Chronic endometritis in groupe of a women of fertile age with infertility and uterine surgery
DOI:
https://doi.org/10.15574/HW.2025.3(178).2833Keywords:
chronic endometritis, assisted reproductive technologies, gynecological surgical interventions, decidualization pathology, placentation disordersAbstract
Chronic endometritis (CE) is known to have a negative impact on decidualization, and therefore is the cause of implantation failure, miscarriage and placentation disorders with the formation of both placental insufficiency and pathological placental invasion.
Aim - to determine the frequency of CE in women of childbearing age without a history of cesarean section (CS), with infertility requiring the use of assisted reproductive technologies (IVF) or uterine surgery, who are planning pregnancy in the short term.
Materials and methods. The study included 309 women of childbearing age, who were divided into 2 groups: the first - 152 women with IVF and without a history of CS; the second - 157 women of childbearing age without a history of CS, who underwent elective uterine surgery. The control group was 54 women without ART and uterine surgery in history, who applied for a scheduled examination. The presence of HE was established when 5 or more plasma cells were found in the endometrial stroma, determining the specific marker of plasma cells - CD138 by immunohistochemical method. Endometrial tissue samples were taken by Pipelle biopsy using a device (Pipelle de Cornier, CCD).
Results. According to the results of the study, HE was detected in 79 (52.0%) women of the first, 73 (46.5%) of the second and in 2 (3.7%) of the control group.
Conclusions. The results of the study showed that in the groups of women with IVF and gynecological surgical interventions on the uterus, a high frequency of HE was observed (52% and 46.5%, respectively), which suggests that HE may be one of the factors contributing to the development of placental disorders. However, further studies are necessary to confirm this hypothesis.
The study was conducted in accordance with the principles of the Declaration of Helsinki. The study protocol was approved by the local ethics committee of the participating institution. Informed consent of the patients was obtained for the study.
The authors declare that there is no conflict of interest.
References
Avagliano L, Massa V, Bulfamante GP. (2016). Histology of Human Placenta: 1-16.
Bayer-Garner IB, Nickell JA, Korourian S. (2004). Routine syndecan-1 immunohistochemistry aids in the diagnosis of chronic endometritis. Arch Pathol Lab Med. 128: 1000-1003. https://doi.org/10.5858/2004-128-1000-RSIAIT; PMid:15335255
Carvalho FM, Aguiar FN, Tomioka R, de Oliveira RM, Frantz N, Ueno J. (2013). Functional endometrial polyps in infertile asymptomatic patients: a possible evolution of vascular changes secondary to endometritis. Eur J Obstet Gynecol Reprod Biol. 170: 152-156. https://doi.org/10.1016/j.ejogrb.2013.05.012; PMid:23773528
Chen YQ, Fang RL, Luo YN, Luo CQ. (2016). 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. BMC Womens Health. 16: 60. https://doi.org/10.1186/s12905-016-0341-3; PMid:27596852 PMCid:PMC5477816
Cicinelli E, Haimovich S, De Ziegler D, Raz N, Ben-Tzur D, Andrisani A et al. (2022). MUM-1 immunohistochemistry has high accuracy and reliability in the diagnosis of chronic endometritis: a multi-centre comparative study with CD-138 immunostaining. J Assist Reprod Genet. 39: 219-226. https://doi.org/10.1007/s10815-021-02356-1; PMid:34791588 PMCid:PMC8866577
Cicinelli E, Matteo M, Tinelli R, Lepera A, Alfonso R, Indraccolo U et al. (2015). Prevalence of chronic endometritis in repeated unexplained implantation failure and the IVF success rate after antibiotic therapy. Hum Reprod. 30: 323-330. https://doi.org/10.1093/humrep/deu292; PMid:25385744
Cicinelli E, Resta L, Nicoletti R, Tartagni M, Marinaccio M et al. (2005). Detection of chronic endometritis at fluid hysteroscopy. J Minim Invasive Gynecol. 12(6): 514-518. https://doi.org/10.1016/j.jmig.2005.07.394; PMid:16337579
Cicinelli E, Vitagliano A, Loizzi V, De Ziegler D, Fanelli M, Bettocchi S et al. (2021). Altered gene expression encoding cytochines, grow factors and cell cycle regulators in the endometrium of women with chronic endometritis. Diagnostics (Basel). 11(3): 471. https://doi.org/10.3390/diagnostics11030471; PMid:33800186 PMCid:PMC7999985
Conrad KP, Rabaglino MB, Post Uiterweer ED. (2017). Emerging role for dysregulated decidualization in the genesis of preeclampsia. Placenta. 60: 119‐129. https://doi.org/10.1016/j.placenta.2017.06.005; PMid:28693893 PMCid:PMC5718949
Crocetto F, Saccone G, Raffone A et al. (2021). Urinary incontinence after planned cesarean hysterectomy for placenta accreta. Urol Int. 105(11-12): 1099-1103. https://doi.org/10.1159/000518114; PMid:34515253
Crum CP, Egawa K, Fenoglio CM, Richart RM. (1983). Chronic endometritis: the role of immunohistochemistry in the detection of plasma cells. Am J Obstetr Gynecol. 147: 812-815. doi: https://doi.org/10.1016/0002-9378(83)90045-5; PMid:6359886
Elder S, Bortoletto P, Romanski PA, Spandorfer S. (2021). Chronic endometritis in women with suspected retained products of conception and their reproductive outcomes. Am J Reprod Immunol. 86: e13410. https://doi.org/10.1111/aji.13410; PMid:33644899
Fan D, Wu S, Liu LI et al. (2017). Prevalence of antepartum hemorrhage in women with placenta previa: a systematic review and meta-analysis. Sci Rep. 7: 40320. https://doi.org/10.1038/srep40320; PMid:28067303 PMCid:PMC5220286
Faraji A, Akbarzadeh-Jahromi M, Bahrami S, Gharamani S, Raeisi Shahraki H, Kasraeian M et al. (2022). Predictive value of vascular endothelial growth factor and placenta growth factor for placenta accreta spectrum. J. Obstet.Gynaecol. 42: 900-905. https://doi.org/10.1080/01443615.2021.1955337; PMid:34558384
Gay C, Hamdaoui N, Pauly V, Rojat Habib M-C, Djemli A, Carmassi M et al. (2021). Impact of antibiotic treatment for chronic endometritis on unexplained recurrent pregnancy loss. J Gynecol Obstetr Hum Reprod. 50: 102034. https://doi.org/10.1016/j.jogoh.2020.102034; PMid:33307243
Gerevich NV, Gychka SG, Vapelnyk SM, Bilyi VI, Govsieiev DO. (2025). Some aspects of the pathogenesis of placenta accreta spectrum (PAS): pathohistology, molecular mechanisms and biomarkers (literature review). Ukrainian Journal Health of Woman. 1(176): 83-98. https://doi.org/10.15574/HW.2025.1(176).8398
Gerevich NV, Vapelnyk SM, Govsieiev DO. (2025). Current structure of risk factors for abnormal invasion (PAS) and placenta previa in Ukraine. Ukrainian Journal of Perinatology and Pediatrics. 2(102): 13-18. https://doi.org/10.15574/PP.2025.2(102).1318
Greenwood SM, Moran JJ. (1981). Chronic endometritis: morphologic and clinical observations. Obstet Gynecol. 58(2): 176-184.
Guo GL, Chen SY, Zhang W, Zhang C, He L. (2013). Diagnosis value of hysteroscopy for chronic endometritis. Clin Exp Obstet Gynecol. 40(2): 250-252.
Herraiz I, Llurba E, Verlohren S, Galindo A. (2018). Update on the diagnosis and prognosis of preeclampsia with the aid of the sFlt-1/PlGF ratio in singleton pregnancies. Fetal Diagn. Ther. 43(2): 81-89. https://doi.org/10.1159/000477903; PMid:28719896
Inki P, Joensuu H, Grenman R, Klemi P, Jalkanen M. (1994). Association between syndecan-1 expression and clinical outcomes in squamous cell carcinoma of the head and neck. Br J Cancer. 70: 319-323. https://doi.org/10.1038/bjc.1994.300; PMid:8054282 PMCid:PMC2033500
Johnston-MacAnanny EB, Hartnett J, Engmann LL, Nulsen JC, Sanders MM, Benadiva CA. (2010). Chronic endometritis is a frequent finding in women with recurrent implantation failure after in vitro fertilization. Fertil Steril. 93: 437-441. https://doi.org/10.1016/j.fertnstert.2008.12.131; PMid:19217098
Kayem G, Seco A, Beucher G et al. (2021). Clinical profiles of placenta accreta spectrum: the PACCRETA population-based study. Bjog. 128(10): 1646-1655. doi: 10.1111/1471-0528.16647. https://doi.org/10.1111/1471-0528.16647; PMid:33393174
Kimura F, Takebayashi A, Ishida M, Nakamura A, Kitazawa J, Morimune A et al. (2019, May). Review: Chronic endometritis and its effect on reproduction. J Obstet Gynaecol Res. 45(5): 951-960. Epub 2019 Mar 6. https://doi.org/10.1111/jog.13937 PMid:30843321
Kitaya K, Matsubayashi H, Takaya Y, Nishiyama R, Yamaguchi K, Takeuchi T et al. (2017). Live birth rate following oral antibiotic treatment for chronic endometritis in infertile women with repeated implantation failure. Am J Reprod Immunol. 78: e12719. https://doi.org/10.1111/aji.12719; PMid:28608596
Kong X, Kong Y, Yan J, Hu JJ, Wang FF, Zhang L. (2017). On opportunity for emergency cesarean hysterectomy and pregnancy outcomes of patients with placenta accreta. Medicine. 96(39): e7930. https://doi.org/10.1097/MD.0000000000007930; PMid:28953615 PMCid:PMC5626258
Kuroda K, Horikawa T, Moriyama A, Nakao K, Juen H, Takamizawa S et al. (2020). Impact of chronic endometritis on endometrial receptivity analysis results and pregnancy outcomes. Immun Inflamm Dis. 8: 650-658. https://doi.org/10.1002/iid3.354; PMid:32969185 PMCid:PMC7654412
Kuroda K, Venkatakrishnan R, James S et al. (2013). Elevated periimplantation uterine natural killer cell density in human endometrium is associated with impaired corticosteroid signaling in decidualizing stromal cells. J Clin Endocrinol Metab. 98: 4429‐4437. https://doi.org/10.1210/jc.2013-1977; PMid:24025400 PMCid:PMC4207949
Li Y, Xu S, Yu S, Huang C, Lin S, Chen W et al. (2021). Diagnosis of chronic endometritis: How many CD138(+) cells/HPF in endometrial stroma affect pregnancy outcome of infertile women? Am J Reprod Immunol. 85: e13369. https://doi.org/10.1111/aji.13369; PMid:33152123
Lumbanraja S, Yaznil MR, Siahaan AM, Berry Eka Parda B. (2022). Soluble FMS-Like Tyrosine Kinase-1: Role in placenta accrete spectrum disorder. F1000Research. 10: 618. https://doi.org/10.12688/f1000research.54719.4; PMid:36127888 PMCid:PMC9478500
Martinelli KG, Garcia EM, Santos Neto ETD, Gama S. (2018). Advanced maternal age and its association with placenta praevia and placental abruption: a meta-analysis. Cad Saude Publica. 34: e00206116. https://doi.org/10.1590/0102-311x00206116; PMid:29489954
McQueen DB, Bernardi LA, Stephenson MD. (2014). Chronic endometritis in women with recurrent early pregnancy loss and/or fetal demise. Fertil Steril. 101: 1026-1030. https://doi.org/10.1016/j.fertnstert.2013.12.031; PMid:24462055
McQueen DB, Perfetto CO, Hazard FK, Lathi RB. (2015). Pregnancy outcomes in women with chronic endometritis and recurrent pregnancy loss. Fertil Steril. 104: 927-931. https://doi.org/10.1016/j.fertnstert.2015.06.044; PMid:26207958
Michels TC. (1995). Chronic endometritis. Am Fam Physician. 52(1): 217-222.
Nijkang NP, Anderson L, Markham R, Manconi F. (2019). Endometrial polyps: pathogenesis, sequelae and treatment. SAGE Open Med. 7: 2050312119848247. https://doi.org/10.1177/2050312119848247; PMid:31105939 PMCid:PMC6501471
Rathbun KM, Hildebrand JP. (2018). Placenta abnormalities. In: StatPearls. Treasure Island (FL): StatPearls Publishing.
Romundstad LB, Romundstad PR, Sunde A, von During V, Skjaerven R, Vatten LJ. (2006). Increased risk of placenta previa in pregnancies following IVF/ICSI; a comparison of ART and non-ART pregnancies in the same mother. Hum Reprod. 21: 2353-2358. https://doi.org/10.1093/humrep/del153; PMid:16728419
Rosenberg T, Pariente G, Sergienko R, Wiznitzer A, Sheiner E. (2011). Critical analysis of risk factors and outcome of placenta previa. Arch Gynecol Obstet. 284: 47-51. https://doi.org/10.1007/s00404-010-1598-7; PMid:20652281
Salker M, Teklenburg G, Molokhia M et al. (2010). Natural selection of human embryos: impaired decidualization of endometrium disables embryo‐maternal interactions and causes recurrent pregnancy loss. PLOS One. 5: e10287. https://doi.org/10.1371/journal.pone.0010287; PMid:20422017 PMCid:PMC2858209
Silver RM. (2015). Abnormal placentation: placenta previa, vasa previa, and placenta accreta. Obstet Gynecol. 126: 654-668. https://doi.org/10.1097/AOG.0000000000001005; PMid:26244528
Song D, He Y, Wang Y, Liu Z, Xia E, Huang X et al. (2021). Impact of antibiotic therapy on the rate of negative test results for chronic endometritis: a prospective randomized control trial. Fertil Steril. 115: 1549-1556. doi: https://doi.org/10.1016/j.fertnstert.2020.12.019; PMid:33549312
Song D, Li TC, Zhang Y, Feng X, Xia E, Huang X et al. (2019). Correlation between hysteroscopy findings and chronic endometritis. Fertil Steril. 111: 772-779. https://doi.org/10.1016/j.fertnstert.2018.12.007; PMid:30683588
Weimar CHE, Kavelaars A, Brosens JJ et al. (2012). Endometrial stromal cells of women with recurrent miscarriage fail to discriminate between high‐and low‐quality human embryos. PLOS One. 7: e41424. https://doi.org/10.1371/journal.pone.0041424; PMid:22848492 PMCid:PMC3405140
Wiesenfeld HC, Hillier SL, Meyin LA, Amortegui AJ, Sweet RL. (2012). Subclinical pelvic inflammatory disease and infertility. Obstet Gynecol. 120(1): 37-43. https://doi.org/10.1097/AOG.0b013e31825a6bc9; PMid:22678036
Wu D, Kimura F, Zheng L, Ishida M, Niwa Y, Hirata K et al. (2017, Mar 4). Chronic endometritis modifies decidualization in human endometrial stromal cells. Reprod Biol Endocrinol. 15(1): 16. doi: https://doi.org/10.1186/s12958-017-0233-x; PMid:28259137 PMCid:PMC5336610
Xiong Y, Chen Q, Chen C, Tan J, Wang Z et al. (2021, Aug). Impact of oral antibiotic treatment for chronic endometritis on pregnancy outcomes in the following frozen-thawed embryo transfer cycles of infertile women: a cohort study of 640 embryo transfer cycles. Fertil Steril.;116(2):413-421. Epub 2021 Apr 26. https://doi.org/10.1016/j.fertnstert.2021.03.036
PMid:33926717
Yang R, Du X, Wang Y, Song X, Yang Y, Qiao J. (2014). The hysteroscopy and histological diagnosis and treatment value of chronic endometritis in recurrent implantation failure patients. Arch Gynecol Obstetr. 289: 1363-1369. https://doi.org/10.1007/s00404-013-3131-2; PMid:24395012
Zhang Y, Xu H, Liu Y, Zheng S, Zhao W, Wu D et al. (2019). Confirmation of chronic endometritis in repeated implantation failure and success outcome in IVFET after intrauterine delivery of the combined administration of antibiotic and dexamethasone. Am J Reprod Immunol. 82: e13177. https://doi.org/10.1111/aji.13177; PMid:31373128
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