Repeat Chlamydia trachomatis Infection in Women: Analysis through a Surveillance Case Registry in Washington State, 19931998
Fujie Xu1,2,
Julia A. Schillinger1,
Lauri E. Markowitz1,
Maya R. Sternberg1,
Mark R. Aubin3 and
Michael E. St. Louis1
1 Division of Sexually Transmitted Disease Prevention, Centers for Disease Control and Prevention, Atlanta, GA.
2 Epidemic Intelligence Service, Division of Applied Public Health Training, Epidemiology Program Office, Centers for Disease Control and Prevention, Atlanta, GA.
3 STD/TB Services, Washington State Department of Health, Olympia, WA.
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ABSTRACT
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Repeat infections with Chlamydia trachomatis are associated with increased risk for long-term sequelae. The authors analyzed the frequency and predictors of repeat chlamydial infection by using a population-based chlamydia registry in Washington State and evaluated whether women would seek care at the same clinic for repeat infections. Among 32,698 women with an appropriately treated initial chlamydial infection during 19931998, 15% developed one or more repeat infections during a mean follow-up time of 3.4 years. Among women less than age 20 years at the time of initial infection, 6% were reinfected by 6 months, 11% by 1 year, and 17% by 2 years. Young age was the strongest predictor for one and two or more repeat infections after controlling for the length of follow-up and other variables. Only 36% of the repeat infections were diagnosed at the same clinical setting as the initial infection, and 50% were diagnosed at the same type of clinic. Adolescent girls had the least consistency in the source of care for chlamydia. This study suggests that efforts to prevent repeat chlamydial infection in young women remain an urgent public health priority and that the burden of repeat infection may be substantially higher than estimates from clinic-based studies.
adolescence; Chlamydia trachomatis; infections; population surveillance; registries; sexually transmitted diseases
Abbreviations:
CDC, Centers for Disease Control and Prevention; OR, odds ratio; STD, sexually transmitted disease.
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INTRODUCTION
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Chlamydia trachomatis infection is the most common bacterial infection in the United States; three million incident cases were estimated to have occurred in 1996 (1
, 2
). Although often asymptomatic, chlamydial infections can lead to serious sequelae, including pelvic inflammatory disease, infertility, and ectopic pregnancy (3

6
). Studies in human as well as animal models suggest that the risk for these sequelae increases with repeat chlamydial infection (7
9
). Therefore, understanding the epidemiology of repeat infection is critical to developing prevention strategies for severe morbidity associated with C. trachomatis infection.
Most studies of repeat chlamydial infections have been conducted in young women attending selected types of clinics, such as sexually transmitted disease (STD) clinics or adolescent clinics (10


14
). The high frequency of repeat infections found in these clinic-based studies has led some authors to recommend screening female adolescents for chlamydia as frequently as every 6 months (13
). For older women, repeat testing after one chlamydia infection has also been proposed (14
). The Centers for Disease Control and Prevention (CDC) currently recommends screening female adolescents during each pelvic examination, at least annually (15
). With the availability of amplification tests, screening for chlamydia by using urine specimens has become feasible (16
, 17
). For these and other reasons, revision of the national recommendations for chlamydia screening is under consideration.
To investigate the frequency and predictors of, and time to, repeat chlamydial infection in reproductive-age women attending various types of clinics, we analyzed data from a population-based chlamydia registry in Washington State, one of the states with the longest history in chlamydia control activities. This analysis elucidates the importance of maintaining and utilizing chlamydia registries and provides data that may be useful for revising strategies for chlamydia screening.
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MATERIALS AND METHODS
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Data source
We used the surveillance database of STD maintained by the Washington State Department of Health for this analysis. Since 1987, all health care providers in Washington State have been legally required to report laboratory-confirmed chlamydial infections to the local or the state health department. The laboratory test must have been approved by the Food and Drug Administration for chlamydia (e.g., culture, direct immnofluorescent antibody, enzyme immunoassay, and nucleic acid amplification tests (i.e., LCR, PCR, or TMA)). Data collected on all chlamydia cases include date of birth or age; race; county of residence at diagnosis; reason for clinic visit; anatomic site of infection; treatment used; reporting clinic; and dates of testing, treatment, and diagnosis. Simultaneous infection with other reportable STDs can also be evaluated because all STDs are reported on a single report form. Since 1992, the STD surveillance system of Washington State has routinely linked episodes of chlamydia reported for the same individual over time by using the patient's name, date of birth, and home address. Thus, it effectively serves as a population-based chlamydia case registry.
Definitions
We constructed a retrospective cohort of women with an initial chlamydial infection to assess factors associated with repeat infections registered in the database. The initial infection was defined as the first appropriately treated chlamydia infection reported during the study period. Our cohort consisted of women who 1) had an initial infection at the cervix, urethra, or rectum that was treated between January 1, 1993 and June 30, 1998; and 2) were between ages 10 and 44 years at the time of the initial infection. A treatment was considered to be appropriate only if one of the CDC-recommended antimicrobials (i.e., azithromycin, doxycycline, erythromycin, or ofloxacin, or, in pregnant women, amoxicillin) was used (18
). A repeat chlamydial infection was defined as a urogenital or rectal infection detected at least 30 days after appropriate treatment for the preceding infection. The 30-day interval was measured from the date on which the preceding infection was treated to the date of testing for the subsequent infection; if the date of testing was missing, the date of treatment or diagnosis was used. We used 30 days as a minimum interval because some data indicate that nucleic acid amplification tests may occasionally detect residual chlamydial DNA or RNA up to 3 weeks after antichlamydial agents are given (19
21
). For women who had more than one repeat chlamydial infection during the study period, we denoted the order of repeat infections as the first repeat infection, the second repeat infection, and so on.
For this study, we defined a county as urban, semiurban, semirural, and rural on the basis of the county's population size: more than 600,000, 200,000600,000, 50,000200,000, and less than 50,000 persons, respectively.
Source of care
In Washington's STD surveillance system, each health care setting/clinic is assigned a unique identifier and then classified into one of 19 clinic/provider types. Chlamydia screening practices are known to vary by clinic type. Family planning and reproductive health clinics provide annual chlamydia screening to all sexually active women who meet two or more of the following screening criteria at the time of clinic visit: age 24 years or less, multiple sex partners in the previous 30 days, new sex partner in the previous 60 days, sex partner with multiple partners in the previous 30 days, or no birth control or use of nonbarrier method of birth control. In addition, women are tested if they ask to be or if they have any of the following characteristics: mucopurulent cervicitis, pelvic inflammatory disease, planned insertion of intrauterine device, positive pregnancy test, rape within the previous 60 days, or a partner with signs and/or symptoms of urethritis. In contrast, STD clinics and jail/correction clinics screen all female clients. The screening practices for chlamydia are not uniform in hospitals, health maintenance organizations, and private clinics and are likely to range from no screening to universal screening.
Statistical analysis
Descriptive analyses, relative risks, and 95 percent confidence intervals were calculated by using standard procedures in SAS 6.12 (22
). Incidence of repeat infection was measured as cumulative risk, i.e., the proportion of women who had at least one repeat infection at the specified time after treatment of an initial infection. Predictors of repeat chlamydial infection were analyzed by using two logistic regression models. Model 1 compared women who had at least one repeat infection with those who had no repeat infection during the study period. Model 2 compared women who had two or more repeat infections with those who had no repeat infection to further characterize those who had multiple repeat infections. To control for differences in the length of follow-up, we included in these models the year in which the initial infection was diagnosed. We also attempted to adjust for differences in screening practices by including in the models the clinic type at the time of the first repeat infection; if no repeat infection was reported during the study period, clinic type at the initial infection was used. All covariates in these models were treated as categorical variables; all characteristics except clinic type were measured at the time of the initial infection.
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RESULTS
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During 19931998, a total of 46,434 episodes of urogenital or rectal chlamydial infection were reported to the Washington State Department of Health. Among 39,401 women who had at least one reported chlamydial infection during this period, 37,419 (95 percent) had an initial infection treated with an antichlamydial agent recommended by CDC. After exclusion of 1,993 women who were outside of the age range we were studying and 2,728 women whose infections were treated outside of the enrol1ment period of our retrospective cohort, this analysis was based on a cohort of 32,698 women.
The characteristics of women in our cohort are shown in table 1. At the time of the initial infection, 48 percent of the women were under age 20 years, at least 62 percent were White, and 47 percent were living in urban counties. About 41 percent of the women in our cohort attended public and not-for-profit clinics, which were largely composed of family planning, STD, reproductive health, and jail/correction clinics. Forty-five percent of the initial infections were reported to be detected through screening. At the time of initial infection, four percent of women were coinfected with gonorrhea and 0.3 percent with other STDs (mainly a first episode of genital herpes).
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TABLE 1. Characteristics of women at the time of initial infection and predictors for repeat chlamydia infection (n = 32,698), Washington State, 19931998
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During a passive follow-up period ranging from 6 months to 6 years (mean, 3.4 years), 15 percent (4,841 of 32,698) of the women developed at least one repeat chlamydial infection, and 3.0 percent (988 of 32,986) developed two or more (range, two to eight). For women who had at least one repeat infection during the study period (n = 4,841), the median time to first repeat infection was 331 days (approximately 11 months). Among those who had at least two repeat infections during the study period (n = 988), no difference was found between the two successive intervals to repeat infection (mean difference = 19 days, paired t test, p = 0.09).
The cumulative risk of at least one repeat chlamydia infection by age group is shown in figure 1, in which the percent reported with a repeat chlamydial infection is shown by 3-month intervals. The risk of repeat infection decreased with increased age at the time of an initial infection (
2 test for trend, p < 0.001 at all 3-month intervals). Girls aged 1014 years had the highest risk of reinfection; 16 percent were reported to be reinfected by 1 year. Girls aged 1519 years had the second highest rate of reinfection, with 11 percent reinfected by 1 year. For all women under age 20 years at the time of the initial infection, 6 percent were reported to be reinfected by 6 months, 11 percent by 1 year, and 17 percent by 2 years after treatment of an initial infection. Among women age 20 years or older, reinfection rates were 4 percent or higher at 1 year and 6 percent or higher at 2 years.
Trends were evaluated over the 5.5-year study period. The proportion of women who were under age 20 years at the time of initial infection was unchanged during 19931998; no change was found in the cumulative risk of at least one repeat infection by 1 year after treatment of an initial infection (both tests for trend, p > 0.6). In contrast, there was a decrease in the annual number of reported female chlamydia cases in Washington State in spite of the increasing use of more sensitive tests for chlamydia during the study period (55 during 19931995 and 52 during 19961998 per 1,000 women of reproductive age (1044 years); test for trend, p < 0.001)). Moreover, some decrease in the prevalence of chlamydia among women aged 1524 years who were attending family planning, STD, and job corps clinics was observed from the Chlamydia Screening and Prevalence Monitoring Project in Washington State (23
25
).
In descriptive analysis, young age at initial infection was the strongest predictor of repeat infection (table 1). Of note, the clinic type (except jail/correction clinic) and the reason for the clinic visit were not strong predictors of repeat infection. Women whose initial infections were treated in earlier years appeared to have higher risk for repeat infection due to the longer follow-up period in which a repeat infection could develop. As in descriptive analysis, age was the strongest predictor of repeat infections after adjustment for the length of follow-up, clinic type, and other covariates in logistic regression models (table 2). Girls aged 1014 years were 6.3 times more likely to develop at least one repeat infection and 11.6 times more likely to develop two or more repeat infections when compared with women aged 3044 years. The risks for at least one and for two or more repeat infections were also elevated in non-White women (odds ratio (OR) = 1.5 and 1.9, respectively) and in women coinfected with gonorrhea (OR = 1.6 and 2.0, respectively). Women living in rural counties were less likely to have repeat chlamydia infections (OR = 0.7 and 0.3, respectively) when compared with women living in urban counties (table 2).
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TABLE 2. Adjusted odds ratios and 95 percent confidence intervals for predictors of repeat infection(s), Washington State, 19931998
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Table 3 summarizes the source of care for two successive episodes of chlamydia in the same individual. The initial infections in our cohort were diagnosed at 1,918 clinics, representing all 19 clinic types in Washington's surveillance system. For this analysis, we limited our cohort to women whose initial infections were treated at family planning clinics, health plan/health maintenance organizations, hospitals, reproductive health clinics, STD clinics, and obstetric/gynecologic or other private clinics. Only 36 percent of the women had both their initial and first repeat infections diagnosed at the same clinic; only 50 percent of the women were seen at the same type of clinic for both infections. The likelihood of being diagnosed at the same clinic or at the same type of clinic for the subsequent infection increased with age (both tests for trend, p < 0.001) and varied by provider type (
2 test, p < 0.001). When the study was limited to only family planning clients (n = 1,141), young women were still less likely to be diagnosed at the same clinic for the subsequent infections (test for trend, p < 0.001), indicating that, at least among family planning clients, this trend of serially seeking care from different providers among young women was not due to confounding by clinic type. The likelihood of being diagnosed at the same clinic or the same type of clinic decreased with the interval between the two episodes of infection: 46 percent of the women were diagnosed at the same clinic if the interval was 6 months or less compared with only 24 percent if the interval was 18 months or more. In addition, the public-private line was often crossed for the care of chlamydia: Among 1,559 women whose initial infections were diagnosed at family planning or STD clinicsa subset of public or not-for-profit clinicsonly 54 percent were subsequently diagnosed at family planning or STD clinics for the subsequent infections, 26 percent at private clinics, 8 percent at hospitals, and the remaining 12 percent at other types of clinics. Nineteen percent of the 1,159 women whose initial infection was diagnosed at a private clinic were seen at a family planning or STD clinic for their first repeat infection.
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DISCUSSION
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Among women of reproductive age with an initial chlamydial infection, we observed a high risk for repeat infection, especially among adolescents. Young age was the strongest predictor of one and of two or more repeat infections. Our analysis also showed that women often receive care at different clinics and that, among all age groups, adolescent girls had the least consistent source of care for chlamydia.
Our finding that the burden of repeat infection is highest in adolescents is consistent with results from other studies (10
, 13
, 26
, 27
). A similar study by Hillis et al. (26
) using Wisconsin surveillance data from 1985 to 1989 found even higher rates of repeat infection in adolescents than those in our study, probably due to differences in the populations under surveillance or in past and current chlamydia control activities. Blythe et al. (10
) prospectively examined 177 female adolescents who had a negative test-of-cure after the initial chlamydial infection was treated; the rate of repeat infection ranged from 12 to 38 percent (average, 27 percent) at follow-up visits made at various times within a year (10
). Our study and others suggest that adolescent girls are at greatest risk for long-term sequelae of chlamydia infection due to their high rate of repeat infection and long time at risk. Efforts to prevent repeat chlamydial infection in young women remain an urgent public health priority in the United States.
The finding that women often change the source of care for chlamydia has implications both for estimating the burden of repeat infection and for case management. Clinic-based studies may substantially underestimate the frequency of repeat chlamydial infection. Population-based chlamydia registries are important for identifying groups at high risk for repeat infection, evaluating prevention efforts, and monitoring trends. Medical records at the individual clinic level are unlikely to present the full picture of a woman's STD history. Strategies need to be developed to link public and private providers who participate in the care of chlamydia. To deliver appropriate counseling and screening services, health care providers should obtain a comprehensive STD history, including a history of previous chlamydial infections and the time of last screening. To improve patients' knowledge about their STD history, health care providers should discuss STD diagnoses with their patients.
The major strengths of our analysis include the large number of chlamydia cases from a population-based surveillance system, the ability to link STDs in the same individual even when diagnoses were made at different clinics, and the retrospective cohort design with which predictors of repeat infection could be examined. Nevertheless, this analysis has several limitations, mostly because the data source was a passive surveillance system. First, it is likely that the number of repeat chlamydial infections among women in our cohort was underestimated. Repeat infections in women who moved out of state would be missed by the surveillance system. More important, the ascertainment of repeat infections is likely to be incomplete because chlamydia detection is largely contingent on screening. Second, predictors of repeat infection identified in this study may be markers of greater screening or more complete reporting. In other words, the higher risk in young women may be partially due to more widespread and frequent screening of this group. Although provider compliance with reporting is perceived to be high in Washington State, it may vary by clinic type. Because non-White women and women living in urban counties are more likely to use public clinics, the observed higher risk for repeat infection in these women may be partially because public clinics have better compliance with screening and reporting (28
, 29
). Finally, some apparent repeat infections may represent persistent infections because we do not have a documented negative test between the initial and repeat infections. However, the frequency of persistent infection is probably low, since this study included only women treated with efficacious medications, and treatment failure is believed to be low even when patient compliance is not ideal (18
, 30
, 31
).
New strategies are needed for chlamydia control, particularly in areas where the prevalence of chlamydial infection has decreased and the problem of repeat infection has become relatively more important. The results of our study support more frequent screening in adolescents and older women with a prior chlamydia infection. In our study, among girls who had an initial infection at ages younger than 20 years, 6 percent were reinfected by 6 months, suggesting that a substantial number of infections would be detected if screening were conducted as frequently as every 6 months. Even in women who had an initial infection at an older age, the cumulative risk of reinfection by 1 year was still 4 percent or higher; annual screening for older women may be warranted in the context of a prior infection. Besides enhanced screening, behavioral interventions and enhanced partner services are two important approaches. A clinical trial indicated that interactive counseling (two sessions; 40 minutes total) was effective in reducing chlamydia infection by 2030 percent at 6 and 12 months when compared with didactic messages. Moreover, a stratified analysis showed that the relative effectiveness of counseling was greatest for adolescent patients with prior STD (32
). Because adolescent girls are frequently reinfected by untreated partners (10
), partner services (notification and treatment of potentially infected sexual partners) should be enhanced to ensure that the sexual partners of adolescent girls are treated before sexual activity is resumed. New approaches to partner treatment, such as partner-delivered therapy, are being evaluated for the effectiveness in preventing repeat chlamydia infections (33
). In theory, more frequent screening (and treatment) alone may actually increase the risk for long-term consequences by returning women to the susceptible pool, at risk for another chlamydial infection. For the risk of long-term sequelae to be reduced, more frequent screening for chlamydia must be accompanied by enhanced efforts to prevent repeat chlamydial infection.
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ACKNOWLEDGMENTS
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The authors thank Gary Baschuk, D. Scott LaMontagne, and other staff in STD/TB Services, Washington State Department of Health, for their efforts in data extraction and for their valuable comments.
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NOTES
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Reprint requests to Dr. Michael E. St. Louis, Information Services, National Center for HIV, STD, and TB Prevention, Centers for Disease Control and Prevention, 1600 Clifton Road, NE, Mailstop E-06, Atlanta, GA 30333.
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Received for publication September 24, 1999.
Accepted for publication March 20, 2000.