Endometritis: The clinical-pathologic syndrome

doi:10.1067/mob.2002.121728

American Journal of Obstetrics and Gynecology

Volume 186, Issue 4, April 2002, Pages 690-695

https://doi.org/10.1067/mob.2002.121728 Get rights and content

Abstract

Objective: The purpose of this study was to evaluate histologically proved endometritis as a clinical syndrome that is distinct from laparoscopically confirmed salpingitis. Study design: This was a cross-sectional study of 152 women in an urban hospital with a suspected pelvic inflammatory disease. All women provided a standardized medical history and underwent physical examination, endometrial biopsy, and laparoscopy. We defined endometritis by the presence of plasma cells in endometrial stroma and neutrophils in the endometrial epithelium. Results: Of 152 women who were enrolled, 43 women had neither endometritis nor salpingitis; 26 women had endometritis alone without salpingitis, and 83 women had salpingitis. Those women with endometritis alone more often had douched recently, had a current intrauterine device, and were in menstrual cycle day 1 to 7, compared with women with no endometritis or salpingitis (P = .007, .04, .005, respectively) or women with acute salpingitis (P = .03, .01, .02, respectively). Infection with Neisseria gonorrhoeae and/or Chlamydia trachomatis was found more frequently in women with endometritis alone than in women with no endometritis or salpingitis (P < .001) and less frequently than in women with salpingitis (P = .05). Lower quadrant, adnexal, cervical motion, rebound tenderness, peritonitis, tenderness score, fever, and laboratory abnormalities that indicated inflammation and detection of gonorrheal or chlamydial infection were significantly less common in women with endometritis alone than in women with salpingitis but were somewhat more common in women with endometritis alone than among women with no salpingitis or endometritis. Conclusion: Among women with suspected pelvic inflammatory disease, the histopathologic manifestations of endometritis were associated with clinical manifestations, infection, and specific risk factors that were intermediate in frequency between women with salpingitis and women with neither endometritis nor salpingitis. (Am J Obstet Gynecol 2002;186:690-5.)

Section snippets

Patient population

As previously described,⁵152 women with clinically suspected PID when examined in the emergency department, women's clinic, or sexually transmitted diseases clinic at Harborview Medical Center from 1984 to 1988 were enrolled into this study of the cause, pathogenesis, and therapy of acute PID. Inclusion criteria for suspected PID were based on lower abdominal pain of ≤3 weeks and abnormal adnexal tenderness on pelvic examination. Exclusion criteria included pregnancy, age of <15 years,

Results

Of 152 women with suspected PID who underwent laparoscopy, 43 women (28%) had neither endometritis nor salpingitis; 26 women (17%) had endometritis alone, and 83 women (55%) had salpingitis. Of the 83 women with salpingitis, 8 women did not undergo endometrial biopsy; 64 of the remaining 75 women (85%) had histologic evidence of endometritis.

Comment

In this study of 152 women with clinically suspected PID, 26 women had histologic manifestations of endometritis without laparoscopic evidence of acute salpingitis. To our knowledge, this is 1 of the largest published studies of women with suspected PID with concurrent endometrial histologic evidence and laparoscopic results, which allowed the women to be stratified into 3 groups: women without evidence of upper genital tract inflammation, women with endometritis alone, and women with

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Chronic endometritis impairs embryo implantation in patients with repeated implantation failure: A retrospective study
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To assess whether chronic endometritis (CE) affects embryo implantation in patients with repeated implantation failure (RIF).
We retrospectively analyzed 126 RIF patients who were never diagnosed with CE and received no prior antibiotic therapy. Endometrial specimens obtained by endometrial scratching during mid-luteal phase were immunostained by CD138, a hallmark plasmacyte marker, to identify CE. Pregnancy outcome in RIF patients who underwent IVF-ET frozen-embryo within transfers 6 months after endometrial scratching was compared between women with and without CE.
The prevalence of CE in patients with RIF was found to be 11.9% (15/126). Moreover, a significantly reduced clinical pregnancy rate was observed in RIF patients with CE (20% vs. 46.85%; p = 0.04). The live birth rate also exhibited a decreasing trend in RIF patients with CE, although there was no statistically significant difference (20% vs. 41.58%; p = 0.109).
CE may be involved in the failure of embryo implantation and reduced clinical pregnancy outcome in patients with RIF.
A practical guide to the evaluation of benign endometrial conditions in biopsy and curettage material
2022, Diagnostic Histopathology
Citation Excerpt :
Even more concerning is the wide variation in the management of chronic endometritis by gynecologists and obstetricians, also described by Margulies et al52 This survey revealed a wide spectrum of deficiencies in the understanding of the pathophysiology of chronic endometritis and the diagnostic methodologies applicable to this disease. While evidence-based, or at least consensus-based recommendations on the diagnostic criteria for chronic endometritis emerge, I make the diagnosis of chronic endometritis using the following (admittedly arbitrary and low-threshold) criteria (Figure 12): 1) two or more plasma cells in an otherwise unremarkable endometrium, or 2) one or more plasma cells in association with fibrotic or edematous stroma and/or mucinous or tubal glandular metaplasia.39,53 Lymphocyte aggregates and eosinophils, by themselves, are not sufficient for the diagnosis, but often accompany plasma cells in cases of chronic endometritis.54
Sampling of the endometrium, via biopsy or dilation and curettage, is an important diagnostic tool in a wide variety of clinical scenarios, ranging from infertility and abnormal uterine bleeding to cancer surveillance in high-risk populations. This review describes the most common methods for endometrial sampling used currently and discusses the issue of specimen adequacy from an evidence-based perspective. It also focuses on select benign conditions involving the endometrium in the setting of abnormal uterine bleeding, ranging from anatomic/structural lesions to patterns indicative of a dysfunctional menstrual cycle. The topic of endometrial sampling evaluation in the context of recurrent pregnancy loss is also discussed, with insights on documentation of endometrial changes during the ovulatory phase and the diagnosis of endometritis.
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
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To investigate the therapeutic effect of antibiotic treatment on pregnancy outcomes in the following frozen-thawed embryo transfer cycles of infertile women.
Retrospective study.
University assisted reproduction unit.
A total of 640 women were included. Among them, the number of CD138+ cells per high-power field (CD138+/HPF) in the endometrium at the first evaluation was 0 in 88 women; 315 women had 1–4 CD138+/HPF and the remaining 237 had ≥5 CD138+/HPF. Finally, 26 of 237 women had persistent chronic endometritis (PCE) diagnosed.
Hysteroscopy and endometrial biopsy were performed in the proliferative phase. After antibiotic treatment, endometrial biopsy samples were collected again.
Live birth rate.
No significant difference in pregnancy outcomes was found between women with CD138+/HPF = 0 and those with CD138+/HPF 1–4. The cure rate was 89.0% in women with CD138+/HPF ≥5 after treatment. The implantation rate (51.6% vs. 32.3%, relative risk [RR] 2.23, 95% confidence interval [CI] 1.07–4.66), clinical pregnancy rate (65.7% vs. 42.3%, RR 2.62, 95% CI 1.17–5.86), live birth rate (52.1% vs. 30.7%, RR 2.45, 95% CI 1.04–5.76), and cumulative live birth rate (64.2% vs. 38.5%, RR 2.88, 95% CI 1.27–6.51) were all significantly higher in women with CD138+/HPF ≤4 than in women with PCE.
CD138+/HPF ≤4 in the endometrium had no negative impact on pregnancy outcomes. Antibiotic treatment was an effective way to improve the reproductive outcomes of women with CD138+/HPF ≥5. PCE was associated with poorer pregnancy outcomes.
Impacto del tratamiento antibiótico por vía oral de la endometritis crónica sobre los resultados de embarazo durante el siguiente ciclo de transferencia embrionaria de congelados en mujeres infértiles: un estudio de cohortes de 640 ciclos de transferencia embrionaria.
Investigar el efecto terapéutico del tratamiento antibiótico sobre los resultados de embarazo durante el siguiente ciclo de transferencia embrionaria de congelados en mujeres infértiles.
Estudio retrospectivo.
Unidad de reproducción asistida universitaria.
Un total de 640 mujeres fueron incluidas. Entre ellas, el número de células CD138+ por campo de gran aumento (CD138+/HPF) en el endometrio durante la primera evaluación fue 0 en 88 mujeres, 315 mujeres tuvieron 1-4 CD138+/HPF y las restantes 237 tuvieron ≥5 CD138+/HPF. Por último, 26 de 237 mujeres fueron diagnosticadas con endometritis crónica persistente (PCE).
Se realizó una histeroscopia y biopsia de endometrio en la fase proliferativa. Después del tratamiento antibiótico, se volvieron a obtener muestras de biopsia.
Tasa de nacidos vivos.
No se halló diferencia significativa en los resultados de embarazo entre mujeres con CD138+/HPF = 0 y aquellas con CD138+/HPF 1-4. La tasa de curación fue 89,0% en mujeres con CD138+/HPF ≥5 tras el tratamiento. La tasa de implantación (51,6% vs 32,3%, riesgo relativo [RR] 2,23, índice de confianza al 95% [CI] 1,07 – 4,66), tasa de embarazo clínico (65,7% vs 42,3%, RR 2,62, 95% CI 1,17–5,86), tasa de nacido vivo (52,1% vs 30,7%, RR 2,45, 95% CI 1,04–5,76), y la tasa acumulativa de nacido vivo (64,2% vs 38,5%, RR 2,88, 95% CI 1,27–6,51) fueron significativamente mayores en mujeres con CD138+/HPF ≤4 que en mujeres con PCE.
CD138+/HPF ≤4 en el endometrio no tuvo un impacto negativo en los resultados de embarazo. El tratamiento antibiótico fue una manera efectiva de mejorar los resultados reproductivos en mujeres con CD138+/HPF ≥5. PCE se asoció con peores resultados de embarazo.
Impact of chronic endometritis in infertility: a SWOT analysis
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Citation Excerpt :
Although immunohistochemical staining for CD138 has been found to improve the sensitivity and accuracy of identifying the plasma cells, the technique is not, however, standardized (Liu et al., 2018). The diagnosis seems to vary depending on the laboratory tests and the quality control used (Torlakivic et al., 2015), the dilution (Kasius et al., 2011; Torlakivic et al., 2015), the incubation time, the temperature, the thickness of endometrial sections, the number and area of sections examined (Adegboyega et al., 2010; Bayer-Garner et al., 2004; Eckert et al., 2002) as well as the menstrual cycle phase in which the biopsy is performed (Punnonen et al., 1989). With respect to the histological diagnosis, the suggestion to include both conventional pathological study and CD138 inmunohistochemical examination is crucial, since there is still a lack of consensus on a universal definition of chronic endometritis.
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.
Nonneoplastic Lesions of the Endometrium
2020, Gynecologic Pathology, Second Edition
This chapter describes the most common benign changes of the endometrium encountered in pathology practice. We present an overview of the histologic appearance of the normal (physiologic) endometrium in reproductive, inactive and gestational states. This is followed by a discussion of the changes seen under exogenous hormonal therapy, as well as the most important anatomic and functional alterations of the endometrium. The chapter concludes with the topic of endometrial metaplasia, and the criteria used for the distinction between benign and pre-malignant / malignant in the setting of endometrial metaplastic change.
Genital Chlamydia infection in hyperlipidemic mouse models exacerbates atherosclerosis
2019, Atherosclerosis
Atherosclerosis is a chronic inflammatory disease, and recent studies have shown that infection at remote sites can contribute to the progression of atherosclerosis in hyperlipidemic mouse models. In this report, we tested the hypothesis that genital Chlamydia infection could accelerate the onset and progression of atherosclerosis.
Apolipoprotein E (Apoe^−/−) and LDL receptor knockout (Ldlr^−/−) mice on a high-fat diet were infected intra-vaginally with Chlamydia muridarum. Atherosclerotic lesions on the aortic sinuses and in the descending aorta were assessed at 8-weeks post-infection. Systemic, macrophage, and vascular site inflammatory responses were assessed and quantified.
Compared to the uninfected groups, infected Apoe^−/− and Ldlr^−/− mice developed significantly more atherosclerotic lesions in the aortic sinus and in the descending aorta. Increased lesions were associated with higher circulating levels of serum amyloid A-1, IL-1β, TNF-α, and increased VCAM-1 expression in the aortic sinus, suggesting an association with inflammatory responses observed during C. muridarum infection. Genital infection courses were similar in Apoe^−/−, Ldlr^−/−, and wild type mice. Further, Apoe^−/− mice developed severe uterine pathology with increased dilatations. Apoe-deficiency also augmented cytokine/chemokine response in C. muridarum infected macrophages, suggesting that the difference in macrophage response could have contributed to the genital pathology in Apoe^−/− mice.
Overall, these studies demonstrate that genital Chlamydia infection exacerbates atherosclerotic lesions in hyperlipidemic mouse and suggest a novel role for Apoe in full recovery of uterine anatomy after chlamydial infection.

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^☆: Supported by National Institutes of Health grant No. AI 12192 and training grant No. AI 07140.

^☆☆: Reprint requests: Linda O. Eckert, MD, Assistant Professor, Department of Obstetrics and Gynecology, University of Washington, Box 359865, 325 9th Ave, Seattle, WA 98104-2499.

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American Journal of Obstetrics and Gynecology

Abstract

Section snippets

Patient population

Results

Comment

References (21)

Objectivized diagnosis of acute pelvic inflammatory disease: diagnostic and prognostic value of routine laparoscopy

Am J Obstet Gynecol

Role of bacterial vaginosis-associated microorganisms in endometritis

Am J Obstet Gynecol

Acute pelvic inflammatory disease: associations of clinical and laboratory findings with laparoscopic findings

Obstet Gynecol

Diagnosis and clinical manifestation of bacterial vaginosis

Am J Obstet Gynecol

Risk factors for plasma cell endometritis among women with cervical Neisseria gonorrhoeae , cervical Chlamydia trachomatis , or bacterial vaginosis

Am J Obstet Gynecol

Pelvic inflammatory disease with intrauterine device use: a reassessment

Fertil Steril

Histopathology of endocervical infection caused by Chlamydia trachomatis , herpes simplex virus, Trichomonas vaginalis , and Neisseria gonorrhoeae

Hum Pathol

Microbiological and histopathological findings in acute pelvic inflammatory disease

Br J Obstet Gynaecol

Microbial causes of proven pelvic inflammatory disease and efficacy of clindamycin and tobramycin

Ann Intern Med

Endometrial histopathology in patients with culture-proved upper genital tract infection and laparoscopically diagnosed acute salpingitis

Am J Surg Pathol

Cited by (89)

Chronic endometritis impairs embryo implantation in patients with repeated implantation failure: A retrospective study

A practical guide to the evaluation of benign endometrial conditions in biopsy and curettage material

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

Impact of chronic endometritis in infertility: a SWOT analysis

Nonneoplastic Lesions of the Endometrium

Genital Chlamydia infection in hyperlipidemic mouse models exacerbates atherosclerosis

General Obstetrics and Gynecology: GynecologyEndometritis: The clinical-pathologic syndrome☆,☆☆

Abstract

Section snippets

Patient population

Results

Comment

Am J Obstet Gynecol

Am J Obstet Gynecol

Obstet Gynecol

Am J Obstet Gynecol

Am J Obstet Gynecol

Fertil Steril

Hum Pathol

Microbiological and histopathological findings in acute pelvic inflammatory disease

Br J Obstet Gynaecol

Microbial causes of proven pelvic inflammatory disease and efficacy of clindamycin and tobramycin

Ann Intern Med

Endometrial histopathology in patients with culture-proved upper genital tract infection and laparoscopically diagnosed acute salpingitis

Am J Surg Pathol

General Obstetrics and Gynecology: Gynecology
Endometritis: The clinical-pathologic syndrome☆,☆☆