Prevention of Pelvic Inflammatory Disease by Screening for Cervical Chlamydial Infection
Delia Scholes, Ph.D., Andy Stergachis, Ph.D., Fred E. Heidrich, M.D., M.P.H., Holly Andrilla, M.S., King K. Holmes, M.D., Ph.D., and Walter E. Stamm, M.D.
Background Chlamydia trachomatis is a frequent cause of pelvicinflammatory disease. However, there is little information fromclinical studies about whether screening women for cervicalchlamydial infection can reduce the incidence of this seriousillness.
Methods We conducted a randomized, controlled trial to determinewhether selective testing for cervical chlamydial infectionprevented pelvic inflammatory disease. Women who were at highrisk for disease were identified by means of a questionnairemailed to all women enrollees in a health maintenance organizationwho were 18 to 34 years of age. Eligible respondents were randomlyassigned to undergo testing for C. trachomatis or to receiveusual care; both groups were followed for one year. Possiblecases of pelvic inflammatory disease were identified througha variety of data bases and were confirmed by review of thewomen's medical records. We used an intention-to-screen analysisto compare the incidence of pelvic inflammatory disease in thetwo groups of women.
Results Of the 2607 eligible women, 1009 were randomly assignedto screening and 1598 to usual care. A total of 645 women inthe screening group (64 percent) were tested for chlamydia;7 percent tested positive and were treated. At the end of thefollow-up period, there had been 9 verified cases of pelvicinflammatory disease among the women in the screening groupand 33 cases among the women receiving usual care (relativerisk, 0.44; 95 percent confidence interval, 0.20 to 0.90). Wefound similar results when we used logistic-regression analysisto control for potentially confounding variables.
Conclusions A strategy of identifying, testing, and treatingwomen at increased risk for cervical chlamydial infection wasassociated with a reduced incidence of pelvic inflammatory disease.
Pelvic inflammatory disease is the most serious sexually transmittedbacterial infection affecting women.1 Recent studies have moreclearly defined the ascending route of infection. Lower genitaltract infection can lead to endometrial and tubal infection(i.e., pelvic inflammatory disease) and, in turn, to complicationssuch as infertility, ectopic pregnancy, and chronic pelvic pain.2,3,4,5There is general agreement that efforts to prevent pelvic inflammatorydisease must address the earliest parts of this causal chain— that is, they must emphasize the primary preventionor early detection of infections of the lower genital tract.5,6,7,8
In the United States, Chlamydia trachomatis is the most commonsexually transmitted bacterial pathogen and a major cause ofpelvic inflammatory disease.1,9,10 It is thus a logical focusfor prevention efforts, but timely detection and control arehampered by the large number of asymptomatic cervical infections.1,5,6,7,8,9,10,11Efforts to control chlamydial infection have been aided in recentyears by the development of screening criteria for use in situationswhere there is a low prevalence of infection.12,13,14,15,16,17Direct evidence that screening programs can contribute to thesecondary prevention of pelvic inflammatory disease is stilllacking, however. To our knowledge, no studies have experimentallyverified that testing and treating women with early chlamydialinfection affects their risk of subsequent pelvic inflammatorydisease.
We developed criteria to identify women at increased risk forchlamydial infection in a low-prevalence population —the enrollees of a health maintenance organization (HMO).17We now report on a randomized, controlled trial in the samepopulation that was designed to evaluate whether the use ofthese criteria to select women to be tested for cervical chlamydialinfection would reduce the incidence of pelvic inflammatorydisease.
Methods
Study Population
This study was conducted between October 1990 and May 1992 atGroup Health Cooperative of Puget Sound, a staff-model HMO locatedin western Washington State. Group Health Cooperative providescomprehensive health care to approximately 380,000 enrolleesand has numerous computerized and manually maintained data baseslinked by the permanent medical-history numbers assigned toeach person on enrollment.18 All study procedures were reviewedand approved by the institutional review board at the HMO.
An earlier study at Group Health Cooperative of 1692 largelyasymptomatic young women attending primary care clinics founda prevalence of chlamydial infection of 3.5 percent.17 An ageof less than 25 years, black race, nulligravidity, two or moresexual partners in the past year, douching within the past year,the presence of cervical ectopy, and being unmarried were independentlyassociated with an increased risk of chlamydial infection.
We then designed a randomized, controlled intervention trialto examine whether testing and treating women identified bythe risk factors would affect the subsequent occurrence of pelvicinflammatory disease. We adapted the earlier predictive modelto exclude married women, in whom the prevalence of chlamydialinfection was very low, and to exclude cervical ectopy as acriterion for screening, since this required an examination.We then developed a brief, self-administered questionnaire thatwe could use to classify women according to risk status. Allwomen from 18 to 34 years of age who were Group Health Cooperativeenrollees as of October 1, 1990, were selected from the computerizedenrollment file. After excluding enrollees whose records listeda spouse, we mailed questionnaires to the remaining 36,547 womenover a 10-month period. Duplicate surveys were mailed to thosewho did not respond. We also telephoned some of the nonresponderseach month to request that they return the questionnaire orgive their responses by telephone. Emphasis was placed on callingnonresponding women assigned to the intervention group in orderto expedite setting up their clinic appointments for testing.
Once the questionnaires were returned, we excluded women whowere currently pregnant, who had never had sexual intercourse,who had undergone hysterectomy, who regularly used antibiotics,or who were married. We then used an algorithm (in which weassigned the following values: age <24 = 1, black race =2, nulligravidity = 1, douching in the preceding 12 months =1, and two or more sexual partners in the preceding 12 months= 1) to assign each woman a risk score. Those with scores of3 or more were eligible for the study, since they were consideredto be at increased risk for asymptomatic chlamydial infection.
Randomization
The women were randomly assigned to either the screening groupor the usual-care group at the time the original sample wasselected in October 1990; the ratio of women in the screeninggroup to women in the control (usual-care) group was 1:2.
Study Intervention
As soon as their surveys were scored, all eligible respondentsin the screening group were invited to come to one of the studyclinics to be tested for C. trachomatis. At the clinic, afterinformed consent was obtained, we collected two cervical samples.A swab was tested by enzyme-linked immunosorbent assay (KallestedPathfinder kit) performed according to the manufacturer's instructions.A second specimen, obtained with a cytobrush, was placed intransport medium and sent to the University of Washington forchlamydial cell culture, as previously described.19 All womenwith positive results on either test were treated for chlamydialinfection by their primary care provider.
Women assigned to the usual-care group saw their providers atGroup Health Cooperative as needed. They were not contactedfurther by the study team until the follow-up evaluation.
Evaluation of Outcomes
Participants were followed for 12 months to assess end pointsof interest. Because funding for this study limited follow-upto a relatively brief period, the end point was the incidenceof pelvic inflammatory disease. We used several methods to identifypotential cases of pelvic infection in the study population.Each participant received a follow-up questionnaire one yearafter enrollment in which she was asked about urogenital infections,diagnosed pelvic inflammatory disease, and other health-relatedevents and behavior. The Group Health Cooperative's outpatientdata base was used to identify study participants who had beenassigned a diagnostic code indicating pelvic inflammatory diseaseor cervicitis during follow-up. Similarly, we used the inpatientdata base to identify participants who had been assigned a diagnosisof acute pelvic inflammatory disease or salpingitis at dischargefrom the hospital. Information on participants with positivetests for chlamydia or gonorrhea during follow-up was obtainedfrom the laboratory records. Finally, women who had not otherwisebeen identified as having pelvic infection but who had received10-day courses of doxycycline were identified from pharmacyrecords.
The medical records of the women with possible cases of pelvicinflammatory disease were then reviewed. We determined whetherthere was evidence of a diagnosis of pelvic inflammatory diseasein the chart and recorded any available information on specificsigns and symptoms (principally abdominal pain of less thanone month's duration, cervical-motion or uterine tenderness,and adnexal tenderness); laboratory findings (positive testsfor gonorrhea or chlamydia); and subsequent diagnoses invalidatingthe diagnosis of pelvic inflammatory disease. The abstracterswere unaware of the participants' study-group assignments.
Statistical Analysis
On the bases of the responses to the initial survey, we determinedthe distributions of prognostic factors and other variablesin the two groups and compared them by means of chi-square testsand t-tests. An intention-to-screen analysis was used to comparethe groups with respect to the incidence of pelvic inflammatorydisease. The incidence of pelvic inflammatory disease in eachgroup was calculated according to total follow-up time (12 monthsor until the women underwent hysterectomy or left the HMO).For all analyses, we included only cases of pelvic inflammatorydisease that were confirmed by the medical-records review. Thatis, in addition to the listing in the data base that was usedto identify a potential case of pelvic inflammatory disease,the diagnosis had to be noted in the medical record. We thenevaluated by rate ratios the risk of pelvic inflammatory diseaseamong the women assigned to the screening group relative tothat among the women assigned to usual care.
We also used unconditional logistic-regression analysis to estimateodds ratios and 95 percent confidence intervals while controllingfor the potentially confounding effects of other base-line variables.Variables considered singly and in combination in the logistic-regressionmodels were age, marital status, douching practices, gravidity,and number of sexual partners.
Results
Final Study Population
We received responses from 20,836 (57 percent) of the 36,547women to whom we mailed the initial survey; 17,725 (85 percent)of those responding were ineligible because they had a low riskscore or another reason for exclusion, and 504 women (2 percent)declined to participate. Of the remaining 2607 eligible women(13 percent), 1009 had been randomly assigned to the screeninggroup and 1598 to the usual-care group.
Base-Line Characteristics
The distribution of prognostic variables and other characteristicsin the screening and usual-care groups at base line is shownin Table 1. The two groups were very similar in terms of thevariables used to evaluate risk status and in their educationallevel, annual income, and history of Pap tests.
Table 1. Prognostic Variables in the Screening and Usual-Care Groups at Base Line.
A total of 645 (64 percent) of the women in the screening groupwere tested for cervical chlamydial infection; 44 (7 percent)had positive tests. All 44 women with positive results receivedtreatment for chlamydial infection from their primary care providers.The 645 women in the screening group who underwent testing weresimilar in terms of the prognostic variables to the 364 whowere not tested (data not shown).
Incidence of Pelvic Inflammatory Disease
At the end of the 12-month follow-up period, we received completedfollow-up questionnaires from 76 percent of the 2607 participants.Ninety-six of the women reported an episode of pelvic inflammatorydisease. The computerized data bases of Group Health Cooperativeidentified 57 participants who had received a diagnosis of pelvicinflammatory disease. Of the 142 women identified in these twoways as having pelvic inflammatory disease, a review of themedical records showed a clinical diagnosis of pelvic inflammatorydisease in 37. Five more women with a recorded diagnosis ofpelvic inflammatory disease were identified by our review ofthe charts of 486 women who reported symptoms typical of pelvicinflammatory disease, had a diagnosis of cervicitis, filledprescriptions for doxycycline, or had positive tests for chlamydiaor gonorrhea during follow-up.
There were 9 confirmed cases of pelvic inflammatory diseaseamong the women in the screening group and 33 among the womenassigned to receive usual care. Seven of the nine cases in thescreening group were in women who had been tested for chlamydia.Additional information on symptoms, other evidence of infection,or indications of severe disease included the following: abdominalpain (noted for 13 women); the presence of two of three symptoms(abdominal pain, cervical-motion or uterine tenderness, andadnexal tenderness, noted for 18); and the presence of all threesymptoms (noted for 6). Seven women had positive tests for chlamydiaor gonorrhea. Three women, all in the usual-care group, werehospitalized for pelvic inflammatory disease.
Follow-up totaled 11,563 woman-months for the 1009 women inthe screening group and 18,265 woman-months for the 1598 womenin the usual-care group. The incidence of pelvic inflammatorydisease was 8 per 10,000 woman-months in the screening groupand 18 per 10,000 in the usual-care group (relative risk, 0.44;95 percent confidence interval, 0.20 to 0.90)(Table 2). In logistic-regressionmodels adjusting for base-line variables, the odds ratios rangedfrom 0.42 (95 percent confidence interval, 0.20 to 0.88) afteradjustment for race or ethnic group or gravidity to 0.44 (95percent confidence interval, 0.21 to 0.91) after adjustmentfor the number of sexual partners in the past 12 months. Simultaneousadjustment for the potentially confounding effects of douching,marital status, and age (odds ratio, 0.42; 95 percent confidenceinterval, 0.20 to 0.89) (Table 2) and other combinations ofthe base-line variables did not substantially alter the reductionin the risk of pelvic inflammatory disease associated with screening.
Table 2. Incidence and Risk of Pelvic Inflammatory Disease According to Study Group.
Discussion
Reducing the incidence of pelvic inflammatory disease is a goalof the Public Health Service for the year 2000.20 Efforts tocontrol this disease are hampered, however, by many problems,including the fact that a variety of pathogens can cause infection,the difficulty of making the diagnosis, the frequency of asymptomaticinfections, and the lack of adequate surveillance systems. Thegreatest hope for progress lies in the prevention and earlydetection of lower genital tract infections, which often leadto pelvic inflammatory disease.
The importance of cervical chlamydial infection in the pathogenesisof pelvic infection is well recognized.1,3,9 More than 4 millionchlamydial infections are estimated to occur annually in theUnited States, and their early detection and treatment clearlyrepresents an important avenue for the prevention of pelvicinflammatory disease. To date, the effects of programs to controlchlamydia on the incidence of pelvic inflammatory disease havebeen evaluated primarily through the use of decision analysisor other models estimating the cost effectiveness of selectivescreening strategies in various populations of patients.13,21,22,23,24,25,26Although very useful, these models rely on assumptions aboutthe prevalence of chlamydia, the characteristics of tests, theefficacy of treatment, patients' compliance, and the risks ofsubsequent pelvic inflammatory disease.
In an earlier study, we identified several readily ascertainablecharacteristics that were associated with an increased riskof cervical chlamydial infection.17 We then conducted a randomized,controlled trial to study the effect of screening and treatingwomen for these infections on the incidence of pelvic inflammatorydisease. Using confirmed clinical diagnoses of pelvic inflammatorydisease as the outcome measure, we found that the women assignedto the screening group had a 56 percent lower incidence of pelvicinflammatory disease than those in the usual-care group.
The selection of Group Health Cooperative as the research settinghad a number of advantages. The well-defined patient populationof this HMO allowed us to identify and contact all female enrolleesof the appropriate age and enabled us to recruit high-risk participantsefficiently from a large pool of women at low risk. Enrolleesalso received most of their health care within the Group HealthCooperative system.18 Rather than rely solely on the women'sreports in the follow-up questionnaire or review the chartsof the entire study group, we used a variety of computerizeddata bases to identify potential cases of pelvic inflammatorydisease. This disease is difficult to identify; therefore, wealso used manually maintained medical records as a method ofverifying its occurrence.
National surveillance systems can monitor only the incidenceof pelvic inflammatory disease in hospitalized patients, yetthe great majority of women with this condition are not admittedto hospitals. Women with chlamydial pelvic inflammatory diseasemay be particularly likely to have relatively mild symptomsand to be treated as outpatients.2,5,20 A recently completedoutpatient reporting system at Group Health Cooperative madeit easier for us to identify women receiving ambulatory carefor pelvic inflammatory disease.
HMOs also offer advantages from the standpoint of integratingthe control of chlamydia with routine patient care. Both screeningfor risk factors and testing can be initiated by either theHMO or the provider. In the latter case, women who come intocontact with the health care system for a variety of reasonscan be evaluated for risk and tested if necessary. Alternatively,the population-based approach that we used to assess the efficacyof screening could be continued at selected intervals. Thisapproach has been adopted at Group Health Cooperative for mammography27and has the potential advantage of reaching women who use healthcare services infrequently.
Our study had limitations that deserve discussion. The one-yearfollow-up period did not allow us to evaluate the frequencyof delayed or uncommon sequelae of chlamydial infection. Timeconstraints also dictated our decision to assign women randomlyto study groups before mailing the first questionnaire. In orderto have enough time to bring participants into the clinics fortesting and still allow 12 months for follow-up, we concentratedon making telephone reminder calls to nonresponders assignedto the screening group. The final ratio of women in the screeninggroup to women in the usual-care group was 1:1.6, rather thanthe initially assigned ratio of 1:2. This smaller proportionof women assigned to the usual-care group who actually participatedin the study suggests the possibility of selection bias. Morewomen assigned to screening than to usual care may have respondedto the reminder calls, and those who agreed to participate inresponse to telephone calls may have differed in some ways fromthose who responded to the initial mailings. However, the scriptused for the reminder telephone calls was identical for bothstudy groups, said nothing about group assignment, and containedthe same information as the cover letters. Our examination ofbase-line variables also showed the two groups to be very similar.
We were able to screen only 64 percent of the 1009 women inthe intervention group who were invited to undergo testing.This relatively low rate of participation is probably a featureof using a population-based approach to identifying and testinghigh-risk women.
The use of pelvic inflammatory disease as a study outcome isproblematic. Given the invasiveness and cost of laparoscopicvisualization, the vast majority of cases must be diagnosedon the basis of clinical signs and symptoms, indicators of inflammation,and laboratory-test results.28,29 In this analysis, we usedmedical records to confirm cases of pelvic inflammatory diseaseidentified through the women's reports or in computer data bases.Nonetheless, some of the women may not have had pelvic inflammatorydisease. It is also possible that some cases of asymptomaticpelvic infection did not come to our attention. It is unlikely,however, that the identification and verification of pelvicinflammatory disease varied greatly between the screening groupand the usual-care group. The same diagnostic codes were usedto identify women with potential cases, and the medical-recordsreviewers were unaware of the participants' group assignments.
This study was conducted in a managed-care setting; the optimalfactors for use in screening and the effects of screening andtreating women for chlamydial infection on the incidence ofpelvic inflammatory disease could differ in other health caresettings. However, a number of screening criteria (for example,age, number of sexual partners, and marital status) have beenconsistently identified and provide a basis for evaluating riskstatus. Our study provides evidence that, once women at highrisk are identified and tested, the incidence of pelvic inflammatorydisease can be reduced.
The costs of pelvic infection in terms of human suffering anduse of health resources are large, and the components of successfulprograms to prevent pelvic inflammatory disease remain elusive.Several pieces of the prevention puzzle have been put in placein recent decades. The prevention of sexually transmitted infectionsthat can cause pelvic inflammatory disease has received deservedlyincreased attention. The elucidation of the role of cervicalchlamydial infections, along with the development of more sensitivediagnostic tests and more effective treatment, was also important,as was the development of efficient ways to target high-riskwomen through selective screening. Our study further shows thata population-based approach to identifying and testing womenat increased risk for cervical C. trachomatis infection canreduce the risk of pelvic inflammatory disease.
Supported in part by a grant (A1-24756) from the National Instituteof Allergy and Infectious Diseases and by a grant from Bristol-MyersSquibb. Dr. Stergachis is a Burroughs Wellcome Scholar in Pharmacoepidemiology.
We are indebted to Elizabeth Foss and Lair Showalter for theirassistance with data management; to Jane Grafton and Byung JooPark for their help with computer programming; to research assistantsKay Brown, Alice Fisher, Joann Habakangas, Gertrude Witt, andMary Sunderland; to the study nurse, Fae Neumann; to Peggy Rogersat the Group Health Cooperative laboratory and the staff ofthe University of Washington Research Laboratory; and to Dr.Edward Wagner for consultation during the course of this project.
Source Information
From the Center for Health Studies (D.S.) and the Department of Family Practice (F.E.H.), Group Health Cooperative of Puget Sound; the Department of Epidemiology, School of Public Health and Community Medicine (D.S., A.S.), the Department of Medicine, School of Medicine (K.K.H., W.E.S.), and the Department of Pharmacy, School of Pharmacy (A.S., H.A.), University of Washington — all in Seattle. Presented in part at the Eighth International Symposium on Human Chlamydial Infections, Gouvieux-Chantilly, France, June 19–24, 1994.
Address reprint requests to Dr. Scholes at the Center for Health Studies, Group Health Cooperative of Puget Sound, 1730 Minor Ave., Suite 1600, Seattle, WA 98101.
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