selected, with inverse variance weighting (IVW) as primary method. Sensitivity analyses, including Cochran’s Q test, MR-Egger regression, and leave-one-out analysis, were conducted to verify the robustness of the results. Statistical significance was set at P<0.01 (Bonferroni correction), and P<0.05 was considered as suggestive significance.

Results‍

Among different locations of endometriosis, ovary (IVW: OR=1.26, 95%CI: 1.17~1.35, P<0.001), pelvic peritoneum (IVW: OR=1.26, 95%CI: 1.20~1.33, P<0.001), rectovaginal septum (IVW: OR=1.11, 95%CI: 1.06~1.16, P<0.001), adenomyosis (IVW: OR=1.16, 95%CI: 1.07~1.25, P<0.001), and other types of endometriosis (IVW: OR=1.10, 95%CI: 1.03~1.17, P=0.004) were significantly associated with infertility. But no such association was observed in fallopian tube and intestinal endometriosis with infertility (P>0.05). Reverse causality analysis indicated that infertility might lead to fallopian tube endometriosis (IVW: OR=1.46, 95%CI: 1.11~1.93, P=0.007), and was associated with ovarian (IVW: OR=1.56, 95%CI: 1.27~1.93, P<0.001), pelvic peritoneal (IVW: OR=1.34, 95%CI: 1.11~1.62, P=0.003), rectovaginal (IVW: OR=1.46, 95%CI: 1.11~1.93, P=0.007), and other types of endometriosis (IVW: OR=1.61, 95%CI: 1.21~2.13, P=0.001). Suggestive significance was observed statistically in infertility promoting adenomyosis (IVW: OR=1.16, 95%CI: 1.07~1.25, P<0.05). It had not been proven yet that infertility could lead to intestinal endometriosis (P>0.05). Sensitivity analyses confirmed the robustness of the results.

Conclusion‍

Bidirectional causal relationships exist between different subtypes of endometriosis and infertility. Our findings based on MR analysis validate the clinical observation that endometriosis can lead to infertility, and we exploratively propose an important conclusion that infertility itself may also induce endometriosis. However, due to limited data, the causal relationships between intestinal/tubal endometriosis and infertility require further investigation.

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目的

本研究旨在通过孟德尔随机化（Mendelian randomization，MR）探讨不同亚型的子宫内膜异位症与女性不孕症之间的双向因果关系。

方法

采用两样本MR方法，数据来源于公共数据库全基因组关联研究的子宫内膜异位症和不孕症队列。为每种亚型选择满足MR假设的工具变量（instrumental variables，IVs），主要方法为逆方差加权（inverse variance weighting，IVW）。通过Cochran’s Q检验、MR-Egger回归和留一法等敏感性分析验证结果的稳健性，统计显著性设定为P<0.01（Bonferroni校正），但当P<0.05时定义为潜在的显著性。

结果

在不同部位的子宫内膜异位症中，卵巢（IVW：OR=1.26，95%CI：1.17~1.35，P<0.001）、盆腔腹膜（IVW：OR=1.26，95%CI：1.20~1.33，P<0.001）、直肠阴道隔（IVW：OR=1.11，95% CI：1.06~1.16，P<0.001）、子宫腺肌症（IVW：OR=1.16，95%CI：1.07~1.25，P<0.001）和其他部位的子宫内膜异位症（IVW：OR=1.10，95%CI：1.03~1.17，P=0.004）与不孕症显著相关。输卵管和肠道子宫内膜异位症未显示出显著关联（P>0.05）。反向因果分析表明，不孕症可能会导致输卵管子宫内膜异位症（IVW：OR=1.46，95%CI：1.11~1.93，P=0.007），并与卵巢（IVW：OR=1.56，95%CI：1.27~1.93，P<0.001）、盆腔腹膜（IVW：OR=1.34，95%CI：1.11~1.62，P=0.003）、直肠阴道隔（IVW：OR=1.46，95%CI：1.11~1.93，P=0.007）、其他部位的子宫内膜异位症（IVW：OR=1.61，95%CI：1.21~2.13，P=0.001）相关。不孕症促进子宫腺肌病的发生具有潜在的统计显著性（IVW：OR=1.16，95%CI：1.07~1.25，P<0.05）。还不能证明不孕症可以导致肠道子宫内膜异位症（P>0.05）。敏感性分析证实了结果的稳健性。

结论

不同亚型的子宫内膜异位症与不孕症之间存在双向因果关系。即本研究应用MR方法验证了子宫内膜异位症可导致不孕症这一临床观察现象，同时还探索性的提出了不孕症本身也可能引发子宫内膜异位症这一重要结论。其中，卵巢子宫内膜异位症对不孕症的影响最大。

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王伟，E-mail：
WANG Wei，E-mail：
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Acta Obstet Gynecol Scand，2017，96（6）：702-706., articleTitle=Endometriosis and uterine malformations：infertility may increase severity of endometriosis, refAbstract=null)], funds=null, companyList=[AuthorCompany(id=1322190385401672361, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1322190384151769760, xref=1, ext=[AuthorCompanyExt(id=1322190385410060970, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1322190384151769760, companyId=1322190385401672361, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1Reproductive Medicine Center，Seventh Medical Center，Chinese PLA General Hospital，Beijing), AuthorCompanyExt(id=1322190385418449579, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1322190384151769760, companyId=1322190385401672361, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=1中国人民解放军总医院第七医学中心生殖医学科，北京)]), AuthorCompany(id=1322190385481364140, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1322190384151769760, xref=2, ext=[AuthorCompanyExt(id=1322190385489752749, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1322190384151769760, companyId=1322190385481364140, language=EN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2Prenatal Diagnosis Center，Beijing Obstetrics and Gynecology Hospital，Capital Medical University/Beijing Maternal and Child Health Care Hospital，Beijing，China), AuthorCompanyExt(id=1322190385498141358, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1322190384151769760, companyId=1322190385481364140, language=CN, country=null, province=null, city=null, postcode=null, companyName=null, departmentName=null, remark=2首都医科大学附属北京妇产医院/北京妇幼保健院产前诊断中心，北京)])], figs=[ArticleFig(id=1322190387150697163, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1322190384151769760, language=EN, label=Figure 1, caption=Core assumptions for Mendelian randomization, figureFileSmall=q77I7XgyxKwl3t69i9p/jA==, figureFileBig=woJ/jQWWAXzAd3Yij+k3BQ==, tableContent=null), ArticleFig(id=1322190389528867532, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1322190384151769760, language=CN, label=图1, caption=孟德尔随机化核心假设

Mendelian randomization yields robust causal inferences only when the 3 fundamental assumptions，independence，exclusion，and relevance，are satisfied. This study employs a bidirectional design in which 7 anatomically distinct sub-phenotypes of endometriosis and infertility serve alternately as the exposure and the outcome

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Owing to the limited case counts for tubal and intestinal endometriosis，the corresponding estimates are presented as exploratory analyses. Inverse-variance weighted （IVW） regression served as primary Mendelian randomization （MR） method，with the odds-ratio （OR） directions derived from the weighted median （WM） and MR-Egger regressions provided for reference. nSNP denotes the number of instrumental variables （IVs） employed in each MR analysis. The OR quantifies the infertility odds among individuals with a specific endometriosis subtype relative to the general population. Heterogeneity was assessed via Cochran’s Q statistic，with Q.P<0.05 indicating significant heterogeneity. An MR-Egger intercept （Egger.intercept） close to zero accompanied by a pleiotropy P value >0.05 is interpreted as the absence of directional pleiotropy

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Due to the limited case counts for tubal and intestinal endometriosis，the corresponding results are reported as exploratory analyses. All other interpretations follow those described for Figure 2

, figureFileSmall=7XrB9p4ee0L5lPpRr2A1kw==, figureFileBig=bpvfQhol9Ra2Ox3OAoOLgA==, tableContent=null), ArticleFig(id=1322190390065738449, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1322190384151769760, language=EN, label=Table 1, caption=

Phenotypes analyzed and the GWAS summary statistics selected as exposure or outcome data

, figureFileSmall=null, figureFileBig=null, tableContent=
PhenotypeGWAS IDCase/ControlSNPs
Endometrioses
Fallopian tubefinn-b-N14_ENDOMETRIOSIS_FALLOPIAN_TUBE116/68 96916376156
Intestinefinn-b-N14_ENDOMETRIOSIS_INTESTINE177/68 96916376157
Ovaryfinn-b-N14_ENDOMETRIOSIS_OVARY3 231/68 96916376686
Pelvic peritoneumfinn-b-N14_ENDOMETRIOSIS_PELVICPERITONEUM2 953/68 96916376599
Rectovaginalfinn-b-N14_ENDOMETRIOSIS_RECTPVAGSEPT_VAGINA1 360/68 96916376472
Uterusfinn-b-N14_ENDOMETRIOSIS_UTERUS2 372/68 96916376529
Othersfinn-b-N14_ENDOMETRIOSIS_NOS1 435/68 96916376331
Infertilityfinn-b-N14_FEMALEINFERT6 481/68 96916377038
), ArticleFig(id=1322190390137041618, tenantId=1146029695717560320, journalId=1319373162502258839, articleId=1322190384151769760, language=CN, label=表1, caption=

分析的表型及选定作为暴露/结果数据的GWAS汇总统计数据

, figureFileSmall=null, figureFileBig=null, tableContent=
PhenotypeGWAS IDCase/ControlSNPs
Endometrioses
Fallopian tubefinn-b-N14_ENDOMETRIOSIS_FALLOPIAN_TUBE116/68 96916376156
Intestinefinn-b-N14_ENDOMETRIOSIS_INTESTINE177/68 96916376157
Ovaryfinn-b-N14_ENDOMETRIOSIS_OVARY3 231/68 96916376686
Pelvic peritoneumfinn-b-N14_ENDOMETRIOSIS_PELVICPERITONEUM2 953/68 96916376599
Rectovaginalfinn-b-N14_ENDOMETRIOSIS_RECTPVAGSEPT_VAGINA1 360/68 96916376472
Uterusfinn-b-N14_ENDOMETRIOSIS_UTERUS2 372/68 96916376529
Othersfinn-b-N14_ENDOMETRIOSIS_NOS1 435/68 96916376331
Infertilityfinn-b-N14_FEMALEINFERT6 481/68 96916377038
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子宫内膜异位症亚型与不孕症的因果关系：双向孟德尔随机化研究
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王业 1 , 钟威 2 , 商微 1 , 王伟 1
陆军军医大学学报 | 临床医学 2025,47(16): 1962-1969
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陆军军医大学学报 |临床医学 2025 , 47 (16) : 1962 -1969
子宫内膜异位症亚型与不孕症的因果关系：双向孟德尔随机化研究
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王业1, 钟威2, 商微1, 王伟1
作者信息
  • 1中国人民解放军总医院第七医学中心生殖医学科，北京
  • 2首都医科大学附属北京妇产医院/北京妇幼保健院产前诊断中心，北京
通讯作者:
王伟，E-mail：
WANG Wei，E-mail：
Causal effects between different sub-phenotypes of endometriosis and female infertility: a bidirectional Mendelian randomization study
Ye WANG1, Wei ZHONG2, Wei SHANG1, Wei WANG1
Affiliations
  • 1Reproductive Medicine Center，Seventh Medical Center，Chinese PLA General Hospital，Beijing
  • 2Prenatal Diagnosis Center，Beijing Obstetrics and Gynecology Hospital，Capital Medical University/Beijing Maternal and Child Health Care Hospital，Beijing，China
出版时间: 2025-08-30 doi: 10.16016/j.2097-0927.202505029
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摘要
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目的

本研究旨在通过孟德尔随机化（Mendelian randomization，MR）探讨不同亚型的子宫内膜异位症与女性不孕症之间的双向因果关系。

方法

采用两样本MR方法，数据来源于公共数据库全基因组关联研究的子宫内膜异位症和不孕症队列。为每种亚型选择满足MR假设的工具变量（instrumental variables，IVs），主要方法为逆方差加权（inverse variance weighting，IVW）。通过Cochran’s Q检验、MR-Egger回归和留一法等敏感性分析验证结果的稳健性，统计显著性设定为P<0.01（Bonferroni校正），但当P<0.05时定义为潜在的显著性。

结果

在不同部位的子宫内膜异位症中，卵巢（IVW：OR=1.26，95%CI：1.17~1.35，P<0.001）、盆腔腹膜（IVW：OR=1.26，95%CI：1.20~1.33，P<0.001）、直肠阴道隔（IVW：OR=1.11，95% CI：1.06~1.16，P<0.001）、子宫腺肌症（IVW：OR=1.16，95%CI：1.07~1.25，P<0.001）和其他部位的子宫内膜异位症（IVW：OR=1.10，95%CI：1.03~1.17，P=0.004）与不孕症显著相关。输卵管和肠道子宫内膜异位症未显示出显著关联（P>0.05）。反向因果分析表明，不孕症可能会导致输卵管子宫内膜异位症（IVW：OR=1.46，95%CI：1.11~1.93，P=0.007），并与卵巢（IVW：OR=1.56，95%CI：1.27~1.93，P<0.001）、盆腔腹膜（IVW：OR=1.34，95%CI：1.11~1.62，P=0.003）、直肠阴道隔（IVW：OR=1.46，95%CI：1.11~1.93，P=0.007）、其他部位的子宫内膜异位症（IVW：OR=1.61，95%CI：1.21~2.13，P=0.001）相关。不孕症促进子宫腺肌病的发生具有潜在的统计显著性（IVW：OR=1.16，95%CI：1.07~1.25，P<0.05）。还不能证明不孕症可以导致肠道子宫内膜异位症（P>0.05）。敏感性分析证实了结果的稳健性。

结论

不同亚型的子宫内膜异位症与不孕症之间存在双向因果关系。即本研究应用MR方法验证了子宫内膜异位症可导致不孕症这一临床观察现象，同时还探索性的提出了不孕症本身也可能引发子宫内膜异位症这一重要结论。其中，卵巢子宫内膜异位症对不孕症的影响最大。

子宫内膜异位症  /  不孕症  /  孟德尔随机化  /  子宫腺肌病
Objective‍

To investigate the bidirectional causal relationship between different subtypes of endometriosis and female infertility using Mendelian randomization (MR).

Methods‍

A two-sample MR analysis was performed on the data sourced from publicly available genome-wide association study (GWAS) of endometriosis and infertility. For each subtype of endometriosis, instrumental variables (IVs) satisfying MR assumptions were selected, with inverse variance weighting (IVW) as primary method. Sensitivity analyses, including Cochran’s Q test, MR-Egger regression, and leave-one-out analysis, were conducted to verify the robustness of the results. Statistical significance was set at P<0.01 (Bonferroni correction), and P<0.05 was considered as suggestive significance.

Results‍

Among different locations of endometriosis, ovary (IVW: OR=1.26, 95%CI: 1.17~1.35, P<0.001), pelvic peritoneum (IVW: OR=1.26, 95%CI: 1.20~1.33, P<0.001), rectovaginal septum (IVW: OR=1.11, 95%CI: 1.06~1.16, P<0.001), adenomyosis (IVW: OR=1.16, 95%CI: 1.07~1.25, P<0.001), and other types of endometriosis (IVW: OR=1.10, 95%CI: 1.03~1.17, P=0.004) were significantly associated with infertility. But no such association was observed in fallopian tube and intestinal endometriosis with infertility (P>0.05). Reverse causality analysis indicated that infertility might lead to fallopian tube endometriosis (IVW: OR=1.46, 95%CI: 1.11~1.93, P=0.007), and was associated with ovarian (IVW: OR=1.56, 95%CI: 1.27~1.93, P<0.001), pelvic peritoneal (IVW: OR=1.34, 95%CI: 1.11~1.62, P=0.003), rectovaginal (IVW: OR=1.46, 95%CI: 1.11~1.93, P=0.007), and other types of endometriosis (IVW: OR=1.61, 95%CI: 1.21~2.13, P=0.001). Suggestive significance was observed statistically in infertility promoting adenomyosis (IVW: OR=1.16, 95%CI: 1.07~1.25, P<0.05). It had not been proven yet that infertility could lead to intestinal endometriosis (P>0.05). Sensitivity analyses confirmed the robustness of the results.

Conclusion‍

Bidirectional causal relationships exist between different subtypes of endometriosis and infertility. Our findings based on MR analysis validate the clinical observation that endometriosis can lead to infertility, and we exploratively propose an important conclusion that infertility itself may also induce endometriosis. However, due to limited data, the causal relationships between intestinal/tubal endometriosis and infertility require further investigation.

endometriosis  /  infertility  /  Mendelian randomization  /  adenomyosis
王业, 钟威, 商微, 王伟. 子宫内膜异位症亚型与不孕症的因果关系：双向孟德尔随机化研究. 陆军军医大学学报, 2025 , 47 (16) : 1962 -1969 . DOI: 10.16016/j.2097-0927.202505029
Ye WANG, Wei ZHONG, Wei SHANG, Wei WANG. Causal effects between different sub-phenotypes of endometriosis and female infertility: a bidirectional Mendelian randomization study[J]. Journal of Army Medical University, 2025 , 47 (16) : 1962 -1969 . DOI: 10.16016/j.2097-0927.202505029
正文
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不孕症作为一种全球性的健康问题，影响着大约16.67%的夫妇［1］。不孕症的病因繁多，包括激素失衡、解剖结构异常、遗传性疾病以及特定的健康状况。这些因素有可能干扰诸如排卵、受精和着床等关键过程，从而阻碍成功妊娠及后续的胚胎发育。子宫内膜异位症是一种常见的妇科疾病，目前被认为与不孕症相关，并且有25%至50%的不孕患者受到该病的影响［2］。该病的特征是子宫内膜样组织在子宫外的异常生长。子宫内膜异位症可能会导致慢性盆腔疼痛、痛经，甚至不孕［3］。尽管子宫内膜异位症与不孕症之间的关联已在临床上得到广泛认可，但它们之间关联的精确机制尚未明确，可能涉及多种途径。
更值得关注的是，反向关联，即不孕症是否会增加罹患子宫内膜异位症的风险，这一观点尚未得到广泛研究，这涉及生殖功能障碍与子宫内膜病理生理学之间复杂相互作用的深刻问题［4］。此外，将不同发生部位的子宫内膜异位症作为独立的对象进行研究，有望揭示新的见解［5］。遗憾的是，受限于特定亚型的患者数量，此前仅有少数研究采用了亚组分析的方式。
既往的观察性研究在探讨子宫内膜异位症与不孕症之间的因果联系时面临挑战［6］，它们往往受到混杂因素和偏倚的影响，无法建立明确的因果联系。此外，诊断子宫内膜异位症通常需要借助腹腔镜等侵入性操作，而这些操作在所有研究环境中可能并不总是可行的，也未必总是符合伦理。因此，目前子宫内膜异位症与不孕症的关联性方面仍呈现出不够完整且可能存在歧义的观点。
孟德尔随机化（Mendelian randomization，MR）方法涉及利用遗传变异来构建工具变量（instrumental variables，IVs），以代表某种感兴趣的暴露因素，从而可以估计暴露因素与结果之间的因果联系。由于等位基因的随机分配不受常见混杂因素的影响，因此通过该方法建立的因果关系通常被认为较为稳健和可靠。
在本研究中，我们利用全基因组关联研究（genome-wide association study，GWAS）所获得的汇总统计数据，开展了一项双向孟德尔随机化研究。本研究的主要目标是评估子宫内膜异位症与不孕症之间的因果联系。此外，鉴于子宫内膜异位症具有异质性，可在不同解剖位置表现出多种形态，并且关于其具体亚型与不孕症之间的关联性一直存在争议［7-9］。因此，本研究深入地分析子宫内膜异位症的不同亚型与不孕症之间的因果关系。
1　材料和方法
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1.1　工具变量的选择与强度检验
在MR研究中，必须满足3个基本假设。第一，要求遗传变量与研究的暴露因素显著相关。第二，要求作为暴露因素的IVs与其他混杂因素相互独立。第三个假设是遗传变量仅通过其对暴露因素来影响结果，从而排除水平多效性（图1）。本研究首先从公开可用的GWAS汇总数据中选取了7种子宫内膜异位症亚型作为暴露因素。这些亚型包括：输卵管、肠道、卵巢、盆腔腹膜、子宫腺肌病、直肠阴道隔和其他部位的子宫内膜异位症。子宫内膜异位症的数据来源于FinnGen队列。利用GWAS汇总统计数据，为每种子宫内膜异位症亚型筛选出IVs，本研究中的IVs为单核苷酸多态性（single nucleotide polymorphism，SNP）。具体来说，将与7种子宫内膜异位症在全基因组水平上显著相关的SNPs（P<5E-6）确定为后续MR研究的候选IVs。随后，为确保每个暴露表型的IVs相互独立，我们进行了基于连锁不平衡的聚类分析，剔除了处于强连锁不平衡（linkage disequilibrium，LD）状态的SNPs（r2=0.1，窗口大小为10 Mb）。对于在暴露数据中不存在的SNPs，我们利用“千人基因组计划”欧洲人群的数据（r2>0.8），找出与其相关性最高的代理SNPs。此外，我们还排除了等位基因不一致以及无法在暴露与结果数据协调过程中解决的回文结构且链方向模糊的SNPs。经过严格筛选的这些SNPs随后被用作我们MR研究的IVs。最后，我们还计算了每个IV的F统计量，F值大于10表示不存在IV偏倚。
1.2　数据收集
所有数据均来源于GWAS平台（https://gwas.mrcieu.ac.uk/）所提供的汇总数据，因此不需要伦理委员会审批。这包括7种亚型的子宫内膜异位症以及不孕症队列（表1）。这是该平台迄今为止符合本研究设计的样本量最大的GWAS研究。本研究进行了两样本MR分析，首先估计各种子宫内膜异位症亚型是否可以导致不孕症。为了探索反向因果关系，本研究还使用不孕症数据作为暴露，7种不同的子宫内膜异位症亚型作为结果。需要说明，由于输卵管和肠道子宫内膜异位症中病例数较少（分别为116例和177例），因此涉及这两种类型的MR分析结论是探索性的。当P值小于0.01（Bonferroni校正的0.05/5）为显著性阈值，并将P值在0.01到0.05之间的结果视为潜在的显著性，以减少假阴性的结论。
子宫内膜异位症根据以下诊断编码进行定义：国际疾病分类第十版（ICD-10）中的N80、ICD-9中的617以及ICD-8中的6253。最终，从FinnGen队列中汇总各种子宫内膜异位症亚型和不孕症的数据，具体信息如表1所示。
1.3　统计方法
所有分析均使用R软件（版本4.3.1）中的TwoSampleMR软件包（版本0.5.6）进行。应用三种基于不同假设的MR方法：IVW、加权平均（WM）和MR-Egger回归。其中，IVW由于最敏感因此作为主要的统计模型。WM和MR-Egger回归的OR方向作为参考。首先，通过汇总每个IV的Wald比率估计值，使用固定效应IVW方法计算因果估计值。在观察到显著的异质性（P<0.05）的情况下，采用随机效应方法。
IVW方法可能因无效IVs而易受偏倚或多重效应的影响。为确保结果的有效性和稳健性，进行多种敏感性分析。为探索因果估计中的异质性，通过Cochran’s Q量化异质性的程度，显著性设定为P<0.05。为评估与IVs相关的水平多效性，我们应用了MR-Egger回归。MR-Egger回归中的截距项表明因果估计中可能存在水平多效性。在IVs中检测到水平多效性的情况下，我们进一步使用PhenoScanner（http://www.phenoscanner.medschl.cam.ac.uk/）来识别并排除可能影响结果的IVs。研究还采用留一法分析，系统地逐一排除每个SNP，随后在剩余的SNPs上进行了MR分析，以识别潜在的IVs异常值。
2　结果
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2.1　工具变量
在本研究中，所有F统计量均大于10，表明弱IV偏倚的可能性较低（补充材料）。值得注意的是，在对某些类型的子宫内膜异位症进行数据协调中，特定的SNPs被排除。在肠道子宫内膜异位症数据中，由于不兼容性，SNP rs75607141被移除。同样地，在卵巢子宫内膜异位症的IVs中，SNP rs142807069被剔除。此外，我们还利用PhenoScanner识别并剔除3个表现出水平多效性的IVs中的SNPs：在直肠阴道隔子宫内膜异位症数据中，两个IVs被排除。在其他部位的子宫内膜异位症数据协调过程中，SNP rs10738609被移除。在以不孕症作为暴露因素的MR研究中，采取相同研究方法来解决水平多效性问题：剔除了SNP rs111992780。该SNP表现出可能与子宫肌瘤有关的潜在关联，而子宫肌瘤可能与子宫内膜异位症有关［10］。
2.2　不同亚型的子宫内膜异位症对不孕症的影响
MR分析结果显示，输卵管和肠道的子宫内膜异位症可能对不孕症没有显著影响（图2）。然而，如前所述，这两种亚型的MR研究的统计效能可能因为病例数量有限受到影响［11］。在其余5种子宫内膜异位症亚型中，卵巢子宫内膜异位症、盆腔腹膜子宫内膜异位症、直肠阴道隔子宫内膜异位症、子宫腺肌病以及其他类型的子宫内膜异位症均与不孕症呈现出正相关性（P<0.01）。所有IVW方法的OR方向与MR-Egger和WM方法的结果方向一致，从而表明结果的稳健性。敏感性分析中的森林图、漏斗图以及留一法分析也表明了该结果的可靠性。
2.3　不孕症对不同亚型的子宫内膜异位症的影响
探索性分析的结果显示（图3），不孕症可能是输卵管子宫内膜异位症的潜在诱发因素（P=0.007），但似乎并不影响肠道子宫内膜异位症的发展（P=0.298）。此外，不孕症可导致其他亚型的子宫内膜异位症：包括卵巢、盆腔腹膜、直肠阴道隔以及其他部位的子宫内膜异位症。所有这些疾病亚型在IVW方法下均观察到统计显著性（P<0.01）。此外，不孕症可能导致子宫腺肌病（IVW：OR=1.16，95%CI：1.07~1.25，0.01<P<0.05）。同样的，敏感性分析也证明了该过程的MR研究结果的稳健性。
3　讨论
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据我们所知，在既往研究中尚未有关于不同亚型子宫内膜异位症与不孕症风险关联的MR研究报道。本研究旨在通过剖析两种疾病间的复杂因果关联，为子宫内膜异位症和不孕症的临床实践提供科学且具价值的参考见解，这一探索将填补该领域研究的空白。
尽管在临床实践中，子宫内膜异位症与不孕症之间的相关性得到了广泛认可，但确切的因果联系仍然是一个存在争议的话题［12］。特别是对于不同亚型的子宫内膜异位症与不孕症之间的关系，目前仍不清楚［13］。为了探讨这种复杂的关系，有必要考虑使用不同亚型的大量病例进行研究，因为每种亚型都有其独特的形态和发病机制［14］。此外，必须认识到，诊断子宫内膜异位症是一个巨大的挑战［15-17］，研究结论必须依赖于高质量的数据。在本研究中，我们进行了双向MR研究，利用多个权威的GWAS汇总数据，探索了七种子宫内膜异位症亚型与不孕症之间的因果关系。总体而言，研究结果表明，不同亚型的子宫内膜异位症和不孕症之间存在双向因果联系。然而，由于输卵管和肠道子宫内膜异位症的数据有限，还需要后续进一步研究以确定其与不孕症的因果关系。
输卵管子宫内膜异位症对生育能力的影响仍然具有争议［18］。一项观察性研究［2］表明，患有输卵管子宫内膜异位症的患者表现出较高的输卵管阻塞发生率。此外，输卵管的正常解剖结构发生扭曲以及卵巢上出现粘连可能会阻碍输卵管与卵巢之间的接触，这是导致输卵管子宫内膜异位症患者不孕的一个关键因素。然而，只有少数患者可能会经历双侧输卵管阻塞［2］。因此对于那些没有明显解剖结构改变的患者，可能存在其他导致不孕的机制。在本研究中，输卵管子宫内膜异位症似乎与不孕风险增加无关。然而，这种关联性的缺乏可能归因于样本量相对较小而导致的统计效能有限。
关于肠道子宫内膜异位症的自然受孕率的数据稀缺，这使得评估该亚型对生育能力的影响变得困难［7］。此外，关于手术干预是否能提高肠道子宫内膜异位症患者的自然妊娠率和体外受精成功率，不同研究之间存在异质性［9］。在本研究中，由于肠道子宫内膜异位症的病例数有限，这阻碍了本研究确定其与不孕症之间明确的因果关系。
卵巢是子宫内膜异位症最常见的发生部位［2-3］。卵巢子宫内膜异位症对生殖功能产生不利影响的主要因素是卵巢储备的下降。这种下降可能归因于子宫内膜异位囊肿的直接性腺毒性作用，或者是手术干预过程中对正常卵巢组织的切除［19］。受影响的患者可能会出现卵泡发育异常和局部炎症，从而导致卵巢储备减少和卵子质量降低。然而，卵巢子宫内膜异位症与生育能力之间的关系仍然存在不确定性［20］。一些研究表明，卵巢子宫内膜异位症本身可能对生育能力没有负面影响［13］。然而，需要注意的是，既往结论主要来源于观察性研究。相比之下，本研究采用的MR方法，提供了更高等级的证据。我们的研究结果表明卵巢子宫内膜异位症与不孕风险增加之间存在强有力的联系（OR=1.26，P<0.001）。此外，考虑到OR值的大小，结果也表明卵巢子宫内膜异位症对不孕症的影响比其他亚型更为显著。这凸显了临床医生在通过影像学或者其他诊断方法检测到卵巢子宫内膜异位症时，为患者提供生育咨询的重要性。
盆腔腹膜子宫内膜异位症是一种浅表型子宫内膜异位症。早期的研究一致表明，这种亚型与不孕症之间存在很强的联系［21］。除了有可能破坏正常的解剖结构外，与子宫内膜异位症本身相关的潜在病理机制也可能导致不孕。我们的结果支持了以往的研究。
直肠阴道隔子宫内膜异位症是深部浸润型子宫内膜异位症的一种表现形式，其特征是子宫内膜组织沉积在直肠和阴道之间。在各种非生殖器官的子宫内膜异位症中，它被认为是最严重的类型，通常伴有剧烈疼痛。与这种情况相关的常见症状包括直肠-会阴疼痛、性交痛以及反复发作的脓性阴道分泌物［22］。目前尚不确定手术是否能提高自然受孕的机会［12］。深部子宫内膜异位症与不孕症之间的联系仍然不确定，解读现有的证据也存在挑战［12，22］。然而，本研究提供了有力的证据，表明直肠阴道隔子宫内膜异位症也能导致不孕症（OR=1.11，P<0.001）。这一发现支持了针对这种严重的子宫内膜异位症亚型，以缓解症状和提高自然妊娠率为目的的手术干预可能是有益的这一观点。
子宫腺肌病的特征是在子宫肌层内存在类似子宫内膜的上皮和间质，这与子宫内膜异位症有所不同。然而，也有观点认为子宫腺肌病是子宫内膜组织在子宫肌层内的异位生长，但并不将其视为子宫内膜异位症的一种形式［23］。由于既往研究有限且研究设计存在差异，子宫腺肌病对生育能力的影响仍有争议［24］。一项涉及超过2000名接受体外受精的受试者的队列研究，排除了卵巢储备减少和同时患有子宫内膜异位症的个体，发现子宫腺肌病对体外受精的结果有负面影响，包括流产风险增加和活产率降低［25］。本研究也支持子宫腺肌病对不孕症的负面影响。因此，在处理患者的不孕问题时，无论是自然受孕还是使用辅助生殖技术，都必须考虑子宫腺肌病的影响。
子宫内膜异位症的其他不常见亚型出现在罕见部位，如膈肌、胸膜、腹壁或中枢和外周神经系统。这些不太常见的子宫内膜异位症形式与不孕症之间的关联此前研究有限。尽管如此，我们的研究表明它们可能会增加不孕症的风险。因此，我们推测子宫内膜异位症本身可能通过各种复杂的机制引发患者生殖系统的紊乱。子宫内膜异位症的发生程度和位置可能是影响对不孕症风险影响程度的关键因素。
本研究为不孕症在子宫内膜异位症发展过程中发挥作用的假设提供了有力支持。这一发现尤为重要。MR方法的应用对于避免观察性研究中常见的逆向因果问题起到了关键作用。尽管在临床上已经公认部分子宫内膜异位症可导致不孕症，但既往一直缺乏明确的方法来研究不孕症本身是否能增加罹患子宫内膜异位症的风险。需要指出的是，女性不孕症的常见原因包括排卵障碍、盆腔粘连、高催乳素血症和子宫内膜异位症［2］，因此和子宫内膜异位症的关系更加错综复杂。此外，不孕症本身可能会引发各种心理健康问题，包括抑郁、焦虑、攻击性、恐惧症、性功能障碍、解离和睡眠障碍，尤其是在症状持续较长时间的情况下［26］。还需要注意，不孕症是最重要的生活压力源之一。长期暴露于慢性压力可能会破坏神经内分泌平衡，导致激素失调［27，28］。因此，这种失调可能是不孕症诱发子宫内膜异位症的机制之一。此外，不明原因不孕的女性可能面临更高的心血管疾病风险［29］，这可能会导致过早死亡［30］。还有研究指出，在有子宫解剖异常的女性中，不孕症可能会加剧子宫内膜异位症的严重程度［31］。综上所述，不孕症本身可能通过多种途径作为一个复杂的触发因素，诱发子宫内膜异位症的发展。
据我们所知，这是首次开展的探讨不同亚型的子宫内膜异位症与不孕症风险之间因果关联的MR研究。这些发现凸显了不孕症与子宫内膜异位症风险之间存在的复杂的双向因果关系。本研究显著地增进了研究者对这两种生殖重要疾病发病机制的理解。可以说，我们的研究结果为未来更广泛的相关研究奠定了基础。这些未来的研究将更深入地探讨特定亚型的子宫内膜异位症在影响不孕症中的具体作用，以及探索这两种状况的复杂因果关系。
当然，本研究有以下的局限性。本研究中使用的GWAS数据代表了迄今为止针对这些特定子宫内膜异位症亚型的最全面的人群队列。但是在寻找与不孕症相关的队列时，我们遇到了潜在样本量重叠的挑战，因为大部分数据都来自FinnGen队列。遗憾的是，目前这个问题还无法避免。在未来，从其他来源获取类似的汇总统计数据以全面验证我们的结论将是至关重要的。此外，本研究的结论来源于欧洲人群。未来在不同种族中开展更多的类似的MR研究将是不可或缺的，因为因果关系可能会在不同种族群体之间存在差异。
总而言之，我们的研究揭示了绝大部分的子宫内膜异位症亚型与不孕症之间的双向因果关系。即不仅创新地应用MR方法验证了子宫内膜异位症可导致不孕症这一临床观察现象，同时还探索性地提出了不孕症本身也可能引发子宫内膜异位症这一重要结论。其中，卵巢子宫内膜异位症对不孕症的影响最大。然而，由于研究中部分病例数据相对不足，输卵管和肠道的子宫内膜异位症与不孕症的确切因果关联还需要后续进一步研究证明。

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doi: 10.16016/j.2097-0927.202505029
  • 接收时间：2025-05-13
  • 首发时间：2026-10-28
  • 出版时间：2025-08-30
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  • 收稿日期：2025-05-13
  • 修回日期：2025-07-22
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    1中国人民解放军总医院第七医学中心生殖医学科，北京
    2首都医科大学附属北京妇产医院/北京妇幼保健院产前诊断中心，北京

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王伟，E-mail：
WANG Wei，E-mail：
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2种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
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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