Microbiological and histopathological findings in acute pelvic inflammatory disease

Upper genital tract infection was investigated in 45 women admitted to hospital for suspected acute pelvic inflammatory disease (PID). Salpingitis was diagnosed by laparoscopy in 30 (67%) women. Histopathological evidence of endometritis was found significantly more often in the 30 women with salpingitis (87%) than in the other 15 women without salpingitis (33%). C. trachomatis or N. gonorrhoeae, or both, were isolated from the upper genital tract in 14 of the 31 women who had both salpingitis and endometritis or endometritis only but in none of the four women who had salpingitis alone and in none of the 10 women who had no evidence of PID. Bacterial vaginosis was associated with histopathological evidence of upper tract infection. Non-chlamydial non-gonococcal organisms were frequently isolated from the upper genital tract. No organisms were isolated from the upper genital tract from 9 of 35 women with laparoscopic or histopathological evidence of PID compared with 7 of 10 women without evidence of PID. C. trachomatis or N. gonorrhoeae in the endometrium was associated with lymphoid follicles comprising transformed lymphocytes, and correlated with the density of plasma cells on biopsy. The microbiological results support the recommendations of broad spectrum antimicrobial therapy for PID.     

Recovery of Chlamydia trachomatis from the endometrium of women at risk for chlamydial infection

Chlamydia trachomatis is the most common sexually transmitted disease in Western Society today and is a major cause of salpingitis and tubal infertility. However, the frequency with which it produces upper genital tract infection in asymptomatic women has not been determined. Endometrial, endocervical, and urethral cultures for C. trachomatis were obtained from 60 women who were at risk for chlamydial infection but who did not have evidence of endometritis or salpingitis on physical examination. Chlamydia was isolated from the lower genitourinary tract in 26 (43%) and from the endometrium in 12 (20%). Thus 12 of 29 (41%) women infected with C. trachomatis had endometrial infections. Upper genital infections appear to be common in women at risk for chlamydial infection, and spread to the upper tract may occur shortly after the infection is acquired.     

Microbial etiology of urban emergency department acute salpingitis: treatment with ofloxacin.

OBJECTIVES: We attempted to define the microbiologic characteristics of acute salpingitis in women presenting to an urban emergency department with pelvic inflammatory disease and to determine the effectiveness of ofloxacin in treating this disease. STUDY DESIGN: Women with pelvic inflammatory disease underwent laparoscopy to confirm the diagnosis and to culture the fallopian tubes and cul-de-sac. All patients (n = 36) were treated with parenteral ofloxacin and discharged on a regimen of oral ofloxacin to complete a 10- to 14-day course. RESULTS: Neisseria gonorrhoeae was isolated from at least one site in 25 patients (69.4%) including the fallopian tube or cul-de-sac in 12 of them. Chlamydia trachomatis was isolated from the endocervix and/or endometrium in 6 patients (16.7%); concomitant Neisseria gonorrhoeae was present in 4 patients (66.6%). A polymicrobial infection was identified in only one patient. All patients responded to antibiotic therapy with ofloxacin. CONCLUSIONS: Acute salpingitis in our urban emergency department population is related primarily to upper genital tract infection with Neisseria gonorrhoeae. Ofloxacin is effective therapy for this disease.     

Performance of clinical and laparoscopic criteria for the diagnosis of upper genital tract infection

Objective: The purpose of this study was to validate the standard minimal clinical criteria and the laparoscopic triad of tubal edema, erythema, and purulent exudate used to diagnose acute upper genital tract infection.Methods: Subjects included women who either met the Centers for Disease Control and Prevention's (CDC) minimal criteria for acute pelvic inflammatory disease or had other signs of upper genital tract infection (i.e., atypical pelvic pain, abnormal uterine bleeding, or cervicitis). The subjects were evaluated with a baseline interview comprehensive laboratory testing, and either an endometrial biopsy or laparoscopy with endometrial and fimbrial biopsies for definitive diagnosis of upper genital tract infection. Patients were considered positive for upper genital tract infection if they had any of the following findings: 1) histologic evidence of endometritis or salpingitis; 2) laparoscopic visualization of purulent exudate in the pelvis without another source; or 3) positive testing for Neisseria gonorrhoeae or Chlamydia trachomatis from the endometrium, fallopian tubes, or pelvis.Results: One hundred twenty-nine women with adequate endometrial samples were evaluated between August 1993 and September 1997, and 62 had complete laparoscopic evaluations. The sensitivities of the CDC's minimal clinical criteria for pelvic inflammatory disease and the laparoscopic triad of edema, erythema, and purulent exudate were 65% and 60%, respectively.Conclusions: Commonly used minimal clinical criteria for pelvic inflammatory disease and the laparoscopic triad of tubal edema, erythema, and purulent exudate have limited sensitivity with correspondingly high false negative rates.     

In vivo tumor necrosis factor production in women with salpingitis.

Immune mediated mechanisms might contribute to damage of the fallopian tube in instances of salpingitis. Using a filter paper technique to obtain samples during the surgical procedure, we examined fluids from the reproductive tract organs of seven women with salpingitis and five controls, for evidence of tumor necrosis factor (TNF). TNF, produced principally by macrophages, is a substantial mediator of inflammatory responses. In three women culture-positive for Chlamydia trachomatis, TNF was identified only in those fallopian tubes with visual evidence of disease. Fluids obtained from morphologically normal tubes, as well as from the ovaries and uterus, were negative. In three women with negative fallopian tube cultures but visual evidence of salpingitis, TNF was also identified in fluids from damaged, but not from normal, tubes. Ovarian and uterine fluids of the women were also TNF positive. The last patient, also culture-negative, had TNF only in one affected tube. All five patients in the control group had negative findings at all genital tract sites. Only one patient had TNF in her serum. Thus, localized cell-mediated immune system activation, identified by TNF production, appears to be a typical component of salpingitis.     

Laparoscopy in women with chlamydial infection and pelvic pain: a comparison of patients with and without salpingitis

A review was made of clinical and laboratory findings in 104 women who, during 1978 to 1981, were subjected to laparoscopy because of symptoms suggestive of acute salpingitis, and who harbored Chlamydia trachomatis but not Neisseria gonorrhoeae in the genital tract. The patients with acute salpingitis (N = 76) did not differ significantly from those with visually normal fallopian tubes (N = 28) in regard to age distribution, parity, contraceptive method used, proportion of women with urethritis symptoms, increased vaginal discharge, vomiting, diarrhea, elevated rectal temperature, elevated white blood cell count, and palpable pelvic masses. The acute salpingitis patients more often had irregular bleeding and an elevated erythrocyte sedimentation rate, whereas the patients without acute salpingitis more often had a short history of pelvic pain. The two groups overlapped considerably with respect to the number of symptoms and clinical signs of pelvic infection. The results emphasize the value of laparoscopy in the diagnosis or exclusion of a tubal infection in association with a chlamydial genital infection and pelvic pain, even if there are comparatively few additional symptoms of ascending infection.     

Hormonal and barrier contraception and risk of upper genital tract disease in the PID Evaluation and Clinical Health (PEACH) study

OBJECTIVE: Among women diagnosed with pelvic inflammatory disease, we examined the associations between hormonal or barrier methods of contraception and upper genital tract infection or inflammation. METHODS: Participants were 563 patients from a treatment trial for pelvic inflammatory disease. All had pelvic pain; pelvic organ tenderness; and leukorrhea, mucopurulent cervicitis, or untreated cervicitis. Contraceptive use within the prior 4 weeks was compared among women with baseline upper genital tract gonorrhea or chlamydia, women with endometritis without upper genital tract gonorrhea or chlamydia, and women with neither upper genital tract gonorrhea or chlamydia nor endometritis. RESULTS: Inconsistent condom use was significantly and independently associated with a 2 to 3 times elevated risk for upper genital tract infection. Upper genital tract gonorrhea or chlamydia was not significantly associated with use of oral contraceptives, use of medroxyprogesterone, condoms used consistently, nor other barrier methods. CONCLUSION: No hormonal or barrier contraceptive method was related to a reduction in upper genital tract disease among women with clinical pelvic inflammatory diseases.     

Recovery of Chlamydia trachomatis from the endometrium in infertile women with serum antichlamydial antibodies

Upper genital tract infection with Chlamydia trachomatis appears to be a frequent cause of salpingitis and tubal infertility. However, the prevalence of active infection in women with infertility has not been well-defined. To examine this question, endocervical and endometrial cultures for C. trachomatis were obtained from infertile women with serum antibodies to C. trachomatis. The first 19 consecutive patients with titers greater than or equal to 1/32 were cultured. C. trachomatis was recovered from the endometrium or endocervix in six (32%) of the women examined and from the endometrium in five (26%). These findings indicate that a significant portion of infertile women with serum antichlamydial antibodies may have active upper genital tract infection with C. trachomatis at the time of presentation.     

Localization of Chlamydia trachomatis infection by direct immunofluorescence and culture in pelvic inflammatory disease

Fifty-five women with suspected pelvic inflammatory disease underwent diagnostic laparoscopy and endometrial and tubal biopsy, with specimens for isolation of Chlamydia trachomatis and for staining with a species-specific monoclonal fluorescein-conjugated antibody to C. trachomatis were obtained from the urethra, rectum, endocervix, endometrium, tubes, and cul-de-sac. C. trachomatis was isolated from 21 patients (38%), including 10 (18%) who had positive endometrial or tubal cultures. The fluorescein-conjugated antibody stain was positive for 43 (86%) of 50 culture-positive specimens, for 14 (18%) of 78 culture-negative specimens from 21 patients who had positive cultures from other sites, and for one (0.5%) of 192 specimens from 34 patients who had negative cultures at all sites. Thus the sensitivity of direct fluorescein-conjugated antibody for culture-positive specimens was 86% and the specificity for specimens from culture-negative patients was 99%. Twelve upper genital tract specimens were positive by fluorescein-conjugated antibody only. Fluorescein-conjugated antibody staining of 50 paraffin-embedded endometrial aspirates showed extracellular or intracellular elementary bodies and or cytoplasmic inclusions in all of seven culture-positive specimens, in four of six culture-negative specimens from patients who had positive cultures at other sites, and in none of 34 specimens from patients with negative cultures. Thus fluorescein-conjugated antibody staining is useful for confirming the role of C. trachomatis in endometritis and salpingitis. It is more sensitive than culture for detection of chlamydia in endometrial or tubal specimens and is able to confirm that the organism is actually present in endometrial tissue (rather than simply reflecting contamination from the cervix) in women with clinical evidence of pelvic inflammatory disease.     

Microbiologic study of chronic inflammation associated with tubal factor infertility: role of Chlamydia trachomatis

One hundred sixty-one women undergoing laparoscopy for infertility of obstructive origin (fallopian tube stenosis or obstruction and periadnexal adhesions) had thorough bacteriologic studies, including Chlamydia trachomatis cultures, of their lower and upper genital tracts. Peritoneal or tubal fluid cytologic features and biopsies of fallopian tubes or adhesions were also studied after each laparoscopy. The serum of each woman was titrated for evidence of C. trachomatis infection. The sera of a control group of 51 women with ovarian infertility but normal fallopian tubes according to laparoscopy and hysterosalpingogram were titrated in an identical manner. The current study confirms previous studies that showed a strong correlation between infertility due to fallopian tube factors and positive C. trachomatis cultures or serologic studies. The current study suggests that C. trachomatis infection does not correlate with a past history of salpingitis or pelvic pain, but that current C. trachomatis infection, as assessed by positive culture, does correlate with gross and histologic evidence of chronic inflammation.     

Early postpartum endometritis: the role of bacteria, genital mycoplasmas, and Chlamydia trachomatis

To characterize the flora of early postpartum endometritis and the clinical features of women with specific organisms, endometrial cultures for facultative and anaerobic bacteria, genital mycoplasmas, and Chlamydia trachomatis were taken with a triple-lumen sampling device. More than one organism was recovered from 80% of the women. Over 60% of the women had Gardnerella vaginalis and/or anaerobes associated with bacterial vaginosis isolated from the endometrium; these women were more likely to have severe illness and to develop a wound infection than were other women. Genital mycoplasmas were isolated frequently, but specific antibiotic therapy was not required for clinical cure in the 10% of patients who had Ureaplasma urealyticum only. Chlamydia trachomatis was infrequently isolated, but C trachomatis commonly remained after therapy.     

Microbiology and pathogenesis of acute salpingitis as determined by laparoscopy: What is the appropriate site to sample?

Acute salpingitis is a polymicrobial disease. Neisseria gonorrhoeae and anaerobic gram-positive cocci were the predominant microorganisms isolated from the fallopian tubes of salpingitis patients. Gonococci were isolated from the fallopian tubes in eight of 35 (23%) patients; anaerobic bacteria were recovered from 10 of 35 (28.5%). Although Chlamydia trachomatis was not recovered from the fallopian tube exudate, there was abundant serologic evidence of chlamydial infection in the salpingitis patients. Twenty-three percent of patients with paired sera had a fourfold rise in IgM and IgG titer, which was consistent with systemic chlamydial infection. Comparison of cultures obtained via laparoscopy and culdocentesis suggested that culdocentesis is not an accurate reflection of the microbial milieu in the fallopian tube.     

Endometritis: the clinical-pathologic syndrome

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.     

Upper genital tract isolates at delivery as predictors of post-cesarean infections among women receiving antibiotic prophylaxis

The introduction of antibiotic prophylaxis for cesarean delivery has decreased the risk of postpartum endometritis and wound infection, but factors that contribute to prophylaxis failure are not understood. To determine factors that might contribute to postpartum infections following antibiotic prophylaxis, we cultured amniotic fluid, decidua, and chorioamniotic membrane specimens for anaerobic and facultative bacteria and for genital mycoplasmas at cesarean delivery. Women were assessed daily for the development of infections, and if endometritis developed, a protected endometrial culture was obtained. Postpartum endometritis developed in 16 and wound infection in four of 102 women. Infection rates were similar for women receiving cefotetan (N = 50) or cefoxitin (N = 52) for prophylaxis. The isolation of group B streptococcus (P less than .001) or Enterococcus faecalis (P = .03) from the upper genital tract at delivery was significantly associated with postpartum endometritis. Antibiotic-resistant organisms (other than enterococci) were recovered uncommonly at delivery or with postpartum infections. Group B streptococcus was susceptible to the prophylactic agents used, suggesting that virulence factors other than antibiotic resistance are important for the development of postpartum endometritis. Group B streptococcus, E faecalis, and bacteria associated with bacterial vaginosis were recovered from the endometrium at the time of postpartum endometritis.     

Severe pneumococcal peritonitis complicating IUD: case report and review of the literature

A case of pneumococcal peritonitis associated with an IUD is presented and four previously reported cases of pneumococcal peritonitis with IUD are reviewed. The infection may occur in previously healthy women who were fitted with an IUD, possibly by ascending infection from the genital tract via the fallopian tubes. The condition is usually accompanied by bilateral salpingitis and may be severe, with fatal outcome. We suggest that any woman over 30 using an IUD, who presents with peritonitis without obvious cause, should be given antibiotics with activity against Streptococcus pneumoniae, following removal of the IUD.     

Vaginal polymorphonuclear leukocytes and bacterial vaginosis as markers for histologic endometritis among women without symptoms of pelvic inflammatory disease

OBJECTIVE: The study was performed to determine whether vaginal polymorphonuclear leukocytes can be used as predictors of histologic endometritis among women at risk for, but without symptoms of, acute pelvic inflammatory disease. STUDY DESIGN: Five hundred thirty-seven women with, or at risk for, pelvic infection underwent pelvic examinations, including endometrial biopsies. These women were assessed for the presence of vaginal polymorphonuclear leukocytes, bacterial vaginosis, sexually transmitted diseases, and histologic endometritis. RESULTS: Vaginal neutrophils were present in 240 (44.7%) and histologic endometritis was present in 77 (14.3%) of the study population. Women with histologic endometritis were significantly more likely to have vaginal neutrophils present, with an odds ratio of 3.2 (95% CI 1.9-5.7). When study subjects were stratified by the presence of sexually transmitted diseases and vaginal neutrophils, the prevalence of histologic endometritis was highest in women with both conditions present, with an odds ratio of 7.0 (95% CI 3.5-14.3). When subjects were stratified by the presence of bacterial vaginosis and vaginal neutrophils, the prevalence of histologic endometritis was again highest in women with both conditions present, with an odds ratio of 4.8 (95% CI 1.4-16.3). The presence of vaginal neutrophils diagnosed by saline wet mount had a high sensitivity (90.9%) and negative predictive value (94.5%), but a low specificity (26.3%) and positive predictive value (17.1%) for the diagnosis of upper genital tract infection. CONCLUSION: The presence of vaginal polymorphonuclear leukocytes has a high sensitivity and negative predictive value for the diagnosis of upper genital tract infection.     

Haemophilus influenzae causes purulent salpingitis

We describe two patients with laparoscopically diagnosed, severe acute salpingitis who had nontypable Haemophilus influenzae isolated directly from the fallopian tubes. Nontypable H. influenzae should be recognized as an important genital pathogen.     

Periappendicitis and chlamydial salpingitis

Periappendicitis seems to be a novel manifestation of infections with Chlamydia trachomatis. In seven of 112 women with laparoscopically verified acute salpingitis, secondary appendicitis was diagnosed and histologically confirmed. The genital tract in all seven patients harbored Chlamydia trachomatis but not Neisseria gonorrhoeae. The fallopian tubes should be scrutinized when an inflamed appendix is removed from a sexually active woman. Signs of salpingitis should then lead to appropriate microbiologic, therapeutic and epidemiologic measures, including contact tracing.     

The association of asymptomatic bacterial vaginosis with upper genital tract infection

Objective: To determine whether asymptomatic bacterial vaginosis (BV) is associated with upper genital tract inflammation or bacterial colonization.Methods: Fifty nonpregnant women with intact uteri who planned to undergo gynecologic surgery and had no recent symptoms of vaginal infection were enrolled. We obtained a vaginal swab for Gram stain, endocervical swab for chlamydia and gonorrhea DNA probe testing, and Pipelle endometrial biopsy for aerobic and anaerobic cultures and histology. We correlated surgical findings and histology of available surgical specimens with the microbiologic results. The diagnosis of BV was made according to Speigel’s criteria. Bacteria isolated from the uterus were classified as high virulence versus low virulence. Contingency tables were analyzed using the chi-square or Fisher Exact tests.Results: Twenty-one of 50 patients had BV on Gram stain, 3 had intermediate BV, and 3 had unreadable slides. Eleven patients had histologic endometritis, including 7 of the 21 with BV. The association between BV and endometritis was not statistically significant. Thirty-eight patients had a positive endometrial culture; 18 of these also had BV and 3 had intermediate BV. Of patients with a positive endometrial culture, isolates from those who also had BV or intermediate BV were more likely to be highly virulent pathogens compared to those who tested negative for BV (P < .05). No patients had positive gonorrhea or chlamydia tests. Of the 37 patients who underwent abdominal surgery, 20 had visible adhesions. The association between adhesions and endometritis, BV, or positive endometrial cultures was not significant.Conclusion: Patients with asymptomatic BV are more likely than patients without BV to have highly virulent bacteria isolated from the endometrium. BV may predispose to upper genital tract infection.     

Lower genital tract infection and endometritis: insight into subclinical pelvic inflammatory disease

OBJECTIVE: To investigate the association between lower genital tract infections and subclinical PID. Fallopian tube damage is a common complication of acute symptomatic pelvic inflammatory disease (PID), yet most women with tubal factor infertility do not have a history of acute PID. Subclinical PID is believed to be an important cause of tubal factor infertility. METHODS: We conducted a cross-sectional study among women attending a sexually transmitted diseases or ambulatory gynecology clinic. A convenience sample of 556 women with bacterial vaginosis, gonorrhea, or chlamydia, or women at risk for gonorrhea or chlamydia were enrolled. Women diagnosed with acute PID were not eligible to participate. The main outcome was subclinical PID, as defined by the presence of histologic endometritis. RESULTS: Subclinical PID was more common in women with lower genital tract infection than in uninfected women. Subclinical PID was present in 27% of women with Chlamydia trachomatis (odds ratio 3.4; 95% confidence interval [CI] 1.8, 6.3) and in 26% of women infected with Neisseria gonorrhoeae (odds ratio 2.4; 95% CI 1.1, 5.1). Among women with bacterial vaginosis, 15% had endometritis (odds ratio 2.7; 95% CI 1.02, 7.2). CONCLUSION: Subclinical PID is common among women with lower genital tract infections. Additional prospective studies are necessary to determine the reproductive impact of these asymptomatic upper genital tract infections.