Research Progress in Pathogenesis and Diagnosis of Chronic Endometritis

doi:10.12280/gjfckx.20220626

Abstract

Abstract:

Establishment of endometrial receptivity is a important condition for successful embryo implantation. With the assisted reproductive technology getting better, endometrial abnormalities have become the most important factor of embryo implantation. Chronic endometritis (CE) is characterized by persistent mucosal stromal edema, focal or diffuse hyperemia and stromal plasmacyte infiltration. CE could cause adverse pregnancy outcomes by affecting endometrial receptivity. By the way, CE may be associated with the occurrence of endometrial polyps, endometriosis and intrauterine adhesions. The treatment of antibiotics could significantly improve the clinical outcomes of assisted reproductive technology. This article reviews the etiology, diagnosis and treatment of CE, and summarize the research progress under the influence of CE on assisted reproductive technology as well.

Key words: Chronic endometritis, Syndecan-1, Embryo implantation, Anti-bacterial agents, Reproductive techniques, assisted, Endometrial receptivity

WANG Xiu-zhu, CHEN Xue-mei, LIU Xue-mei. Research Progress in Pathogenesis and Diagnosis of Chronic Endometritis[J]. Journal of International Obstetrics and Gynecology, 2023, 50(1): 102-108.

References 46

[1]	Craciunas L, Gallos I, Chu J, et al. Conventional and modern markers of endometrial receptivity: a systematic review and meta-analysis[J]. Hum Reprod Update, 2019, 25(2):202-223. doi: 10.1093/humupd/dmy044. doi: 10.1093/humupd/dmy044 pmid: 30624659
[2]	Buzzaccarini G, Vitagliano A, Andrisani A, et al. Chronic endometritis and altered embryo implantation: a unified pathophysiological theory from a literature systematic review[J]. J Assist Reprod Genet, 2020, 37(12):2897-2911. doi: 10.1007/s10815-020-01955-8. doi: 10.1007/s10815-020-01955-8
[3]	Cicinelli E, Matteo M, Tinelli R, et al. Chronic endometritis due to common bacteria is prevalent in women with recurrent miscarriage as confirmed by improved pregnancy outcome after antibiotic treatment[J]. Reprod Sci, 2014, 21(5):640-647. doi: 10.1177/1933719113508817. doi: 10.1177/1933719113508817 pmid: 24177713
[4]	Vicetti Miguel RD, Chivukula M, Krishnamurti U, et al. Limitations of the criteria used to diagnose histologic endometritis in epidemiologic pelvic inflammatory disease research[J]. Pathol Res Pract, 2011, 207(11):680-685. doi: 10.1016/j.prp.2011.08.007. doi: 10.1016/j.prp.2011.08.007 pmid: 21996319
[5]	Cicinelli E, Matteo M, Trojano G, et al. Chronic endometritis in patients with unexplained infertility: Prevalence and effects of antibiotic treatment on spontaneous conception[J]. Am J Reprod Immunol, 2018, 79(1). doi: 10.1111/aji.12782. doi: 10.1111/aji.12782
[6]	Cicinelli E, Vitagliano A, Kumar A, et al. Unified diagnostic criteria for chronic endometritis at fluid hysteroscopy: proposal and reliability evaluation through an international randomized-controlled observer study[J]. Fertil Steril, 2019, 112(1):162-173.e2. doi: 10.1016/j.fertnstert.2019.03.004. doi: S0015-0282(19)30247-X pmid: 31104760
[7]	Peng J, Guo F, Liu H, et al. Correlation between hysteroscopy findings in patients with hydrosalpinx and chronic endometritis[J]. Int J Gynaecol Obstet, 2022, 157(2):471-475. doi: 10.1002/ijgo.13895. doi: 10.1002/ijgo.13895
[8]	Espinós JJ, Fabregues F, Fontes J, et al. Impact of chronic endometritis in infertility: a SWOT analysis[J]. Reprod Biomed Online, 2021, 42(5):939-951. doi: 10.1016/j.rbmo.2021.02.003. doi: 10.1016/j.rbmo.2021.02.003 pmid: 33736994
[9]	宣瑞红. CD38和CD138及MUM-1在慢性子宫内膜炎病理诊断中的应用[J]. 临床医药实践, 2022, 31(7):513-515.
[10]	Li Y, Xu S, Yu S, et al. Diagnosis of chronic endometritis: How many CD138+ cells/HPF in endometrial stroma affect pregnancy outcome of infertile women?[J]. Am J Reprod Immunol, 2021, 85(5):e13369. doi: 10.1111/aji.13369. doi: 10.1111/aji.13369
[11]	Chen YQ, Fang RL, Luo YN, et al. Analysis of the diagnostic value of CD138 for chronic endometritis, the risk factors for the pathogenesis of chronic endometritis and the effect of chronic endometritis on pregnancy: a cohort study[J]. BMC Womens Health, 2016, 16(1):60. doi: 10.1186/s12905-016-0341-3. doi: 10.1186/s12905-016-0341-3
[12]	Kasius JC, Broekmans FJ, Sie-Go DM, et al. The reliability of the histological diagnosis of endometritis in asymptomatic IVF cases: a multicenter observer study[J]. Hum Reprod, 2012, 27(1):153-158. doi: 10.1093/humrep/der341. doi: 10.1093/humrep/der341
[13]	McQueen DB, Perfetto CO, Hazard FK, et al. Pregnancy outcomes in women with chronic endometritis and recurrent pregnancy loss[J]. Fertil Steril, 2015, 104(4):927-931. doi: 10.1016/j.fertnstert.2015.06.044. doi: S0015-0282(15)00473-2 pmid: 26207958
[14]	Kitaya K, Tada Y, Taguchi S, et al. Local mononuclear cell infiltrates in infertile patients with endometrial macropolyps versus micropolyps[J]. Hum Reprod, 2012, 27(12):3474-3480. doi: 10.1093/humrep/des323. doi: 10.1093/humrep/des323
[15]	Parks RN, Kim CJ, Al-Safi ZA, et al. Multiple Myeloma 1 Transcription Factor Is Superior to CD138 as a Marker of Plasma Cells in Endometrium[J]. Int J Surg Pathol, 2019, 27(4):372-379. doi: 10.1177/1066896918814307. doi: 10.1177/1066896918814307 pmid: 30482071
[16]	Cicinelli E, Haimovich S, De Ziegler D, et al. MUM-1 immunohistochemistry has high accuracy and reliability in the diagnosis of chronic endometritis: a multi-centre comparative study with CD-138 immunostaining[J]. J Assist Reprod Genet, 2022, 39(1):219-226. doi: 10.1007/s10815-021-02356-1. doi: 10.1007/s10815-021-02356-1
[17]	Zeng S, Liu X, Liu D, et al. Research update for the immune microenvironment of chronic endometritis[J]. J Reprod Immunol, 2022, 152:103637. doi: 10.1016/j.jri.2022.103637. doi: 10.1016/j.jri.2022.103637
[18]	Ojosnegros S, Seriola A, Godeau AL, et al. Embryo implantation in the laboratory: an update on current techniques[J]. Hum Reprod Update, 2021, 27(3):501-530. doi: 10.1093/humupd/dmaa054. doi: 10.1093/humupd/dmaa054 pmid: 33410481
[19]	Santos ED, Moindjie H, Sérazin V, et al. Preimplantation factor modulates trophoblastic invasion throughout the decidualization of human endometrial stromal cells[J]. Reprod Biol Endocrinol, 2021, 19(1):96. doi: 10.1186/s12958-021-00774-5. doi: 10.1186/s12958-021-00774-5
[20]	Liu L, Yang H, Guo Y, et al. The impact of chronic endometritis on endometrial fibrosis and reproductive prognosis in patients with moderate and severe intrauterine adhesions: a prospective cohort study[J]. Fertil Steril, 2019, 111(5):1002-1010.e2. doi: 10.1016/j.fertnstert.2019.01.006. doi: S0015-0282(19)30013-5 pmid: 30922643
[21]	Fraser R, Smith R, Lin CJ. A 3D endometrial organotypic model simulating the acute inflammatory decidualisation initiation phase with epithelial induction of the key endometrial receptivity marker, integrin αVβ3[J]. Hum Reprod Open, 2021, 2021(4): hoab034. doi: 10.1093/hropen/hoab034. doi: 10.1093/hropen/hoab034
[22]	Xu Y, Mei J, Diao L, et al. Chronic endometritis and reproductive failure: Role of syndecan-1[J]. Am J Reprod Immunol, 2020, 84(3):e13255. doi: 10.1111/aji.13255. doi: 10.1111/aji.13255
[23]	Alecsandru D, Garcia Velasco JA. The excessive presence (percentage or number) of endometrial immune cells in patients with chronic endometritis cannot be associated with reduced endometrial receptivity or recurrent pregnancy failure[J]. Fertil Steril, 2020, 113(1):85-86. doi: 10.1016/j.fertnstert.2019.10.008. doi: S0015-0282(19)32478-1 pmid: 32033734
[24]	Kitazawa J, Kimura F, Nakamura A, et al. Alteration in endometrial helper T-cell subgroups in chronic endometritis[J]. Am J Reprod Immunol, 2021, 85(3):e13372. doi: 10.1111/aji.13372. doi: 10.1111/aji.13372
[25]	Von Woon E, Greer O, Shah N, et al. Number and function of uterine natural killer cells in recurrent miscarriage and implantation failure: a systematic review and meta-analysis[J]. Hum Reprod Update, 2022, 28(4):548-582. doi: 10.1093/humupd/dmac006. doi: 10.1093/humupd/dmac006 pmid: 35265977
[26]	Giuliani E, Parkin KL, Lessey BA, et al. Characterization of uterine NK cells in women with infertility or recurrent pregnancy loss and associated endometriosis[J]. Am J Reprod Immunol, 2014, 72(3):262-269. doi: 10.1111/aji.12259. doi: 10.1111/aji.12259
[27]	Li Y, Yu S, Huang C, et al. Evaluation of peripheral and uterine immune status of chronic endometritis in patients with recurrent reproductive failure[J]. Fertil Steril, 2020, 113(1):187-196.e1. doi: 10.1016/j.fertnstert.2019.09.001. doi: S0015-0282(19)32314-3 pmid: 31718829
[28]	Kushnir VA, Solouki S, Sarig-Meth T, et al. Systemic Inflammation and Autoimmunity in Women with Chronic Endometritis[J]. Am J Reprod Immunol, 2016, 75(6):672-677. doi: 10.1111/aji.12508. doi: 10.1111/aji.12508
[29]	Shin JS, Kim I, Moon JS, et al. Intranuclear Delivery of HIF-1α-TMD Alleviates EAE via Functional Conversion of TH17 Cells[J]. Front Immunol, 2021, 12:741938. doi: 10.3389/fimmu.2021.741938. doi: 10.3389/fimmu.2021.741938
[30]	Qin XY, Shen HH, Zhou WJ, et al. Insight of Autophagy in Spontaneous Miscarriage[J]. Int J Biol Sci, 2022, 18(3):1150-1170. doi: 10.7150/ijbs.68335. doi: 10.7150/ijbs.68335
[31]	Netea-Maier RT, Plantinga TS, van de Veerdonk FL, et al. Modulation of inflammation by autophagy: Consequences for human disease[J]. Autophagy, 2016, 12(2):245-260. doi: 10.1080/15548627.2015.1071759. doi: 10.1080/15548627.2015.1071759 pmid: 26222012
[32]	Ribeiro VR, Romao-Veiga M, Nunes PR, et al. Increase of autophagy marker p62 in the placenta from pregnant women with preeclampsia[J]. Hum Immunol, 2022, 83(5):447-452. doi: 10.1016/j.humimm.2022.02.005. doi: 10.1016/j.humimm.2022.02.005 pmid: 35210117
[33]	Wang WJ, Zhang H, Chen ZQ, et al. Endometrial TGF-β, IL-10, IL-17 and autophagy are dysregulated in women with recurrent implantation failure with chronic endometritis[J]. Reprod Biol Endocrinol, 2019, 17(1):2. doi: 10.1186/s12958-018-0444-9. doi: 10.1186/s12958-018-0444-9
[34]	Cicinelli E, Bettocchi S, de Ziegler D, et al. Chronic Endometritis, a Common Disease Hidden Behind Endometrial Polyps in Premenopausal Women: First Evidence From a Case-Control Study[J]. J Minim Invasive Gynecol, 2019, 26(7):1346-1350. doi: 10.1016/j.jmig.2019.01.012. doi: 10.1016/j.jmig.2019.01.012
[35]	Kuroda K, Takamizawa S, Motoyama H, et al. Analysis of the therapeutic effects of hysteroscopic polypectomy with and without doxycycline treatment on chronic endometritis with endometrial polyps[J]. Am J Reprod Immunol, 2021, 85(6):e13392. doi: 10.1111/aji.13392. doi: 10.1111/aji.13392
[36]	Freitag N, Pour SJ, Fehm TN, et al. Are uterine natural killer and plasma cells in infertility patients associated with endometriosis, repeated implantation failure, or recurrent pregnancy loss?[J]. Arch Gynecol Obstet, 2020, 302(6):1487-1494. doi: 10.1007/s00404-020-05679-z. doi: 10.1007/s00404-020-05679-z
[37]	Jiang I, Yong PJ, Allaire C, et al. Intricate Connections between the Microbiota and Endometriosis[J]. Int J Mol Sci, 2021, 22(11):5644. doi: 10.3390/ijms22115644. doi: 10.3390/ijms22115644
[38]	Holzer I, Ott J, Kurz C, et al. Is Chronic Endometritis Associated with Tubal Infertility? A Prospective Cohort Study[J]. J Minim Invasive Gynecol, 2021, 28(11):1876-1881. doi: 10.1016/j.jmig.2021.04.011. doi: 10.1016/j.jmig.2021.04.011
[39]	Xiao S, Wan Y, Xue M, et al. Etiology, treatment, and reproductive prognosis of women with moderate-to-severe intrauterine adhesions[J]. Int J Gynaecol Obstet, 2014, 125(2):121-124. doi: 10.1016/j.ijgo.2013.10.026. doi: 10.1016/j.ijgo.2013.10.026 pmid: 24598346
[40]	Cicinelli E, Matteo M, Tinelli R, et al. Prevalence of chronic endometritis in repeated unexplained implantation failure and the IVF success rate after antibiotic therapy[J]. Hum Reprod, 2015, 30(2):323-330. doi: 10.1093/humrep/deu292. doi: 10.1093/humrep/deu292
[41]	Johnston-MacAnanny EB, Hartnett J, Engmann LL, et al. Chronic endometritis is a frequent finding in women with recurrent implantation failure after in vitro fertilization[J]. Fertil Steril, 2010, 93(2):437-441. doi: 10.1016/j.fertnstert.2008.12.131. doi: 10.1016/j.fertnstert.2008.12.131 pmid: 19217098
[42]	Workowski KA, Bachmann LH, Chan PA, et al. Sexually Transmitted Infections Treatment Guidelines, 2021[J]. MMWR Recomm Rep, 2021, 70(4):1-187. doi: 10.15585/mmwr.rr7004a1. doi: 10.15585/mmwr.rr7004a1 pmid: 34292926
[43]	赵静, 黄国宁, 孙海翔, 等. 辅助生殖技术中异常子宫内膜诊疗的中国专家共识[J]. 生殖医学杂志, 2018, 27(11):1057-1064. doi: 10.3969/j.issn.1004-3845.2018.11.003. doi: 10.3969/j.issn.1004-3845.2018.11.003
[44]	Zhang Y, Xu H, Liu Y, et al. Confirmation of chronic endometritis in repeated implantation failure and success outcome in IVF-ET after intrauterine delivery of the combined administration of antibiotic and dexamethasone[J]. Am J Reprod Immunol, 2019, 82(5):e13177. doi: 10.1111/aji.13177. doi: 10.1111/aji.13177
[45]	Molina NM, Sola-Leyva A, Saez-Lara MJ, et al. New Opportunities for Endometrial Health by Modifying Uterine Microbial Composition: Present or Future?[J]. Biomolecules, 2020, 10(4):593. doi: 10.3390/biom10040593. doi: 10.3390/biom10040593
[46]	Hashem NM, Gonzalez-Bulnes A. The Use of Probiotics for Management and Improvement of Reproductive Eubiosis and Function[J]. Nutrients, 2022, 14(4):902. doi: 10.3390/nu14040902. doi: 10.3390/nu14040902