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Impact of chronic endometritis in infertility: a SWOT analysis

Published:February 11, 2021DOI:https://doi.org/10.1016/j.rbmo.2021.02.003

      Abstract

      Chronic endometritis is a pathology often associated with reproductive failure, but there are still no clear recommendations on whether its inclusion in the initial study of infertile couples is necessary. In this discussion paper, based on a SWOT (Strengths, Weaknesses, Opportunities, Threats) analysis, the different aspects of the repercussions of chronic endometritis in fertility are evaluated. To avoid possible subjectivity in the analysis and results of this study, the researchers followed the Oxford criteria for the evaluation of evidence. The results from the evaluation of the reviewed literature seem to indicate that, pending new evidence, it would be advisable not to include chronic endometritis in the initial baseline study before assisted reproduction in order not to delay other assisted reproduction treatments. However, it would be advisable in cases of repetitive implantation failure and pregnancy loss after having undergone IVF with viable embryos and before continuing with costly reproductive processes, since results could be improved. The development of randomized studies assessing the impact of antibiotic treatment as a possible therapeutic option in infertile women with chronic endometritis, as well as the possible impact on endometrial microbiota and receptivity/implantation, would allow for the establishment of more precise clinical guidelines in this regard.

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      REFERENCES

        • Adegboyega P.A.
        • Pei Y.
        • McLarty J.
        Relationship between eosinophils and chronic endometritis.
        Hum. Pathol. 2010; 41: 33-37
        • Akopians A.L.
        • Pisarska M.D.
        • Wang E.T.
        The role of inflammatory pathways in implantation failure: chronic endometritis and hydrosalpinges.
        Semin. Reprod. Med. 2015; 33: 298-304
        • Baker J.M.
        • Chase D.M.
        • Herbst-Kralovetz M.M.
        Uterine Microbiota: Residents, Tourists, or Invaders?.
        Front. Immunol. 2018; 9: 208
        • Bayer-Garner I.B.
        • Korourian S.
        Plasma cells in chronic endometritis are easily identified when stained with syndecan-1.
        Mod. Pathol. 2001; 14: 877-889
        • Bayer-Garner I.B.
        • Nickell J.A.
        • Korourian S.
        Routine syndecan-1 immunohistochemistry aids in the diagnosis of chronic endometritis.
        Arch. Pathol. Lab. Med. 2004; 128: 1000-1003
        • Bellver J.
        • Bosch E.
        • Espinós J.J.
        • Fabregues F.
        • Fontes J.
        • García-Velasco J.
        • Llácer J.
        • Requena A.
        • Checa M.A.
        • Spanish Infertility SWOT Group (SISG)
        Second-generation preimplantation genetic testing for aneuploidy in assisted reproduction: a SWOT analysis.
        Reprod. Biomed. Online. 2019; 39: 905-915
        • Bellver J.
        • Simón C.
        Implantation failure of endometrial origin: what is new?.
        Curr. Opin. Obstet. Gynecol. 2018; 30: 229-236
        • Benner M.
        • Ferwerda G.
        • Joosten I.
        • van der Molen R.G.
        How uterine microbiota might be responsible for a receptive, fertile endometrium.
        Hum. Reprod. Update. 2018; 24: 393-415
        • Blockeel C.
        • Drakopoulos P.
        • Santos-Ribeiro S.
        • Polyzos N.P.
        • Tournaye H.
        A fresh look at the freeze-all protocol: a SWOT analysis.
        Hum. Reprod. 2016; 31: 491-497
        • Bosch E.
        • Espinós J.J.
        • Fabregues F.
        • Fontes J.
        • García-Velasco J.
        • Llácer J.
        • Requena A.
        • Checa M.A.
        • Bellver J.
        • on behalf of the Spanish Infertility SWOT Group (SISG)
        Always ICSI? A SWOT analysis.
        J. Assist. Reprod. Genet. 2020; (https://doi.org/)https://doi.org/10.1007/s10815-020-01836-0
        • Bouet P.E.
        • El Hachem H.
        • Monceau E.
        • Gariépy G.
        • Kadoch I.J.
        • Sylvestre C.
        Chronic endometritis in women with recurrent pregnancy loss and recurrent implantation failure: Prevalence and role of office hysteroscopy and immunohistochemistry in diagnosis.
        Fertil. Steril. 2016; 105: 106-110
        • Bradshaw C.S.
        • Morton A.N.
        • Hocking J.
        High recurrence rates of bacterial vaginosis over the course of 12 months after oral metronidazole therapy and factors associated with recurrence.
        J. Infect. Dis. 2006; 193: 1478-1486
        • Burney R.O.
        • Talbi S.
        • Hamilton A.E.
        • Vo K.C.
        • Nyegaard M.
        • Nezhat C.R.
        • Lessey B.A.
        • Giudice L.C.
        Gene expression analysis of endometrium reveals progesterone resistance and candidate susceptibility genes in women with endometriosis.
        Endocrinology. 2007; 148: 3814-3826
        • Checa M.A.
        • Bellver J.
        • Bosch E.
        • Espinós J.J.
        • Fabregues F.
        • Fontes J.
        • García-Velasco J.
        • Requena A.
        • Spanish Infertility SWOT Group (SISG)
        Hysteroscopic septum resection and reproductive medicine: A SWOT analysis.
        Reprod. Biomed. Online. 2018; 37: 709-715
        • Chen C.
        • Song X.
        • Wei W.
        • Zhong H.
        • Dai J.
        • Lan Z.
        • Li F.
        • Yu X.
        • Feng Q.
        • Wang Z.
        • Xie H.
        • Chen X.
        • Zeng C.
        • Wen B.
        • Zeng L.
        • Du H.
        • Tang H.
        • Xu C.
        • Xia Y.
        • Xia H.
        • Yang H.
        • Wang J.
        • Wang J.
        • Madsen L.
        • Brix S.
        • Kristiansen K.
        • Xu X.
        • Li J.
        • Wu R.
        • Jia H.
        The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases.
        Nat. Commun. 2017; 8: 875
        • Chen Y.
        • Liu L.
        • Luo Y.
        • Chen M.
        • Huan Y.
        • Fang R.
        Prevalence and Impact of Chronic Endometritis in Patients With Intrauterine Adhesions: A Prospective Cohort Study.
        J. Minim. Invasive Gynecol. 2017; 24: 74-79
        • Cicinelli E.
        • De Ziegler D.
        • Nicoletti R.
        • Tinelli R.
        • Saliani N.
        • Resta L.
        Poor reliability of vaginal and endocervical cultures for evaluating microbiology of endometrial cavity in women with chronic endometritis.
        Gynecol. Obstet. Invest. 2009; 68: 108-115
        • Cicinelli E.
        • Matteo M.
        • Tinelli R.
        • Lepera A.
        • Alfonso R.
        • Indraccolo U.
        Prevalence of chronic endometritis in repeated unexplained implantation failure and the IVF success rate after antibiotic therapy.
        Hum. Reprod. 2015; 30: 323-330
        • Cicinelli E.
        • Matteo M.
        • Tinelli R.
        • Pinto V.
        • Marinaccio M.
        • Indraccolo U.
        • De Ziegler D.
        • Resta L.
        Chronic endometritis due to common bacteria is prevalent in women with recurrent miscarriage as confirmed by improved pregnancy outcome after antibiotic treatment.
        Reprod. Sci. 2014; 21: 640-647
        • Cicinelli E.
        • Matteo M.
        • Trojano G.
        • Mitola P.C.
        • Tinelli R.
        • Vitagliano A.
        • Crupano F.M.
        • Lepera A.
        • Miragliotta G.
        • Resta L.
        Chronic endometritis in patients with unexplained infertility: Prevalence and effects of antibiotic treatment on spontaneous conception.
        Am. J. Reprod. Immunol. 2018; 79: e12782
        • Cicinelli E.
        • Resta L.
        • Nicoletti R.
        • Tartagni M.
        • Marinaccio M.
        • Bulletti C.
        • Colafiglio G.
        Detection of chronic endometritis at fluid hysteroscopy.
        J. Minim. Invasive Gynecol. 2005; 12: 514-518
        • Cicinelli E.
        • Tinelli R.
        • Colafiglio G.
        • Pastore A.
        • Mastrolia S.
        • Lepera A.
        • Clevin L.
        Reliability of narrow-band imaging (NBI) hysteroscopy: a comparative study.
        Fertil. Steril. 2010; 94: 2303-2307
        • Cicinelli E.
        • Vitagliano A.
        • Kumar A.
        • Lasmar R.B.
        • Bettocchi S.
        • Haimovich S
        • International Working Group for Standardization of Chronic Endometritis Diagnosis
        Unified diagnostic criteria for chronic endometritis at fluid hysteroscopy: proposal and reliability evaluation through an international randomized-controlled observer study.
        Fertil. Steril. 2019; 112 (162-173.e2)
        • Coughlan C.
        • Ledger W.
        • Wang Q.
        • Liu F.
        • Demirol A.
        • Gurgan T.
        • Cutting R.
        • Ong K.
        • Sallam H.
        • Li TC.
        Recurrent implantation failure: definition and management.
        Reprod. Biomed. Online. 2014; 28: 14-38
        • Crum C.P.
        • Egawa K.
        • Fenoglio C.M.
        • Richart R.M.
        Chronic endometritis: the role of immunohistochemistry in the detection of plasma cells.
        Am. J. Obstet. Gynecol. 1983; 147: 812-815
        • De Ziegler D.
        • Pirtea P.
        • Ayoubi J.M.
        Inflammation and uterine fibrosis: the possible role of chronic endometritis.
        Fertil. Steril. 2019; 111: 890-891
        • Di Pietro C.
        • Cicinelli E.
        • Guglielmino M.R.
        • Ragusa M.
        • Farina M.
        • Palumbo MA
        Altered transcriptional regulation of cytokines, growth factors and apoptotic proteins in the endometrium of infertile women with chronic endometritis.
        Am. J. Reprod. Immunol. 2013; 69: 509-517
        • Di Pietro C.
        • Caruso S.
        • Battaglia R.
        • Iraci M.
        • La Ferlita A.
        • Strino F.
        • Bonaventura G.
        • Di Mauro M.
        • Barcellona M.L.
        • Perciavalle V.
        • Purrello M.
        • Cianci A.
        MiR-27a-3pand miR-124 3p, upregulated in endometrium and serum from women affected by Chronic Endometritis, are new potential molecular markers of endometrial receptivity.
        Am. J. Reprod. Immunol. 2018; 80: e12858
        • Du. J.
        • Li Y.
        • Lv S.
        • Wang Q.
        • Sun C.
        • Dong X.
        • He M.
        • Ulain Q.
        • Yuan Y.
        • Tuo X.
        • Batchu N.
        • Song Q.
        • Li Q.
        Endometrial sampling devices for early diagnosis of endometrial lesions.
        J. Cancer Res. Clin. Oncol. 2016; 142: 2515-2522
        • Eckert L.O.
        • Hawes S.E.
        • Wolner-Hanssen P.K.
        • Kiviat N.B.
        • Wasserheit J.N.
        • Paavonen J.A.
        Endometritis: the clinical-pathologic syndrome.
        Am. J. Obstet. Gynecol. 2002; 186: 690-695
        • Eckert L.O.
        • Moore D.E.
        • Patton D.L.
        • Agnew K.J.
        • Eschenbach D.A.
        Relationship of vaginal bacteria and inflammation with conception and early pregnancy loss following in-vitro fertilization.
        Infect. Dis. Obstet. Gynecol. 2003; 11: 11-17
        • El-Toukhy T.
        • Campo R.
        • Khalaf Y.
        • Tabanelli C.
        • Gianaroli L.
        • Gordts S.S.
        • Gordts S.
        • Mestdagh G.
        • Mardesic T.
        • Voboril J.
        • Marchino G.L.
        • Benedetto C.
        • Al-Shawaf T.
        • Sabatini L.
        • Seed P.T.
        • Gergolet M.
        • Grimbizis G.
        • Harb H.
        • Coomarasamy A.
        Hysteroscopy in recurrent in-vitro fertilisation failure (TROPHY): a multicentre, randomised controlled trial.
        Lancet. 2016; 387: 2614-2621
        • Engmann L.
        • Benadiva C.
        • Humaidan P.
        GnRH agonist trigger for the induction of oocyte maturation in GnRH antagonist IVF cycles: a SWOT analysis.
        Reprod. Biomed. Online. 2016; 32: 274-285
        • Esteves S.C.
        • Agarwal A.
        • Cho C.L.
        • Majzoub A.
        A Strengths-Weaknesses-Opportunities-Threats (SWOT) analysis on the clinical utility of sperm DNA fragmentation testing in specific male infertility scenarios.
        Transl. Androl. Urol. 2017; 6: S734-S760
        • Fatemi H.M.
        • Popovic-Todorovic B.
        • Ameryckx L.
        • Bourgain C.
        • Fauser B.
        • Devroey P.
        In vitro fertilization pregnancy in a patient with proven chronic endometritis.
        Fertil. Steril. 2009; 91 (1293.e9-11)
        • Franasiak J.M.
        • Werner M.D.
        • Juneau C.R.
        • Tao X.
        • Landis J.
        • Zhan Y.
        Endometrial microbiome at the time of embryo transfer: next-generation sequencing of the 16S ribosomal subunit.
        J. Assist. Reprod. Genet. 2016; 33: 129-136
        • Frank T.S.
        • Himebaugh K.S.
        • Wilson M.D.
        Granulomatous endometritis associated with histologically occult cytomegalovirus in a healthy patient.
        Am. J. Surg. Pathol. 1992; 16: 716-720
        • Gilmore H.
        • Fleischhacker D.
        • Hecht J.L.
        Diagnosis of chronic endometritis in biopsies with stromal breakdown.
        Human Pathol. 2007; 38: 581-584
        • Greenwood S.M.
        • Moran J.J.
        Chronic endometritis: Morphologic and clinical observations.
        Obstet. Gynecol. 1981; 58: 176-184
        • Haggerty C.L.
        • Hillier S.L.
        • Bass D.C.
        • Ness R.B.
        PID Evaluation and Clinical Health study investigators: bacterial vaginosis and anaerobic bacteria are associated with endometritis.
        Clin. Infect. Dis. 2004; 39: 990-995
        • Inki P.
        Expression of syndecan-1 in female reproductive tract tissues and cultured keratinocytes.
        Mol. Hum. Reprod. 1997; 3: 299-305
        • Johnstone F.D.
        • Williams A.R.
        • Bird G.A.
        • Bjornsson S.
        Immunohistochemical characterization of endometrial lymphoid cell populations in women infected with human immunodeficiency virus.
        Obstet. Gynecol. 1994; 83: 586-593
        • Johnston-MacAnanny E.B.
        • Hartnett J.
        • Engmann L.L.
        • Nulsen J.C.
        • Sanders M.M.
        • Benadiva C.A.
        Chronic endometritis is a frequent finding in women with recurrent implantation failure after in vitro fertilization.
        Fertil. Steril. 2010; 93: 437-441
        • Kaku S.
        • Kubo T.
        • Kimura A.
        • Kitazawa J.
        • Morimune A.
        • Takahashi A.
        • Takebayashi A.
        • Takashima A.
        • Kushima R.
        • Murakami T.
        Relationship of chronic endometritis with chronic deciduitis in cases of miscarriage.
        BMC Women´s Health. 2020; 20: 114
        • Kasius J.C.
        • Broekmans F.J.
        • Sie-Go D.M.
        • Bourgain C.
        • Eijkemans M.J.
        • Fauser B.C.
        • Devroey P.
        • Fatemi H.M.
        The reliability of the histological diagnosis of endometritis in asymptomatic IVF cases: a multicenter observer study.
        Human Reproduction. 2012; 27: 153-158
        • Kasius J.C.
        • Fatemi H.M.
        • Bourgain C.
        The impact of chronic endometritis on reproductive outcome.
        Fertil. Steril. 2011; 96: 1451-1456
        • Kitaya K.
        • Matsubayashi H.
        • Takaya Y.
        • Nishiyama R.
        • Yamaguchi K.
        • Takeuchi T.
        • Ishikawa T.
        Live birth rate following oral antibiotic treatment for chronic endometritis in infertile women with repeated implantation failure.
        Am. J. Reprod. Immunol. 2017; 78: e12719
        • Kitaya K.
        • Matsubayashi H.
        • Yamaguchi K.
        • Nishiyama R.
        • Takaya Y.
        • Ishikawa T.
        • Yasuo T.
        • Yamada H.
        Chronic endometritis: potential cause of infertility and obstetric and neonatal complications.
        Am. J. Reprod. Immunol. 2015; 75: 13-22
        • Kitaya K.
        • Tada Y.
        • Hayashi T.
        • Taguchi S.
        • Funabiki M.
        • Nakamura Y.
        Comprehensive endometrial immunoglobulin subclass analysis in infertile women suffering from repeated implantation failure with or without chronic endometritis.
        Am. J. Reprod. Immunol. 2014; 72: 386-391
        • Kitaya K.
        • Takeuchi T.
        • Mizuta S.
        • Matsubayashi H.
        • Ishikawa T.
        Endometritis: new time, new concepts.
        Fertil. Steril. 2018; 110: 344-350
        • Kitaya K.
        • Yasuo T.
        Aberrant expression of selectin E, CXCL1, and CXCL13 in chronic endometritis.
        Mod. Pathol. 2010; 23: 1136-1146
        • Kitaya K.
        • Yasuo T.
        Inter-observer and intra-observer variability in immunohistochemical detection of endometrial stromal plasmacytes in chronic endometritis.
        Exp. Ther. Med. 2013; 5: 485-488
        • Kitaya K.
        Prevalence of chronic endometritis in recurrent miscarriages.
        Fertil. Steril. 2011; 95: 1156-1158
        • Kovaleva Y.V.
        The application of low-frequency ultrasound for the comprehensive treatment and rehabilitation of the patients presenting with chronic endometritis.
        Vopr Kurortol Fizioter Lech Fiz Kult. 2017; 94: 32-38
        • Kuroda K.
        • Horikawa T.
        • Moriyama
        • Nakao K.
        • Juen H.
        • Takamizawa S.
        • Ojiro Y.
        • Nakagawa K.
        • Sugiyama R.
        Impact of chronic endometritis on endometrial receptivity analysis results and pregnancy outcomes.
        Immun. Inflamm. Dis. 2020; : 651-657
        • Kushnir V.A.
        • Solouki S.
        • Sarig-Meth T.
        • Vega M.G.
        • Albertini D.F.
        • Darmon S.K.
        Systemic inflammation and autoimmunity in women with chronic endometritis.
        Am. J. Reprod. Immunol. 2016; 75: 672-677
        • Laurence M.
        • Hatzis C.
        • Brash D.E.
        Common Contaminants in Next-Generation Sequencing that Hinder Discovery of Low-Abundance Microbes.
        PLoS ONE. 2014; 9 (e97876*)
        • Liu H.
        • Wang J.
        • Wang H.
        • Tang N.
        • Li Y.
        • Zhang Y.
        • Hao T.
        The plasma and peritoneal fluid concentrations of matrix metalloproteinase-9 are elevated in patients with endometriosis.
        Ann. Clin. Biochem. 2016; 53: 599-605
        • Liu L.
        • Yang H.
        • Guo Y.
        • Yang G.
        • Chen Y.
        The impact of chronic endometritis on endometrial fibrosis and reproductive prognosis in patients with moderate and severe intrauterine adhesions: a prospective cohort study.
        Fertil. Steril. 2019; 111: 1002-1010
        • Liu Y.
        • Chen X.
        • Huang J.
        • Wang C.C.
        • Yu M.Y.
        • Laird S.
        • Li T.C.
        Comparison of the prevalence of chronic endometritis as determined by means of different diagnostic methods in women with and without reproductive failure.
        Fertil. Steril. 2018; 109: 832-839
        • Llor C.
        • Bjerrum L.
        Antimicrobial resistance: risk associated with antibiotic overuse and initiatives to reduce the problem.
        Ther. Adv. Drug. Saf. 2014; 5 (2014): 229-241
        • McQueen D.B.
        • Bernardi L.A.
        • Stephenson M.D.
        Chronic endometritis in women with recurrent early pregnancy loss and/or fetal demise.
        Fertil. Steril. 2014; 101: 1026-1030
        • McQueen D.B.
        • Perfetto C.O.
        • Hazard F.K.
        • Lathi R.B.
        Pregnancy outcomes in women with chronic endometritis and recurrent pregnancy loss.
        Fertil. Steril. 2015; 104: 927-931
        • Melkumyan A.R.
        • Priputnevich T.V.
        • Ankirskaya A.S.
        • Murav'eva V.V.
        • Lubasovskaya L.A.
        Effects of antibiotic treatment on the lactobacillus composition of vaginal microbiota.
        Bull. Exp. Biol. Med. 2015; 158: 766-768
        • Molina N.M.
        • Sola-Leyva A.
        • Saez-Lara M.J.
        • Plaza-Diaz J.
        • Tubić-Pavlović A.
        • Romero B.
        • Clavero A.
        • Mozas-Moreno J.
        • Fontes J.
        • Altmäe S.
        New Opportunities for Endometrial Health by Modifying Uterine Microbial Composition: Present or Future?.
        Biomolecules. 2020; 10
        • Moreno I.
        • Cicinelli E.
        • Garcia-Grau I.
        • Gonzalez M.
        • Bau D.
        • Vilella F.
        • De Ziegler D.
        • Resta L.
        • Valbuena D.
        • Simon C.
        The diagnosis of chronic endometritis in infertile asymptomatic women: a comparative study of histology, microbial cultures, hysteroscopy, and molecular microbiology.
        Am. J. Obstet. Gynecol. 2018; 218 (602.e1–16)
        • Moreno I.
        • Codoner F.M.
        • Vilella F.
        • Valbuena D.
        • Martinez-Blanch J.F.
        • Jimenez-Almazan J
        Evidence that the endometrial microbiota has an effect on implantation success or failure.
        Am. J. Obstet. Gynecol. 2016; 215: 684-703
        • Ozturk M.
        • Ulubay M.
        • Alanbay I.
        • Keskin U.
        • Karasahin E.
        • Yenen M.C.
        Using narrow-band imaging with conventional hysteroscopy increases the detection of chronic endometritis in abnormal uterine bleeding and postmenopausal bleeding.
        J. Obstet. Gynaecol. Res. 2016; 42: 67-71
        • Peric A.
        • Weiss J.
        • Vulliemoz N.
        • Baud D.
        • Stojanov M.
        Bacterial Colonization of the Female Upper Genital Tract.
        IJMS. 2019; 20: 3405
        • Pinto V.
        • Matteo M.
        • Tinelli R.
        • Mitola P.C.
        • De Ziegler D.
        • Cicinelli E.
        Altered uterine contractility in women with chronic endometritis.
        Fertil. Steril. 2015; 103: 1049-1052
        • Pitsos M.
        • Skurnick J.
        • Heller D.
        Association of pathologic diagnoses with clinical findings in chronic endometritis.
        J. Reprod. Med. 2009; 54: 373-377
        • Polisseni F.
        • Bambirra E.A.
        • Camargos A.F.
        Detection of chronic endometritis by diagnostic hysteroscopy in asymptomatic infertile patients.
        Gynecol. Obstet. Invest. 2003; 55: 205-210
      1. PubMed. Accessed at:https://www.ncbi.nlm.nih.gov/pubmed/?term=chronic+endometritis. (20/1/ 2020)

        • Puente E.
        • Alonso L.
        • Laganà A.S.
        • Ghezzi F.
        • Casarin J.
        • Carugno J.
        Chronic Endometritis: Old Problem, Novel Insights and Future Challenges.
        Int. J. Fertil. Steril. 2020; 13: 250-256
        • Punnonen R.
        • Lehtinen M.
        • Teisala K.
        • Aine R.
        • Rantala I.
        • Heinonen P.K.
        • Miettinen A.
        • Laine S.
        • Paavonen J.
        The relation between serum sex steroid levels and plasma cell infiltrates in endometritis.
        Arch. Gynecol. Obstet. 1989; 244: 185-191
        • Quaas A.
        • Dokras A.
        Diagnosis and treatment of unexplained infertility.
        Rev. Obstet. Gynecol. 2008; 1: 69-76
        • Resta L.
        • Palumbo M.
        • Rossi R.
        • Piscitelli D.
        • Grazia M.
        • Cicinelli E.
        Histology of micro polyps in chronic endometritis.
        Histopathology. 2012; 60: 670-674
        • Romero R.
        • Espinoza J.
        • Mazor M.
        Can endometrial infection/inflammation explain implantation failure, spontaneous abortion, and preterm birth after in vitro fertilization?.
        Fertil. Steril. 2004; 82: 799-804
      2. Royal College of Obstetricians and Gynaecologists, Scientific Advisory Committee, Guideline No. 17. The Investigation and treatment of couples with recurrent miscarriage. 2011. [Accessed January 10, 2019]. Available from:http://www.rcog.org.uk/womens-health/clinical-guidance/investigation-and-treatmentcouples-recurrent-miscarriage-green-top-

        • Ruiz-Alonso M.
        • Blesa D.
        • Díaz-Gimeno P.
        The endometrial receptivity array for diagnosis and personalized embryo transfer as a treatment for patients with repeated implantation failure.
        Fertil. Steril. 2013; 100: 818-824
        • Samodelkin E.I.
        • Mercucheva N.G.
        • Kosareva P.V.
        • Nesterova L.Y.
        The role of prostaglandins and cyclooxygenase in pathogenesis of chronic endometritis.
        Patol. Fiziol. Eksp. Ter. 2017; 61: 98-100
        • Sekulovski N.
        • Whorton A.E.
        • Shi M.
        • MacLean J.A.
        • Hayashi K.
        Endometriotic inflammatory microenvironment induced by macrophages can be targeted by niclosamide.
        Biol. Reprod. 2019; 100: 398-408
        • Sfakianoudis K.
        • Simopoulou M.
        • Nikas Y.
        Efficient treatment of chronic endometritis through a novel approach of intrauterine antibiotic infusion: a case series.
        BMC Womens Health. 2018; 18: 197
        • Sfakianoudis K.
        • Simopoulou M.
        • Nitsos N.
        • Lazaros L.
        • Rapani A.
        • Pantou A.
        • Koutsilieris M.
        • Nikas Y.
        • Pantos K.
        Successful Implantation and Live Birth Following Autologous Platelet-rich Plasma Treatment for a Patient with Recurrent Implantation Failure and Chronic Endometritis.
        In Vivo. 2019; 33: 515-521
        • Slade P.
        • Emery J.
        • Lieberman B.A.
        A prospective, longitudinal study of emotions and relationships in in-vitro fertilization treatment.
        Hum. Reprod. 1997; 12: 183-190
        • Smit J.G.
        • Kasius J.C.
        • Eijkemans M.J.C.
        • Koks C.A.M.
        • van Golde R.
        • Nap A.W.
        • Scheffer G.J.
        • Manger P.A.P
        • Hoek A.
        • Schoot B.C.
        • van Heusden A.M.
        • Kuchenbecker W.K.H
        • Perquin D.A.M.
        • Fleischer K.
        • Kaaijk E.M.
        • Sluijmer A.
        • Friederich J.
        • Dykgraaf R.H.M.
        • van Hooff M.
        • Louwe L.A.
        • Kwee J.
        • de Koning C.H.
        • Janssen I.C.A.H.
        • Mol F.
        • Mol B.W.J
        • Broekmans F.J.M
        • Torrance H.L.
        Hysteroscopy before in-vitro fertilisation (inSIGHT): a multicentre, randomised controlled trial.
        Lancet. 2016; 387: 2622-2629
        • Smith M.
        • Hagerty K.A.
        • Skipper B.
        • Bocklage T.
        Chronic endometritis: A combined histopathologic and clinical review of cases from 2002 to 2007.
        Int. J. Gynecol. Pathol. 2010; 29: 44-50
        • Soboleva G.M.
        • Shurshalina A.V.
        • Sukhikh G.T.
        Serum activity of matrix metalloproteinases-2 and-9.
        Bull. Exp. Biol. Med. 2006; 141: 247-249
        • Song D.
        • Feng X.
        • Zhang Q.
        • Xia E.
        • Xiao Y.
        • Xie W.
        • Li T.C.
        Prevalence and confounders of chronic endometritis in premenopausal women with abnormal bleeding or reproductive failure.
        Reprod. Biomed. Online. 2018; 36: 78-83
        • Song D.
        • Li T.C.
        • Zhang Y.
        • Feng X.
        • Xia E.
        • Huang X.
        • Xiao Y.
        Correlation between hysteroscopy findings and chronic endometritis.
        Fertil. Steril. 2019; 111: 772-779
        • Streuli I.
        • Benard J.
        • Hugon-Rodin J.
        • Chapron C.
        • Santulli P.
        • Pluchino N.
        Shedding light on the fertility preservation debate in women with endometriosis: a swot analysis.
        Eur. J. Obstet. Gynecol. Reprod. Biol. 2018; 229: 172-178
        • Tabibzadeh S.S.
        • Bettica A.
        • Gerber M.A.
        Variable expression of Ia antigens in human endometrium and in chronic endometritis.
        Am. J. Clin. Pathol. 1986; 86: 153-160
        • Tersoglio A.E.
        • Salatino D.R.
        • Reinchisi G.
        • Gonzalez A.
        • Tersoglio S.
        • Marlia C.
        Repeated implantation failure in oocyte donation. What to do to improve the endometrial receptivity?.
        JBRA Assist. Reprod. 2015; 19: 44-52
        • Torlakivic E.E.
        • Nielsen S.
        • Vyberg M.
        • Taylor C.R.
        Getting controls under control: the time is now for immunochemistry.
        J. Clin. Pathol. 2015; 68: 879-882
        • Tortorella C.
        • Piazzolla G.
        • Matteo M.
        • Pinto V.
        • Tinelli R.
        • Sabba C.
        Interleukin-6, interleukin-1b, and tumor necrosis factor a in menstrual effluents as biomarkers of chronic endometritis.
        Fertil. Steril. 2014; 101: 242-247
        • Utida G.M.
        • Kulak Jr., J.
        Hysteroscopic and aspiration biopsies in the histologic evaluation of the endometrium, a comparative study.
        Medicine (Baltimore). 2019; 98: e17183
        • Vaskivuo T.E.
        • Stenbäck F.
        • Tapanainen J.S.
        Apoptosis and apoptosis related factors Bcl-2, Bax, tumor necrosis factor-alpha, and NFkappaB in human endometrial hyperplasia and carcinoma.
        Cancer. 2002; 95: 1463-1471
        • Vatansever H.S.
        • Lacin S.
        • Ozbilgin M.K.
        Changed Bcl:Bax ratio in endometrium of patients with unexplained infertility.
        Acta Histochem. 2005; 107: 345-355
        • Verhaak C.
        • Smeenk J.
        • Van Minnen A.
        • Kremer J.
        • Kraaimaat F.
        A longitudinal, prospective study on emotional adjustment before, during and after consecutive fertility treatment cycles.
        Hum. Reprod. 2005; 20: 2253-2260
        • Vicetti R.D.
        • Chivukula M.
        • Krishnamurti U.
        • Amortegui A.J.
        • Kant J.A.
        • Sweet R.L.
        • Wiesenfeld H.C.
        • Phillips J.M.
        • Cherpes T.L.
        Limitations of the criteria used to diagnose histologic endometritis in epidemiologic pelvic inflammatory disease research.
        Pathol. Res. Pract. 2011; 207: 680-685
        • Vitagliano A.
        • Saccardi C.
        • Noventa M.
        • Di Spiezio A.
        • Saccone G.
        • Cicinelli E.
        • Pizzi S.
        • Andrisani A.
        • Litta P.S.
        Effects of chronic endometritis therapy on invitro fertilization outcome in women with repeated implantation failure: a systematic review and meta-analysis.
        Fertil. Steril. 2018; 110: 103
        • Vitale S.G.
        • Bruni S.
        • Chiofalo B.
        • Riemma G.
        • Lasmar R.B.
        Updates in office hysteroscopy: a practical decalogue to perform a correct procedure.
        Updates Surg. 2020; (Available from:)
        • Volodarsky-Perel A.
        • Badeghiesh A.
        • Shrem G.
        • Steiner N.
        • Tulandi T.
        Prevalence of chronic endometritis in patients with endometrial polyps and unexplained infertility.
        Fertility and Steril. 2019; 112: e332
        • Wiesenfeld H.C.
        • Hillier S.L.
        • Meyn L.A.
        • Amortegui A.J.
        • Sweet R.L.
        Subclinical pelvic inflammatory disease and infertility.
        Obstet. Gynecol. 2012; 120: 37-43
        • Will A.J.
        • Sanchack K.E.
        Endometrial Biopsy. [Updated 2019 May 5].
        StatPearls [Internet]. StatPearls Publishing, Treasure Island (FL)2020 (2020 Jan-. Available from:)
        • Winters A.D.
        • Romero R.
        • Gervasi M.T.
        • Gomez-Lopez N.
        • Tran M.R.
        • Garcia-Flores V.
        • Pacora P.
        • Jung E.
        • Hassan S.S.
        • Hsu C.
        Does the endometrial cavity have a molecular microbial signature?.
        Sci. Rep. 2019; 9: 9905
        • Wu D.
        • Kimura F.
        • Zheng L.
        • Ishida M.
        • Niwa Y.
        • Hirata K.
        Chronic endometritis modifies decidualization in human endometrial stromal cells.
        Reprod. Biol. Endocrinol. 2017; 15: 16
        • Yang R.
        • Du X.
        • Wang Y.
        • Song X.
        • Yang Y.
        • Qiao J.
        The hysteroscopy and histological diagnosis and treatment value of chronic endometritis in recurrent implantation failure patients.
        Arch. Gynecol. Obstet. 2014; 289: 1363-1369
        • Yoshii N.
        • Hamatani T.
        • Inagaki N.
        • Hosaka T.
        • Inoue O.
        • Yamada M.
        • Machiya R.
        • Yoshimura Y.
        • Odawara Y.
        Successful implantation after reducing matrix metalloproteinase activity in the uterine cavity.
        Reprod. Biol. Endocrinol. 2013; 11: 37
        • Zolghadri J.
        • Momtahan M.
        • Aminian K.
        • Ghaffarpasand F.
        • Tavana Z.
        The value of hysteroscopy in diagnosis of chronic endometritis in patients with unexplained recurrent spontaneous abortion.
        Eur. J. Obstet. Gynecol. Reprod. Biol. 2011; 155: 217-220

      Biography

      Juan José Espinós is a Specialist in Reproductive Endocrinology, Co-Director of Fertty-Barcelona and Professor of UAB, Spain. He is also co-founder of the Interest Group on Reproductive Endocrinology of the Spanish Fertility Society and President of the National Spanish Fertility Society Meeting held in Barcelona in 2014.
      Key message
      Pending new evidence, it would be advisable not to include chronic endometritis in the initial baseline study before assisted reproduction in order not to delay other assisted reproduction treatments.