open access

Ahead of Print
Review paper
Published online: 2022-12-09
Get Citation

Chronic endometritis — is it time to clarify diagnostic criteria?

Katarzyna Klimaszyk1, Henriette Svarre Nielsen2, Ewa Wender-Ozegowska1, Malgorzata Kedzia1
DOI: 10.5603/GP.a2022.0147
·
Pubmed: 36511457
Affiliations
  1. Department of Reproduction, Poznan University of Medical Sciences, Poznan, Poland
  2. The Recurrent Pregnancy Loss Unit, The Capital Region, The Fertility Clinic, Copenhagen University Hospitals Rigshospitalet and Hvidovre, Copenhagen, Denmark, Denmark

open access

Ahead of Print
REVIEW PAPERS Gynecology
Published online: 2022-12-09

Abstract

Chronic endometritis is a persistent, low-intensity inflammation of endometrial mucosa, characterized by the infiltration of plasma cells into the endometrial stroma This immunological alteration is thought to be a consequence of a bacterial infection. For a long time, chronic endometritis was poorly investigated and rarely considered in clinical practice because it is either asymptomatic or presents with no specific symptoms. Its association with adverse effects on fertility and retrospectively reported effectiveness of antibiotic treatment were the main reasons for a growing interest in this endometrial pathology. Chronic endometritis is now a hot topic in recurrent pregnancy loss and recurrent implantation failure research.

Nevertheless, there are still no recommendations to include chronic endometritis investigation in a clinical evaluation of infertile patients. The uncertain role of this condition is an effect of significant differences in study results presented by different research groups. One important reason for these inconsistent findings is a lack of standardised chronic endometritis diagnostic methods.

We present a review of the literature, focusing on the currently available chronic endometritis diagnostic techniques. The review is subdivided into three parts concerning the diagnostic accuracy of three main diagnostic modalities. Histopathological examination of endometrial tissue, hysteroscopic evaluation of uterine cavity and identification of the bacterial factor.

In conclusion, it is of great importance to establish a consensus on the diagnostic criteria for chronic endometritis. This is the only way to enhance international cooperation and create well-design multicenter studies to evidence the role of this endometrial pathology in infertility.

Abstract

Chronic endometritis is a persistent, low-intensity inflammation of endometrial mucosa, characterized by the infiltration of plasma cells into the endometrial stroma This immunological alteration is thought to be a consequence of a bacterial infection. For a long time, chronic endometritis was poorly investigated and rarely considered in clinical practice because it is either asymptomatic or presents with no specific symptoms. Its association with adverse effects on fertility and retrospectively reported effectiveness of antibiotic treatment were the main reasons for a growing interest in this endometrial pathology. Chronic endometritis is now a hot topic in recurrent pregnancy loss and recurrent implantation failure research.

Nevertheless, there are still no recommendations to include chronic endometritis investigation in a clinical evaluation of infertile patients. The uncertain role of this condition is an effect of significant differences in study results presented by different research groups. One important reason for these inconsistent findings is a lack of standardised chronic endometritis diagnostic methods.

We present a review of the literature, focusing on the currently available chronic endometritis diagnostic techniques. The review is subdivided into three parts concerning the diagnostic accuracy of three main diagnostic modalities. Histopathological examination of endometrial tissue, hysteroscopic evaluation of uterine cavity and identification of the bacterial factor.

In conclusion, it is of great importance to establish a consensus on the diagnostic criteria for chronic endometritis. This is the only way to enhance international cooperation and create well-design multicenter studies to evidence the role of this endometrial pathology in infertility.

Get Citation

Keywords

chronic endometritis; diagnostic techniques; immunohistochemistry; hysteroscopy; endometrial microbiome

About this article
Title

Chronic endometritis — is it time to clarify diagnostic criteria?

Journal

Ginekologia Polska

Issue

Ahead of Print

Article type

Review paper

Published online

2022-12-09

Page views

137

Article views/downloads

120

DOI

10.5603/GP.a2022.0147

Pubmed

36511457

Keywords

chronic endometritis
diagnostic techniques
immunohistochemistry
hysteroscopy
endometrial microbiome

Authors

Katarzyna Klimaszyk
Henriette Svarre Nielsen
Ewa Wender-Ozegowska
Malgorzata Kedzia

References (45)
  1. Greenwood SM, Moran JJ. Chronic endometritis: morphologic and clinical observations. Obstet Gynecol. 1981; 58(2): 176–184.
  2. 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. Reprod Sci. 2014; 21(5): 640–647.
  3. McQueen DB, Perfetto CO, Hazard FK, et al. Pregnancy outcomes in women with chronic endometritis and recurrent pregnancy loss. Fertil Steril. 2015; 104(4): 927–931.
  4. Wiesenfeld HC, Hillier SL, Meyn LA, et al. Subclinical pelvic inflammatory disease and infertility. Obstet Gynecol. 2012; 120(1): 37–43.
  5. Song D, Li TC, Zhang Y, et al. Correlation between hysteroscopy findings and chronic endometritis. Fertil Steril. 2019; 111(4): 772–779.
  6. Kasius JC, Broekmans FJM, Sie-Go DM, et al. The reliability of the histological diagnosis of endometritis in asymptomatic IVF cases: a multicenter observer study. Hum Reprod. 2012; 27(1): 153–158.
  7. Song D, He Y, Wang Y, et al. Impact of antibiotic therapy on the rate of negative test results for chronic endometritis: a prospective randomized control trial. Fertil Steril. 2021; 115(6): 1549–1556.
  8. Cicinelli E, Resta L, Loizzi V, et al. Antibiotic therapy versus no treatment for chronic endometritis: a case-control study. Fertil Steril. 2021; 115(6): 1541–1548.
  9. 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. Hum Reprod. 2015; 30(2): 323–330.
  10. Xiong Y, Chen Qi, Chen C, et al. 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. 2021; 116(2): 413–421.
  11. Gay C, Hamdaoui N, Pauly V, et al. Impact of antibiotic treatment for chronic endometritis on unexplained recurrent pregnancy loss. J Gynecol Obstet Hum Reprod. 2021; 50(5): 102034.
  12. Cicinelli E, Matteo M, Trojano G, et al. Chronic endometritis in patients with unexplained infertility: Prevalence and effects of antibiotic treatment on spontaneous conception. Am J Reprod Immunol. 2018; 79(1).
  13. Practice Committee of the American Society for Reproductive Medicine. Electronic address: asrm@asrm.org, Practice Committee of the American Society for Reproductive Medicine. Evidence-based treatments for couples with unexplained infertility: a guideline. Fertil Steril. 2020; 113(2): 305–322.
  14. Bender Atik R, Christiansen OB, Elson J, et al. ESHRE Guideline Group on RPL. ESHRE guideline: recurrent pregnancy loss. Hum Reprod Open. 2018; 2018(2): hoy004.
  15. Huang W, Liu Bo, He Y, et al. Variation of diagnostic criteria in women with chronic endometritis and its effect on reproductive outcomes: A systematic review and meta-analysis. J Reprod Immunol. 2020; 140: 103146.
  16. Liu Y, Chen X, Huang J, et al. 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(5): 832–839.
  17. Farooki MA. Epidemiology and pathology of chronic endometritis. Int Surg. 1967; 48(6): 566–573.
  18. 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. Fertil Steril. 2010; 93(2): 437–441.
  19. Moreno I, Cicinelli E, Garcia-Grau I, et al. 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(6): 602.e1–602.e16.
  20. Inki P. Expression of syndecan-1 in female reproductive tract tissues and cultured keratinocytes. Mol Hum Reprod. 1997; 3(4): 299–305.
  21. O’Connell F, Pinkus J, Pinkus G. CD138 (Syndecan-1), a Plasma Cell Marker. Am J Clin Pathol. 2004; 121(2): 254–263.
  22. Kannar V, Lingaiah HK, Sunita V. Evaluation of endometrium for chronic endometritis by using syndecan-1 in abnormal uterine bleeding. J Lab Physicians. 2012; 4(2): 69–73.
  23. 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(2): 485–488.
  24. McQueen DB, Maniar KP, Hutchinson A, et al. Redefining chronic endometritis: the importance of endometrial stromal changes. Fertil Steril. 2021; 116(3): 855–861.
  25. Cicinelli E, Haimovich S, De Ziegler D, et al. International Working Group for Standardization of Chronic Endometritis Diagnosis. 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. 2022; 39(1): 219–226.
  26. 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. Int J Surg Pathol. 2019; 27(4): 372–379.
  27. Hirata K, Kimura F, Nakamura A, et al. Histological diagnostic criterion for chronic endometritis based on the clinical outcome. BMC Womens Health. 2021; 21(1): 94.
  28. 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? Am J Reprod Immunol. 2021; 85(5): e13369.
  29. Margulies SL, Dhingra I, Flores V, et al. The diagnostic criteria for chronic endometritis: a survey of pathologists. Int J Gynecol Pathol. 2021; 40(6): 556–562.
  30. Zolghadri J, Momtahan M, Aminian K, et al. The value of hysteroscopy in diagnosis of chronic endometritis in patients with unexplained recurrent spontaneous abortion. Eur J Obstet Gynecol Reprod Biol. 2011; 155(2): 217–220.
  31. Cicinelli E, Resta L, Nicoletti R, et al. Endometrial micropolyps at fluid hysteroscopy suggest the existence of chronic endometritis. Hum Reprod. 2005; 20(5): 1386–1389.
  32. Cicinelli E, Resta L, Nicoletti R, et al. Detection of chronic endometritis at fluid hysteroscopy. J Minim Invasive Gynecol. 2005; 12(6): 514–518.
  33. Cicinelli E, De Ziegler D, Nicoletti R, et al. Chronic endometritis: correlation among hysteroscopic, histologic, and bacteriologic findings in a prospective trial with 2190 consecutive office hysteroscopies. Fertil Steril. 2008; 89(3): 677–684.
  34. Zargar M, Ghafourian M, Nikbakht R, et al. Evaluating chronic endometritis in women with recurrent implantation failure and recurrent pregnancy loss by hysteroscopy and immunohistochemistry. J Minim Invasive Gynecol. 2020; 27(1): 116–121.
  35. Bouet PE, El Hachem H, Monceau E, et al. 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(1): 106–110.
  36. Cicinelli E, Vitagliano A, Kumar A, et al. 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(1): 162–173.e2.
  37. Gkrozou F, Tsonis O, Dimitriou E, et al. In women with chronic or subclinical endometritis is hysteroscopy suitable for setting the diagnosis? A systematic review. J Obstet Gynaecol Res. 2020; 46(9): 1639–1650.
  38. Buzzaccarini G, Vitagliano A, Andrisani A, et al. Chronic endometritis and altered embryo implantation: a unified pathophysiological theory from a literature systematic review. J Assist Reprod Genet. 2020; 37(12): 2897–2911.
  39. Cicinelli E, De Ziegler D, Nicoletti R, et al. Poor reliability of vaginal and endocervical cultures for evaluating microbiology of endometrial cavity in women with chronic endometritis. Gynecol Obstet Invest. 2009; 68(2): 108–115.
  40. Kitaya K, Matsubayashi H, Takaya Y, et al. Live birth rate following oral antibiotic treatment for chronic endometritis in infertile women with repeated implantation failure. Am J Reprod Immunol. 2017; 78(5).
  41. Chen C, Song X, Wei W, et al. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat Commun. 2017; 8(1): 875.
  42. Ding T, Schloss PD. Dynamics and associations of microbial community types across the human body. Nature. 2014; 509(7500): 357–360.
  43. Moreno I, Codoñer FM, Vilella F, et al. Evidence that the endometrial microbiota has an effect on implantation success or failure. Am J Obstet Gynecol. 2016; 215(6): 684–703.
  44. Moreno I, Garcia-Grau I, Perez-Villaroya D, et al. Endometrial microbiota composition is associated with reproductive outcome in infertile patients. Microbiome. 2022; 10(1): 1.
  45. D'Ippolito S, Di Nicuolo F, Pontecorvi A, et al. Endometrial microbes and microbiome: Recent insights on the inflammatory and immune "players" of the human endometrium. Am J Reprod Immunol. 2018; 80(6): e13065.

Regulations

Important: This website uses cookies. More >>

The cookies allow us to identify your computer and find out details about your last visit. They remembering whether you've visited the site before, so that you remain logged in - or to help us work out how many new website visitors we get each month. Most internet browsers accept cookies automatically, but you can change the settings of your browser to erase cookies or prevent automatic acceptance if you prefer.

By VM Media Group sp. z o.o., ul. Świętokrzyska 73, 80–180 Gdańsk
tel.:+48 58 320 94 94, faks:+48 58 320 94 60, e-mail:  viamedica@viamedica.pl