J Clin Pathol 1985;38:726-732

Chlamydial endometritisJORMA PAAVONEN,* RISTO AINE, KLAUS TEISALA, PENTTI K HEINONEN,REIJO PUNNONEN, MATTI LEHTINEN, ARI MIETTINEN, PAUL GRONROOS

From the Departments ofClinical Sciences and Biomedical Sciences, University of Tampere, and DepartmentsofObstetrics and Gynaecology, Pathology, and Medical Microbiology, University Central Hospital, Tampere,

Finland

SUMMARY Endometrial biopsies were obtained from 32 women with suspected pelvic inflamma-tory disease, of whom 23 (72%) had histopathological evidence of endometritis. Chlamydiatrachomatis was isolated from the endometria of nine (39%) women (chlamydia group) but not

from the other 14 (non-chlamydia group). Severe plasma cell endometritis and lymphoid follicleswith transformed lymphocytes were significantly more common in the chlamydia group than inthe non-chlamydia group. This suggests that C trachomatis is an invasive endometrial pathogenwhich often causes severe inflammation. The association was independent of predisposing factorssuch as use of intrauterine contraceptive devices.

Chlamydia trachomats is the most important causeof acute pelvic inflammatory disease.' Cervicalchlamydial infection ascends intraluminally to theupper genital tract, the endometrium, and fallopiantubes.23 C trachomatis has been directly isolatedfrom the fallopian tubes of women with acute sal-pingitis.' Endometritis as an intermediate state ofsuch ascending chlamydial infection has been littlestudied, and only a few cases of C trachomatisassociated endometritis have been reported.4-8 Thusthe histopathological characteristics of this infectionare largely unknown. We have investigated the his-topathological manifestations of chlamydial andnon-chlamydial endometritis associated with pelvicinflammatory disease.

Material and methods

STUDY POPULATIONThe study population consisted of 32 women seenconsecutively as part of an ongoing study of acutepelvic inflammatory disease at the Department ofObstetrics and Gynaecology, University CentralHospital, Tampere, Finland. Women who had takenantibiotics or those who had undergone gynaeco-logical operations or any investigations of the upper

*Present address: Department of Obstetrics and Gynecology, Uni-versity of Washington, School of Medicine, Harborview MedicalCenter, 325 Ninth Avenue, Seattle, WA 98104, USA.

Accepted for publication 21 February 1985

genital tract within the previous month wereexcluded from the study. Patients were evaluated aspreviously described.9 All patients underwentlaparoscopy and endometrial biopsy after the natureof the procedures had been fully explained andinformed consent obtained.

COLLECTION OF SPECIMENSSpecimens for isolation of C trachomatis, Neisseriagonorrhoeae, Mycoplasma hominis, Urea plasmaurealyticum, herpes simplex virus, and facultativeand anaerobic bacteria were obtained from the cer-vix, endometrium, fallopian tubes, and cul de sac asdescribed previously.'0 Endometrial specimens wereobtained during general anaesthesia by transcervicalaspiration. The cervix was first wiped carefully and asterile disposable fertility cannula (Pro-Ception,Milex Co, USA) was inserted into the endocervicalcanal through the internal os. When the catheter wasin place, the stylet was removed, and a disposablebaby feeding catheter was inserted through the can-nula beyond the internal os until it touched theuterine fundus. A 10 ml syringe was then attachedto the catheter and endometrial material was aspi-rated for isolation of the micro-organisms. A singlestrip endometrial biopsy specimen was obtainedtranscervically using a disposable Vabra (FerrosanCo, Denmark) endometrial suction currette equip-ped with a 3 mm metallic tip. The biopsy specimenswere fixed in 10% buffered formalin and processedby routine histological methods, including staining

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by the method of Herovici." Haematoxylin andeosin, Giemsa, and methyl green pyronin'2 stainingswere also used. Deeper parts of endometrium wereinadequate in four biopsies. In one case theendometrial biopsy specimen was too small forevaluation of all the histopathological variablesused. This patient was excluded from furtheranalysis.

MICROBIOLOGICAL STUDIESC trachomatis was isolated using cycloheximidetreated McCoy cells" and the inclusion bodies werevisualised by iodine. Cultures for N gonorrhoeaewere performed by inoculation of the swabs, initiallytransported in Stuart's media, on to Thayer-Martinagar plates. Oxidase positive colonies wereidentified as N gonorrhoeae by an immunofluores-cence technique using fluorescein isothiocyanateconjugated rabbit anti-N gonorrhoeae antibodies(Difco, USA) .4 Specimens for culture of M hominisand U urealyticum were inoculated into SP-4'5 and10-B'6 media respectively. Subcultures foridentification ofM hominis were performed on SP-4plates, and positive isolation was verified by agrowth inhibition test using discs impregnated withantiserum.'7 Specimens for culture of U urealyticumwere subcultured on differential agar medium A7and identified as described previously.'8 Port-A-Cspecimens for isolation of facultative and anaerotbacteria were handled as described elsewhere.'0Specimens for isolation of herpes simplex virus weplaced in viral transport media (Virocult, OrionDiagnostica, Finland) and inoculated on to humanembryonic fibroblast monolayers.20

HISTOPATHOLOGICAL METHODSThe biopsy specimens were reviewed by one of us

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without knowledge of any clinical or microbiologicalfindings. Standard terms of evaluating his-topathological and cellular findings were used.The histopathological diagnosis of endometritis

was based on identification of plasma cells.2' 22 In allcases the presence of plasma cells was confirmedwith methyl green pyronin staining. The averagenumber of plasma cells was quantitated as 1 + to 3+according to the following scheme: 1+ when fewerthan 20 plasma cells were seen per high power fieldin at least five fields (1+ plasma cells were usuallyseen in superficial parts of the functional endomet-rium); 2+ when 20 to 60 plasma cells were seen perhigh power field; and 3+ when more than 60 plasmacells were seen per high power field. Dense infiltra-tions of lymphocytes-that is, lymphoid follicles-were recorded as present or absent. Lymphoid folli-cles were defined as rounded follicular accumula-tions of large transformed lymphocytes. They wereusually surrounded by dense inflammatory infiltratesof plasma cells. The number of polymorphonuclearleucocytes was quantitated as follows: 1+ when afew were present focally in the superficial parts ofendometrium; 2+ when diffuse infiltrations andfocal collections were seen; and 3+ when larger col-lections and confluent infiltrations were present allover the specimen. The presence or absence offocal polymorphonuclear leucocyte infiltrations ofendometrial glands (microabscesses), tissueoedema, haemorrhagia, necrosis, and fibrosis wasalso recorded.

Endometritis was classified into mild, moderate,and severe. This was based mainly on the number ofplasma cells present, but attention was also paid toassociated inflammatory abnormalities in the func-tional endometrium. In mild endometritis theinflammatory infiltrate was slight and scattered in

Fig. 1 Mild endometritis withslight diffuse plasma cell

.hL fie. <..infitration. Haematoxylin andeosin. x 132.

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the superficial part of oedematous endometrialstroma (Fig. 1) Only focal aggregates of plasma cellswere seen. In moderate endometritis more pro-nounced infiltrations of plasma cells were seenthroughout the specimen (Fig. 2). Lymphocytes andplasma cells were also found in larger focus likeaggregates, which sometimes became confluent. Thedensity of the endometrial stroma was more promi-nent than in mild endometritis. Endometritis wasconsidered severe when pronounced diffuse infiltra-tions of plasma cells were seen all over the biopsyspecimen replacing the endometrial stroma (Fig. 3).Besides plasma cells, other inflammatory cells weremore abundant. Infiltration of endometrial glandsby polymorphonuclear leucocytes was more promi-nent than in moderate endometritis. Lymphoid fol-licular structures were often present within the

inflammatory stromal infiltrate. Because of severeinflammatory changes histopathological dating ofthe endometrium was often impossible.

STATISTICAL ANALYSISAnalysis of variance, Fisher's exact test, and X2 test,where appropriate, were used for statisticalanalyses.

Results

PREVALENCE OF ENDOMETRITISEndometrial biopsy showed endometritis in 23(72%) of the 32 women with suspected pelvicinflammatory disease. Of those 23 women withpathological evidence of endometritis, 19 (83%)had salpingitis at laparoscopy and four (17%) did

Fig. 2 Moderate endometritiswith confluent focus like aggregatesofinflammatory cells.Haematoxylin and eosin. x 66.

Fig. 3 Severe endometritis withpronounced plasma cellinflltration. Haematoxylin andeosin. x 66.

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not. Endometritis was mild in six (26%) cases, mod-erate in six (26%) cases, and severe in 11 (48%)cases. Table 1 shows the correlation of histologicalfindings with selected demographic and clinicalfindings. There were more women with moderateand severe endometritis using intrauterine con-

traceptive devices than those with mild endometritisand they also had longer histories of symptoms.There was a significant correlation between the sev-

erity of endometritis and the acute phase erythro-cyte sedimentation rate.

ISOLATION OF SPECIFIC MICRO-ORGANISMSFROM THE ENDOMETRIUMC trachomatis was the most prevalent organism: itwas isolated from the endometrium of nine womenand from the cervix of 10. Three women had Ctrachomatis isolated from the cervix but not from theendometrium, and two women had C trachomatisisolated from the endometrium but not from thecervix. Three women had C trachomatis isolatedfrom the cervix, endometrium, and fallopian tubes.C trachomatis was the only organism isolated fromthe endometrium in three cases, and in six cases

other organisms were isolated as well (Table 2).N gonorrhoeae was isolated from the endomet-

rium in three cases, M hominis in four cases, U

urealyticum in three cases, herpes simplex virus type

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2 in one case, facultative bacteria (including Strep-tococcus a-haemolyticus, group B streptococcus,Staphylococcus aureus, Haemophilus influenzae) insix cases, and anaerobic bacteria (including Pepto-streptococcus spp, Bacteroides bivius, and Bmelaninogenicus) in seven cases. Since Ctrachomatis was the most prevalent organism iso-lated we divided the cases into two groups accordingto whether or not C trachomatis was isolated fromthe endometrium (Table 2). There was no correla-tion of the isolation of C trachomatis with the isola-tiQn of other specific micro-organisms from theendometrium (Table 2). None in the chlamydiagroup had mycoplasmas isolated.

CORRELATION OF HISTOPATHOLOGICALCHARACTERISTICS OF ENDOMETRITIS WITH THE

ISOLATION OF C TRACHOMA TISTable 3 shows that severe endometritis was

significantly associated with the isolation of Ctrachomatis. Thus seven (87%) of the eight womenwho had C trachomatis isolated from the endomet-rium showed severe endometritis compared withonly four (29%) of the 14 women who did not haveC trachomatis isolated from the endometrium (p =

0.023) (one of the four women with severe

endometritis in the latter group had C trachomatisisolated from the cervix). After adjusting for the

Table 1 Correlation of histopathological findings with selected demographic and clinical findings in 23 women withendometritis

Finding Severity of endometritis

Mild (n = 6) Moderate (n = 6) Severe (n = 11)

Age (yr)* 23 (4) 25 (9) 27 (8)Method of birth control (no (%))

Birth control pills 2 (33) 0(-) 1 (9)Intrauterine contraceptive device 0 (-) 4 (67) 5 (45) 1,tOther 3 (50) 0 (-) 5 (45)None 1(17) 2(33) °(-)

Duration of symptoms (days)* 2-2 (1-0) 10-8 (11-5) 10-5 (7-9)Temperature on admission (°C)* 37-7 (0.9) 37 5 (0-8) 37-2 (0-7)Erythrocyte sedimentation rate (mm in the first hour)* 17 (10) 31 (22) 52 (18)C reactive protein concentration (mg/I)* 48 (52) 57 (69) 69 (34)

*Values given as mean (standard deviation).tp = 0-049 (X2 test).tp = 0 0027 (analysis of variance).

Table 2 Correlation ofthe isolation of Chlamydia trachomatis with the isolation ofother micro-organisms from theendometrial cavities of23 women with plasma cell endometritis

Micro-organism C trachomatis isolated (n = 9) C trachomatis not isolated (n = 14) Total (n = 23)

Neisseria gonorrhoeae 1 (11) 2 (14 3(13)Mycoplasma hominis 0 4 (29 4 (17)Urea plasma urealyticum 0 3 (21 3 (13)Herpes simplex virus type 2 1 (11) 0 1 (4)Facultative bacteria 2 (22 4 (29 6 (26Anaerobic bacteria 4 (44 4 (29) 8 (35)

Values given as number (%) of women.

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Paavonen, Aine, Teisala, Heinonen, Punnonen, Lehtinen, Miettinen, Gronroospresence or absence of an intrauterine contraceptivedevice, the association between pathological evi-dence of severe endometritis and the isolation of Ctrachomatis from the endometrium was even morepronounced (p = 0.0013) among those women whowere not using intrauterine contraceptive devices.The histopathological picture of severe endomet-

ritis was characterised by pronounced diffuseinflammatory infiltrates of plasma cells, and lym-phocytes were seen in the endometrial stromathroughout the biopsy specimen. Lymphoid follicltswith transformed lymphocytes were seen in six(75%) of the eight patients who had positiveendometrial cultures for C trachomatis (one casewith a relatively small biopsy specimen showedsevere inflammation but follicular structures were

not seen) compared with none of those without Ctrachomatis isolated from the endometrium (p =

0-0004). In three cases the lymphoid follicles weresmall and in three cases medium sized or large. Thecells comprising these lymphoid follicles were largeor medium sized transformed lymphocytes withabundant pyronin positivity in the cytoplasm. Starrysky phagocytes were seen infrequently. Denseinfiltrations of plasma cells was usually seen in theperiphery of these lymphoid follicles. Fig. 4 shows atypical lymphoid follicle. No correlation was foundbetween the presence of polymorphonuclearleucocytes and the isolation of C trachomatis (Table2). One patient with chlamydial endometritis hadsmall numbers of eosinophils.Other inflammatory changes such as cytoplasmic

eosinophilia and squamous metaplasia of the surfaceepitheliumn, as well as focal inflammatory infiltra-tions of the endometrial glands (microabscesses),

were more common in severe endometritis, but no

significant differences were found between cases

with or without C trachomatis. Intracytoplasmicinclusions in swollen epithelial cells were seen in onecase with C trachomatis isolated from the endomet-rium.

Fibrous tissue was seen in two (25%) cases inwhich C trachomatis was isolated from the endomet-rium and in four (29%) cases in which C trachomatiswas not isolated. One of the latter four women hadC trachomatis isolated from the cervix.

Neither of the two women with N gonorrhoeaeisolated from the endometrium had lymphoidfollicles present. One had moderate superficialendometritis with 2+ plasma cells, and the otherhad mild diffuse endometritis with 1 + plasma cells.

Epitheloid cell granulomas with necrosis and giantcells of Langhans' type were not seen in any of thespecimens.

Discussion

Endometritis is often an obscure entity to pathol-ogists, although it is commonly seen in uterine curet-tings obtained after abortion and parturition.23Furthermore, histopathological studies among infer-tile patients have shown that endometritis is not anuncommon finding.2' 24 The presence of plasma cellswithin the endometrium is generally accepted as ahistopathological definition of endometritis.22 Thepresence of polymorphonuclear leucocytes and lym-

phocytes are not included because they can also befound during the normal menstrual cycle.

In this study histopathological evidence ofendometritis was found in 72% of 32 patients refer-

Table 3 Correlation ofselected histopathological characteristics ofendometritis with the isolation ofChlamydiatrachomatis from the endometrium

Characteristics of endometritis C trachomatis isolated (n = 8) C trachomatis not isolated (n = 14) p

SeverityMild 0 6 (42)Moderate 1 (13) 4 (29) 0-023Severe 7 (87) 4 (29)

Lymphoid follicles with transformed lymphocytes 6 (75) 0 0 0004Plasma cells+ 0 5(36)+ + 5 (62) 6 (43) NS*+++ 33(38) 3(21)

Polymorphonuclear leucocytes+ 5 (62) 3 (21)t++ 2 (25) 5 (36) NS+ + + 1 (13) 1 (7)

Polymorphonuclear leucocytes in endometrialglands (microabscesses) 3 (38) 3 (21) NS

Fibrosis 2 (25) 4 (29) NSOedema 2 (25) 4 (29) NSNecrosis 2 (25) 3 (21) NSHaemorrhagia 5 (62) 14 (100) NSIntracytoplasmic inclusions 1 (13) 0 NS* NS = not significant.tNot seen in five patients (36%).Values given as number (%) of women.

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Fig. 4 Follicular lymphoidinfitrate comprising transformedlymphocytes. Note thedemarcations which are quiteindistinct (arrows). Haematoxylinand eosin. x 66.

red for acute pelvic inflammatory disease. This pre-valence is relatively high and supports the conceptthat endometritis is associated with non-puerperalpelvic inflammatory disease. Furthermore, it is inagreement with a recent related study which showedpathological evidence of endometritis in 40% of 35patients with mucopurulent cervicitis who did nothave frank pelvic inflammatory disease.2 Theseresults suggest that the pathogenesis of acute salpin-gitis entails intraluminal spread of infection from thecervix via the endometrium to the fallopian tubes.We found that C trachomatis was the most preval-

ent (39%) micro-organism isolated from theendometrium. A previous study by Stray-Pedersenet a!24 implicated mycoplasmas in the aetiology ofendometritis, but they did not control for Ctrachomatis. In the present study none in thechlamydia group had mycoplasmas isolated,whereas in the non-chlamydia group U urealyticumwas isolated from three women and M hominis wasisolated from four. Since C trachomatis was the mostprevalent organism isolated and there were nosignificant differences between those with and thosewithout C trachomatis in the presence of othermicro-organisms, it is conceivable that the his-topathological differences observed between thetwo groups were caused by C trachomatis and not byother organisms.We isolated N gonorrhoeae from the endomet-

rium in three cases only (one patient had Ctrachomatis isolated as well). One patient withgonococcal endometritis had mild and the otherpatient had moderate endometritis. Because of therelatively small number of patients studied and thelow isolation rate of N gonorrhoeae, we cannot

exclude the possibility that some of the his-topathological findings we described might becaused by N gonorrhoeae as well. On the otherhand, gonococcal endometritis is usually milder andtransient, and lymphocytic response with trans-formed lymphocytes has not been described.25Gonococcal endometritis and endometritis causedby facultative and anaerobic bacteria may be limitedto the superficial mucosal surface, whereas Ctrachomatis may cause deeper endometrial infec-tion. In this study tuberculous endometritis was eas-ily excluded by the absence of typical epitheloid cellgranulomas surrounded by lymphocytic infiltrations.We found that severe endometritis and lymphoid

follicles comprising transformed lymphocytes weresignificantly more common in the chlamydialendometritis group than in the non-chlamydialendometritis group, which suggests that Ctrachomatis is an invasive endometrial pathogen.Not unexpectedly, use of an intrauterine contracep-tive device was also associated with the severity ofendometritis. After excluding women using thesedevices, however, the difference between the twogroups remained significant. We also found that thepresence of microabscesses was more commonamong those with chlamydial infection (38% v21%). Interestingly, some of these findings, such assevere inflammation with active lymphoid follicles,are close to those described in chlamydial eyeinfection (trachoma) and chlamydial cervicitis.26-30

Previous studies have described severe endomet-ritis associated with C trachomatis in a limitednumber of cases-8 but no uniform criteria, havebeen used and no detailed histopathological descrip-tion of the infection has been given. Furthermore,

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the presence or absence of micro-organisms otherthan C trachomatis has generally not been studied.In one recent study8 histopathological examinationshowed pronounced inflammation of the endomet-rium in four of eight patients from whom endomet-rial biopsies were obtained. Endometrial cultures oftwo of the four patients were positive for Ctrachomatis. Moller et all reported one case with"follicular lymphoid endometritis" probably repres-enting a morphological finding similar to thatdescribed in our study.

Further studies are now warranted to characterisein detail the nature of the lymphoid hyperplasiaassociated with chlamydial endometritis. It is con-ceivable that the lymphoid hyperplasia indicates astrong B cell activation caused by C trachomatis. Invitro C trachomatis stimulates human peripheralblood B lymphocytes to proliferate and secretepolyclonal immunoglobulins.3' In vivo, however, theimmunopathological phenomena associated withchlamydial pelvic inflammatory disease are as yetlargely unknown. Genital infections caused by Ctrachomatis have been recognised as a major publichealth problem with serious sequelae in women suchas infertility and pregnancy associated morbidity.Clinically unrecognised endometritis and salpingitisundoubtedly occur among women with "asymp-tomatic" chlamydial infection since less than half ofthe women with tubal infertility have a history offrank pelvic inflammatory disease.32

This study was supported by a grant (7939/304/83)from the Academy of Finland.

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