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Chronic Endometritis Due to Common Bacteria Is Prevalent in Women With Recurrent Miscarriage as Confirmed by Improved Pregnancy Outcome After Antibiotic Treatment

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Abstract

Recurrent miscarriage (RM) is defined as 3 or more miscarriages before 20 weeks’ pregnancy. In recent years, interest has been focused on chronic endometritis (CE), a subtle inflammation thought to be associated with RM. We aimed to evaluate the relationships between CE and RM. The records of 360 women with unexplained RM were retrospectively analyzed. Data from hysteroscopy, endometrial histology, endometrial culture, and polymerase chain reaction for chlamydia, performed before and after antibiotic treatment for CE, were analyzed. The occurrence of successful pregnancies within 1 year after treatment was also evaluated. Results showed that 208 (57.8%) women with RM showed CE at hysteroscopy; 190 (91.3%), positive at hysteroscopy, were also positive at histology, and 142 (68.3%) had positive cultures. Common bacteria were found in 110 (77.5%) patients. Mycoplasma and Ureaplasma were found in 36 (25.3%) patients and Chlamydia in 18 patients (12.7%). In 102 (71%) women, antibiogram-based antibiotic treatment normalized hysteroscopy, histology, and cultures (group 1); while in 40 (28.2%) patients, CE was still present at hysteroscopy (group 2). In 16 of the 66 patients positive at hysteroscopy, but not at cultures, the hysteroscopy becomes normal (group 3) after a Centers for Disease Control and Prevention-based therapy; while in 50 women, CE was still present (group 4). One year after treatment, group 1 showed a significantly higher number of pregnancies (78.4%) compared to group 2 (17.5%; P < .001) and group 4 (15.3%; P = .005). The CE is frequent in women with RM. Antibiotic treatment seems to be associated with an improved reproductive outcome.

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References

  1. Rai R, Regan L. Recurrent miscarriage. Lancet. 2006;368(9535): 601–611.

    Article  Google Scholar 

  2. La Sala GB, Montanari R, Dessanti L, Cigarini C, Sartori F. The role of diagnostic hysteroscopy and endometrial biopsy in assisted reproductive technologies. Fertil Steril. 1998;70(2):378–380.

    Article  Google Scholar 

  3. Oliveira FG, Abdelmassih VG, Diamond MP, Dozortsev D, Nagy ZP, Abdelmassih R. Uterine cavity findings and hysteroscopic interventions in patients undergoing in vitro fertilization-embryo transfer who repeatedly cannot conceive. Fertil Steril. 2003;80(6):1371–1375.

    Article  Google Scholar 

  4. Demirol A, Gurgan T. Effect of treatment of intrauterine pathologies with office hysteroscopy in patients with recurrent IVF failure. Reprod Biomed Online. 2004;8(5):590–594.

    Article  Google Scholar 

  5. Rama Raju GA, Shashi Kumari G, Krishna KM, Prakash GJ, Madan K. Assessment of uterine cavity by hysteroscopy in assisted reproduction programme and its influence on pregnancy outcome. Arch Gynecol Obstet. 2006;274(3):160–164.

    Article  CAS  Google Scholar 

  6. Bosteels J, Weyers S, Puttemans P, et al. The effectiveness of hysteroscopy in improving pregnancy rates in subfertile women without other gynaecological symptoms: a systematic review. Hum Reprod Update. 2010;16(1):1–11.

    Article  Google Scholar 

  7. Fatemi HM, Kasius JC, Timmermans A, et al. Prevalence of unsuspected uterine cavity abnormalities diagnosed by office hysteroscopy prior to in vitro fertilization. Hum Reprod. 2010;25(8): 1959–1965.

    Article  CAS  Google Scholar 

  8. Makrakis E, Pantos K. The outcomes of hysteroscopy in women with implantation failures after in-vitro fertilization: findings and effect on subsequent pregnancy rates. Curr Opin Obstet Gynecol. 2010;22(4):339–343.

    PubMed  Google Scholar 

  9. Greenwood SM, Moran JJ. Chronic endometritis: morphologic and clinical observations. Obstet Gynecol. 1981;58(2):176–184.

    CAS  PubMed  Google Scholar 

  10. Resta L, Palumbo M, Rossi R, Piscitelli D, Grazia Fiore M, Cicinelli E. Histology of micro polyps in chronic endometritis. Histopathology. 2012;60(4):670–674.

    Article  Google Scholar 

  11. Cicinelli E, Resta L, Nicoletti R, Zappimbulso V, Tartagni M, Saliani N. Endometrial micropolyps at fluid hysteroscopy suggest the existence of chronic endometritis. Hum Reprod. 2005;20(5):1386–1389.

    Article  Google Scholar 

  12. Cicinelli E, Resta L, Nicoletti R, et al. Detection of chronic endometritis at fluid hysteroscopy. J Minim Invasive Gynecol. 2005; 12(6):514–518.

    Article  Google Scholar 

  13. 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 hyster-oscopies. Fertil Steril. 2008;89(3):677–684.

    Article  Google Scholar 

  14. Matteo M, Cicinelli E, Greco P, et al. Abnormal pattern of lymphocyte subpopulations in the endometrium of infertile women with chronic endometritis. Am J Reprod Immunol. 2009;61(5):322–329.

    Article  Google Scholar 

  15. Kitaya K, Yasuo T. Aberrant expression of selectin E, CXCL1, and CXCL13 in chronic endometritis. Mod Pathol. 2010;23(8): 1136–1146.

    Article  CAS  Google Scholar 

  16. Johnston-MacAnanny EB, Hartnett J, Engmann LL, Nulsen JC, Sanders MM, Benadiva CA. Chronic endometritis is a frequent finding in women with recurrent implantation failure after in vitro fertilization. Fertil Steril. 2010;93(2):437–441.

    Article  Google Scholar 

  17. Kasius JC, Fatemi HM, Bourgain C, et al. The impact of chronic endometritis on reproductive outcome. Fertil Steril. 2011;96(6): 1451–1456.

    Article  Google Scholar 

  18. Workowski KA, Berman S; Centers for Disease Control and Prevention (CDC). Sexually transmitted diseases treatment guidelines, 2010. MMWR Recomm Rep. 2010;59(RR-12):1–110.

    PubMed  Google Scholar 

  19. Nigro G, Mazzocco M, Mattia E, Di Renzo GC, Carta G, Anceschi MM. Role of the infections in recurrent spontaneous abortion. J Matern Fetal Neonatal Med. 2011;24(8):983–989.

    Article  Google Scholar 

  20. Ness RB, Soper DE, Holley RL, et al. Effectiveness of inpatient and outpatient treatment strategies for women with pelvic inflammatory disease: results from the Pelvic Inflammatory Disease Evaluation and Clinical Health (PEACH) randomized trial. Am J Obstet Gynecol. 2002;186(5):929–937.

    Article  Google Scholar 

  21. Espinoza J, Erez O, Romero R. Preconceptional antibiotic treatment to prevent preterm birth in women with a previous preterm delivery. Am J Obstet Gynecol. 2006;194(3):630–637.

    Article  CAS  Google Scholar 

  22. Kamiyama S, Teruya Y, Nohara M, Kanazawa K. Impact of detection of bacterial endotoxin in menstrual effluent on the pregnancy rate in in vitro fertilization and embryo transfer. Fertil Steril. 2004;82(4):788–792.

    Article  Google Scholar 

  23. Cowling P, McCoy DR, Marshall RJ, Padfield CJ, Reeves DS. Bacterial colonization of the non-pregnant uterus: a study of pre-menopausal abdominal hysterectomy specimens. Eur J Clin Microbiol Infect Dis. 1992;11(2):204–205.

    Article  CAS  Google Scholar 

  24. Cicinelli E, Ballini A, Marinaccio M, et al. Microbiological findings in endometrial specimen: our experience. Arch Gynecol Obstet. 2012;285(5):1325–1329.

    Article  Google Scholar 

  25. Korn AP, Bolan G, Padian N, Ohm-Smith M, Schachter J, Landers DV. Plasma cell endometritis in women with symptomatic bacterial vaginosis. Obstet Gynecol. 1995;85(3):387–390.

    Article  CAS  Google Scholar 

  26. Eckert LO, Moore DE, Patton DL, Agnew KJ, Eschenbach DA. Relationship of vaginal bacteria and inflammation with conception and early pregnancy loss following in-vitro fertilization. Infect Dis Obstet Gynecol. 2003;11(1):11–17.

    Article  Google Scholar 

  27. 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(4):799–804.

    Article  Google Scholar 

  28. Romero R, Mazor M. Infection and preterm labor. Clin Obstet Gynecol. 1988;31(3):553–584.

    Article  CAS  Google Scholar 

  29. Salim R, Ben-Shlomo I, Colodner R, Keness Y, Shalev E. Bacterial colonization of the uterine cervix and success rate in assisted reproduction: results of a prospective survey. Hum Reprod. 2002;17(2):337–340.

    Article  Google Scholar 

  30. Haggerty CL, Totten PA, Astete SG, Ness RB. Mycoplasma genitalium among women with nongonococcal, nonchlamydial pelvic inflammatory disease. Infect Dis Obstet Gynecol. 2006;2006:30184.

    Article  Google Scholar 

  31. Stern RA, Svoboda-Newman SM, Frank TS. Analysis of chronic endometritis for Chlamydia trachomatis by polymerase chain reaction. Hum Pathol. 1996;27(10):1085–1088.

    Article  CAS  Google Scholar 

  32. 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.

    Article  Google Scholar 

  33. Valli E, Zupi E, Marconi D, et al. Hysteroscopic findings in 344 women with recurrent spontaneous abortion. J Am Assoc Gynecol Laparosc. 2001;8(3):398–401.

    Article  CAS  Google Scholar 

  34. Bohlmann MK, von Wolff M, Luedders DW, et al. Hysteroscopic findings in women with two and with more than two first-trimester miscarriages are not significantly different. Reprod Biomed Online. 2010;21(2):230–236.

    Article  Google Scholar 

  35. Cicinelli E, Parisi C, Galantino P, Pinto V, Barba B, Schonauer S. Reliability, feasibility, and safety of minihysteroscopy with a vaginoscopic approach: experience with 6,000 cases. Fertil Steril. 2003;80(1):199–202.

    Article  Google Scholar 

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Authors and Affiliations

  1. Department of Biomedical and Human Oncological Science (DIMO), 3rd Unit of Obstetrics and Gynecology, University of Bari, Piazza Giulio Cesare, 70124, Bari, Italy

    Ettore Cicinelli MD, Vincenzo Pinto MD & Marco Marinaccio MD

  2. Department of Medical and Surgical Sciences, Institute of Obstetrics and Gynecology, University of Foggia, Foggia, Italy

    Maria Matteo MD

  3. Department of Obstetrics and Gynecology, San Bastiano Hospital, Bassano del Grappa, Vicenza, Italy

    Raffaele Tinelli MD

  4. Operative Unit of Obstetric and Gynecology of Civitanova Marche, Civitanova Marche, Italy, Italy

    Ugo Indraccolo MD

  5. Department of Obstetrics, Gynecology and Reproductive Medicine, Université Paris Descartes, Paris Sorbonne Cité-Assistance Publique Hôpitaux de Paris, CHU Cochin, Paris, France

    Dominique De Ziegler MD

  6. Department of Pathology, University of Bari, Bari, Italy

    Leonardo Resta MD

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  1. Ettore Cicinelli MD
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  2. Maria Matteo MD
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  3. Raffaele Tinelli MD
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  4. Vincenzo Pinto MD
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  5. Marco Marinaccio MD
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  7. Dominique De Ziegler MD
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  8. Leonardo Resta MD
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Correspondence to Ettore Cicinelli MD.

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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. 21, 640–647 (2014). https://doi.org/10.1177/1933719113508817

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  • DOI: https://doi.org/10.1177/1933719113508817

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