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Endometritis is an infection of the gastrointestinal flora from the lower genital tract to the uterine uterine that is grouped cavity during childbirth (7,8). The route of delivery dictates the under the more general classification likelihood of endometritis onset, with vaginal delivery having of pelvic inflammatory (PID) a 1% to 3%, scheduled Cesarean deliveries 5% to 15% and along with , tubo-ovarian unscheduled Cesarean deliveries 15% to 90% associated abscesses and pelvic peritonitis. risks, respectively. These incidences are of particular concern These terms are used to designate the extent of ascending as the number of Cesarean deliveries annually continues to infection within the (1). Diagnosis of PID is imprecise, rise and accounted for approximately 30% of all births in 2008 as it is typically reliant upon vague clinical symptomologies, (8,9). The rates associated with Cesarean deliveries vary including tenderness in the pelvic region, basal temperatures greatly depending upon when prophylactic therapy of 101oF or greater and mucopurulent cervical or vaginal was administered with lower incidence rates associated with discharge. A history of infection with the sexually transmitted presurgical administration (10,11). Complications during Chlamydia trachomatis or Neisseria gonorrhoeae is childbirth, including prolonged labor with multiple vaginal also suggestive of PID (Table 1). More recently, studies have exams, premature rupture of membranes (PROM), preterm implicated several other pathogens as having an association labor, and lower socio-economic status are with endometritis (Table 2). Left untreated, such infections all risk factors that increase the likelihood of endometritis. can have very serious deleterious outcomes in individuals Pathogens associated with Bacterial Vaginosis (BV) have ranging from repeated bouts of infection to increased also been implicated as causative agents of endometritis as incidence of ectopic or even sterility (2-4). a large number of women with PID were also identified as BV positive (3,4). Table 1. Clinical associations suggestive of endometritis.

General Endometritis: Table 2. Pathogens detected in cases of endometritis. • Abnormal or discharge Pathogen Reference • • General malaise Chlamydia trachomatis 1,5,7,8,12 • Previous episode of PID (5) Neisseria gonorrhoeae 1,5,7,8,12 • Preceded by confirmed infection with either Actinomyces israelii 13,14 Chlamydia trachomatis or Neisseria gonorrhoeae (5) Enterococcus faecalis 12,15 • Presence of bacteria within the uterine cavity Escherichia coli 7,12 Puerperal Endometritis: Group A Streptococcus 15,16 • Recently gave birth Klebsiella pneumoniae 17 • Foul-smelling post-partum • Identification of bacteria within the uterine cavity genitalium 18-20 Acute Endometritis: Proteus mirabilis 17,21 • Presence of neutrophils in wet prep Pseudomonas aeruginosa 22 • Fever 12,15,23 Chronic Endometritis: 21 • Presence of lymphocytes in wet prep (6) 15,16,24 • Previous surgical procedures Group B Streptococcus 10,25,26 • Presence of Peptostreptococcus 8 Causality Staphylococcus spp. 12,15 Infectious causality is generally defined as either puerperal Streptococcus spp. 7,12 or non-obstetrically related. Puerperal endometritis is a BV-related pathogens 2,4 polymicrobial infection usually involving two or three different = Higher Prevalence organisms resulting from the ascension of normal vaginal or

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• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • TM 5_11 Medical Diagnostic Laboratories, L.L.C. CLINICAL www.mdlab.com • 877.269.0090 DIAGNOSTICS Pathologically, there are two distinct classifications of revealed an added benefit associated with the suction endometritis, acute and chronic, that are differentiated by cannula method of collecting endometrial samples whereby the type of infiltrating immune cells present at the time of the induction of localized injury within the endometrium was analysis. Acute endometritis is typified by infiltration of found to improve implantation efficiency (34,35). the endometrial glands by neutrophils and usually results from either an invasive gynecologic procedure or infection Diagnosis with a sexually transmitted disease (STD). Chronic Diagnosis of endometritis is difficult due to the confounding endometritis is associated with lymphocytes, or plasma nature of the presenting symptoms, making consideration cells, within the stroma of the endometrium. Proper analyses of the patient’s past medical history and current lifestyle for diagnostic purposes requires a trained pathologist essential. Due to the lack of specific symptoms, diagnosis skilled at differentiating immune infiltrates resulting from is typically one of exclusion. A combination of physical endometrial infection from those that are present during examination and non-invasive testing methods are combined various premenstrual and menstrual phases (27). As the to eliminate disorders with overlapping symptoms. Pelvic actual number of infiltrating cells does not differ dramatically examination revealing vaginal or cervical discharge and between the two scenarios, other morphological features cervical, adnexal and uterine tenderness are presumptive, must be considered for a definitive diagnosis of endometritis. therefore necessitating the collection of wet preps, blood Causal factors associated with chronic endometritis cases cultures and vaginal swabs to identify associated pathogens. are rather broad and encompass any event that could Reliance upon vaginal swabs with respect to the identification theoretically induce an inflammatory reaction within the of an infectious etiology can prove misleading. Cicinelli et endometrium, including the presence of an intrauterine al. evaluated swabs collected from both the vaginal and device, surgical procedures or the presence of common endometrial tracts of women with chronic endometritis for the bacteria (28). These two classifications also differ from one presence of specific pathogens and found that the vaginal another symptomatically, whereby acute cases typically flora differed dramatically from that of the endometrium in present with pelvic pain accompanied by some of the 67.4% of the 438 cases analyzed (Table 3) (39). Urinalysis symptoms noted in Table 1, while chronic cases are often and urine cultures serve as differential diagnoses to rule asymptomatic or accompanied by very mild symptoms and out possible urinary tract infections. Localizing the infection run a greater risk of going untreated and thereby resulting in to the genital tract is also presumptive as a number of more dire consequences for the individual. disorders fall under the PID heading. As a result, the CDC in their 2010 Sexually Transmitted Disease Treatment Association of Endometritis with Guidelines recommended endometrial biopsy followed by The association of chronic endometritis relating to infertility is histopathologic evaluation for the diagnosis of endometritis a notion that dates back over a century (29). The advancement and discouraged the use of laparoscopy as this method is of medicine has since provided the clinical tools to confirm more suitable for advanced infections, like salpingitis (1). this early observation. Chronic endometritis has been linked with fertility issues, including an inability to conceive, Table 3. Presence of bacterial pathogens within the uterine cavity recurrent implantation failure (RIF) and spontaneous abortion and their association with endometritis. Numbers in parentheses (30-32). While most cases have been associated with more within the endometrium column refer to cases having associated severe forms of PID that result in structural damage within fertility issues. (Adapted from 39). this region, particularly scarring of the fallopian tubes, recent evidence reveals less severe infections are also a cause Treatment for concern (33-35). While Neisseria gonorrhoeae and Chlamydia trachomatis are typically considered causative Chronic endometritis Control group factors of infertility, studies of women who have failed multiple at hysteroscopy (n=100) rounds of in vitro fertilization have identified a number of (n=438) Infectious pathogenic agents that were more commonly detected Endometrium Vagina Endometrium than Neisseria gonorrhoeae and Chlamydia trachomatis. Agent One study revealed a 10% detection rate of Ureaplasma E. coli 38 50 (20 15 1 urealyticum in their patient population compared to a 2.7% Streptococci 80 122 (60) 16 2 Staphylococci 0 20 (17) 1 0 rate for Chlamydia (12). There are several techniques that E. faecalis 22 62 (26) 7 1 can aid in identifying the reason for recurrent implantation Chlamydia 2 12 (11) 0 0 failure, including karyotypic analyses, screening for serum Ureaplasma 86 44 (26) 5 1 immunologic modulators and complete assessment of the Yeast 26 10 (3) 10 0 uterine cavity (33). In such cases, endometrial biopsy has Total 254 320 54 5 proven to be a useful, inexpensive and minimally invasive method of analyzing the endometrium. This study also Parenteral and oral are the main form of Pathogen treatment for both PID and endometritis and are equivalent Chlamydia trachomatis with respect to efficacy in women with mild or moderate infections (1). Due to the polymicrobial nature of endometritis, Neisseria gonorrhoeae recommendations include the use of a combination of Actinomyces israelii broad spectrum antibiotics capable of combating both Enterococcus faecalis Gram positive and Gram negative bacteria. Escherichia coli inclusion should also be considered to offer the broadest level of coverage based on the reported association Group A Streptococcus between BV and endometritis (1). Clinical response to Klebsiella species therapy and attenuation of symptoms should be noticeable within the first seventy-two hours of antibiotic therapy. If the patient’s condition does not improve within this time frame, the diagnosis should be confirmed and the patient placed on Proteus mirabilus parenteral therapy (1). Pseudomonas aeruginosa Sampling the Endometrial Cavity Ureaplasma urealyticum While there are several methods recommended for sampling Table 4. Endometritis-specific assays offered by MDL in the endometrium, clinical studies have demonstrated conjunction with the Endocell™ endometrial cell sampler. reduced risk of procedure-induced complications and Use of the Endocell™ device should be in compliance with patient-reported pain to be associated with suction cannula the manufacturer’s guidelines. Please carefully read all collection devices compared to the once standard D&C safety information included in the Wallach product brochure method (37,38). Suction cannula collection devices are before using the Endocell™ endometrial cell sampler. Once minimally invasive in comparison to curettage methods the sample has been collected, the cells can be discharged and can be performed in the physician’s office as opposed into the OneSwab® specimen transport vial for submission to the hospital; in most cases, cervical dilation is not to the laboratory. Pathogen identification at the sensitive necessary. Administration of an NSAID a few hours prior molecular level will aid in endometritis diagnosis, as well as to the procedure has been shown to alleviate the mild in the selection of the most efficacious antibiotic regimen discomfort and cramping some women report as a result of the procedure. References 1. Centers for Disease Control and Prevention. Sexually Transmitted Treatment Guidelines, 2010. MMWR 2010; 59(No. RR-12): 63-67. 2. Haggerty CL, Totten PA, Ferris M, et al. 2009. Clinical characteristics of bacterial vaginosis among women testing positive for fastidious bacteria. Sex Trans Infect. 85: 242-8. 3. Ness RB, Hillier SL, Kip KE, et al. 2004. Bacterial vaginosis and risk of pelvic inflammatory disease.Obstet Gynecol. 104:1-9. 4. Ness RB, Kip KE, Hillier SE, et al. 2005. A cluster analysis of bacterial vaginosis-associated microflora and pelvic inflammatory disease. Am J Epidemiol. 162: 585-90. 5. Chen KT. Endometritis unrelated to pregnancy. Accessed February 4, 2011. http://www.uptodate.com/contents/ Figure 1. A diagram demonstrating the proper sampling technique endometritis-unrelated-to-pregnancy? for suction cannula collection devices. 6. Hagerty CL, Smith M, Bocklage T. Chronic endometritis MDL provides an Endometrial Sampling Kit that includes revisited: a review of the pathology and clinical findings. In press. the Endocell™ endometrial cell sampler manufactured Accessed February 1, 2011. http://repository.unm.edu/bitstream/ by Wallach Surgical Devices, Inc. in conjunction with its handle/1928/6822/Hagerty%20Endometritis%20Research%20 Paper%20with%20Tables.pdf?sequence=1. OneSwab® specimen transport vial to provide physicians with the tools necessary to properly diagnose genital tract 7. Chandran L, Puccio JA. 2008. Endometritis. Accessed February 8, 2011. http://emedicine.medscape.com/ article/953320-print. infections from the uterine cavity (Table 4). Collection of endometrial samples should be limited to patients with 8. Simmons GT. 2010. Endometritis. Accessed January 24, 2011. http://emedicine.medscape.com/article/ 254169-print. suspected chronic endometritis resulting from suspected bacterial infection and should not be used to diagnose 9. Centers for Disease Control and Prevention, Division of Vital Statistics. Births: Final data for 2008. Accessed February 8, cervicovaginal infections. Please ensure that all laboratory 2011. http://www.cdc.gov/nchs/data/nvsr/ nvsr59/nvsr59_01.pdf. tests are medically necessary. 10. Faro, S. 2005. Postpartum endometritis. Clin Perinatol. 32: 803- 26. Winn HN. 2007. Group B Streptococcus infection in pregnancy. 14. Clin Perinatol. 34: 387-92. 11. Tita, ATN, Hauth JC, Grimes A, et al. 2008. Decreasing 27. McCluggage WG. 2006. My approach to the interpretation of incidence of postcesarean endometritis with extended-spectrum endometrial biopsies and curettings. J Clin Pathol. 59: 801-12. antibiotic prophylaxis. Obstet Gynecol. 111: 51-6. 28. Smith M, Hagerty K, Skipper B, Bocklage T. 2009. Chronic 12. Cicinelli E, De Ziegler D, Nicoletti R, et al. 2008. Chronic endomteritis: a combine histopathologic and clinical review of endometritis: correlation among hysteroscopic, histologic, and cases from 2002 to 2007. Int J Gynecol. 29: 44-50. bacteriologic findings in a prospective trial with 2,190 consecutive 29. Edis, AW. 1878. On chronic cervical endometritis as a frequently office hysteroscopies. Fertil Steril. 89: 677-84. overlooked cause of sterility and abortion. Br Med J. 2: 717-8. 13. Monif GR. 1986. Short-term failure of IUD removal to alter 30. Oliviera FG, Abdelmassih VG, Diamond MP, et al. 2003. bacterial flora in a patient with chronic anaerobic endometritis. Uterine cavity findings and hsyteroscopic interventions in patients Am J Reprod Immunol Microbiol. 12: 55-7. undergoing in vitro fertilization embryo transfer who repeatedly 14. Yamagishi, Y, Mikamo H, Tanaka K, Watanabe K. 2010. A case cannot conceive. Fertil Steril. 80: 1371-5. of uterine endometritis caused by Atopobium vaginae. J Infect 31. Polisseni F, Bambirra EA, Camargos AF. 2003. Detection of Chemother. 17: 119-21 chronic endometritis by diagnostic hysteroscopy in asymptomatic 15. Andrews WW, Goldenberg RL, Hauth JC, et al. 2005. infertile patients. Gynecol Obstet Invest. 55: 205-10. Endometrial microbial colonization and plasma cell endometritis 32. Romero R, Espinoza J, Mazor M. 2004. Can endometrial after spontaneous or indicated preterm after spontaneous or infection/inflammation explain implantation failure, spontaneous indicated preterm versus term delivery. AM J Obstet Gynecol. abortion and after in vitro fertilization? Fertil Steril. 193: 739-45. 82: 799-804. 16. Moller BR, Kristiansen FV, Thorsen P, et al. 1995. Sterility of 33. Johnston-MacAnanny EB, Hartnett J, Engmann LL, et al. the uterine cavity. Acta Obstet Gynecol Scand. 74: 216-9. 2010. Chronic endometritis is a frequent finding in women with 17. Gibbs RS, Blanco JD, Bernstein S. 1985. Role of aerobic gram- recurrent implantation failure after in vitro fertilization. Fertil Steril. negative bacilli in endometritis after cesarean section. Rev Infect 93: 437-41. Dis. 7Suppl 4: S690-5. 34. Barash A, Dekel N, Fieldust S, et al. 2003. Local injury to the 18. Cohen CR, Manhart LE, Bukusi EA, et al. 2002. Association endometrium doubles the incidence of successful in between Mycoplasma genitalium and acute endometritis. Lancet. patients undergoing in vitro fertilization. Fertil Steril. 79: 1317-22. 359: 765-6. 35. Raziel A, Schachter M, Strassburger D, et al. 2007. Favorable 19. Haggerty CL, Totten PA, Astete SG, Ness RB. 2006. influence of local injury to the endometrium in intracytoplasmic Mycoplasma genitalium among women with nongonococcal, sperm injection patients with high-order implantations failure. nonchlamydia pelvic inflammatory disease. Infect Dis Obstet Fertil Steril. 87: 198-201. Gynecol. 2006: 30184. 36. Cicinelli, W, De Ziegler N, Tinelli R, et al. 2009. Poor reliability 20. Haggerty CL. 2008. Evidence for a role in Mycoplasma genitalium of vaginal and endocervical cultures for evaluating microbiology of in pelvic inflammatory disease. Curr Opin Infect Dis 21: 65-9. endometrial cavity in women with chronic endometritis. Gynecol 21. Martens MG, Faro S, Maccato M, et al. 1991. Susceptibility of Obstet Invest. 68: 108-15. female pelvic pathogens to oral antibiotic agents in patients who 37. Lambert B, Gonthier M, Dery J-P, Lepage, Y. 1998. Compared develop postpartum endometritis. Am J Obstet Gynecol. 164: randomized roles and pain factor by Vabra and Wallach Endocell 1383-6. in endometrial evaluation. Gynecol and Obstet Invest. 45: 258-61. 22. Faro, S. 1988. Infectious disease relations to cesarean section. 38. Wallach Surgical. The Wallach Endocell™: Endometrial Sampling Obstet Gynecol Clin North Am. 15: 685-95. with Simplicity, Safety and Economy. Accessed February 8, 2011. 23. Andrews WW, Shah SR, Goldenberg RL, et al. 1995. Association http://www.wallachsurgical.com/ Products/Single-Use-Products. of post-Cesarean delivery endometritis with colonization of the aspx?ApplicationId=10. chorioamnion by Ureaplasma urealyticum. Obstet Gynecol. 85: 39. 5 Minute Consult Clinical Decision Support. 2008. Endometrial 509-14. biopsy. Accessed February 8, 2011. http://5minuteconsult.com/ 24. Andrews WW, Hauth JC, Cliver SP, et al. 2006. Association popup.aspx?aid=1508599&printTopic=true. of asymptomatic bacterial vaginosis with endometrial microbial colonization and plasma cell endometritis in nonpregnant women. Am J Obstet Gynecol. 195: 1611-6. 25. Krohn MA, Hillier SL, and Baker SJ. 1999. Maternal peripartum complications associated with vaginal group B Streptococci colonization. JID. 179: 1410-5.

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