Sexually Transmitted Diseases:
Acquisition of Chlamydia trachomatis by Young Women During Their First Year of Military Service
SHAFER, MARY-ANN B. MD*; BOYER, CHERRIE B. PhD*; POLLACK, LANCE M. PhD†; MONCADA, JEANNE MT‡; CHANG, Y JASON MS†; SCHACHTER, JULIUS PhD‡
From the *Department of Pediatrics, Division of Adolescent Medicine; †Center for AIDS Prevention Studies; and ‡Department of Laboratory Medicine, University of California, San Francisco, California.
Supported by Department of Defense Grant under the Women's Health Initiative (DAMD17-95-C-5077) from funds allocated to the United States Army Medical Research and Materiel Command, Fort Detrick, MD, and in part by the Leadership Education in Adolescent Health (LEAH), Maternal and Child Health Bureau (Grant MCH000978) who, in part, supported Drs. Shafer and Boyer.
The sources of funding had no role in the study design, collection, analysis, and interpretation of data nor in the writing or decision to submit the article for publication.
Correspondence: Mary-Ann B. Shafer, MD, Department of Pediatrics, Division of Adolescent Medicine, University of California, San Francisco, 3333 California Street, Suite 245, San Francisco, CA 94941. E-mail: firstname.lastname@example.org.
Received for publication May 10, 2007, and accepted September 19, 2007.
Objectives: To define the acquisition rate of Chlamydia trachomatis among a cohort of young, nonhealth-care seeking, sexually active women with well-defined exposure periods over a 12-month period.
Goal: The long-term goal is to inform public health practitioners and young women of the risk of reinfection with C. trachomatis and the need for frequent active screening to eliminate asymptomatic infections over time.
Study Design: Young sexually active female Marine Corps recruits (N = 332), serving as “controls” for an intervention to prevent sexually transmitted infections, were screened for C. trachomatis using nucleic acid amplification tests (treated if positive) at entry (T1). They were rescreened and completed self-report behavioral surveys at 4 weeks (T2) and 9 to 12 months (T3) from recruit training.
Main Outcome Measure: The rate of C. trachomatis acquisition during a contiguous 12-month period.
Results: Based on microbiologic laboratory testing alone, the acquisition rate for C. trachomatis was 3.6% (T2) and 9.9% (T3) yielding a total of 13.0%. The self-reported acquisition rate for the period since graduation from recruit training was 8.1% yielding a total acquisition rate of 19.9%.
Conclusions: The acquisition rate among this cohort of nonhealth-care seeking young women, who have universal health care access is as high or higher than most clinic-based studies, suggesting the need for increased implementation of active screening in primary, urgent, and nonclinic settings.
CHLAMYDIA TRACHOMATIS (CT) REMAINS the most commonly reported bacterial sexually transmitted infection (STI), especially among adolescent and young adult females,1 despite public health efforts to impact its continued transmission. This situation persists even though noninvasive urine-based testing is widely available, accurate, acceptable, and cost-effective2–5; intensive interventions aimed at prevention of acquisition have been shown to be effective.6–9
Defining the scope of the chlamydial epidemic has been hampered by the wide variation in a lack of standardization in both “target” population sampling and microbiologic testing methodologies.1,2,6,10–13 For example, published chlamydial prevalence rates in sexually active young women range from a rate of 5% among adolescents and young adults in a nationally representative sample,14 and 7% (adults) and 13% (teens) from the National Health and Nutrition Examination Survey population-based survey,15 to as high as 24% among young, urban, largely economically disadvantaged black, adolescents.10,11,16 Observed acquisition rates vary from 4% among ethnically diverse urban adolescents attending an HMO teen clinic17 to 6.3% to 21% among adolescent and young adult women seeking care at sexually transmitted disease (STD), family planning, and school-based clinics.10,11,16,18,19 These studies are difficult to compare because the intervals between testing and retesting varied widely and limited because they represent only women seeking health care in clinic settings.
The current study seeks to overcome some of these methodological shortcomings by prospectively examining the acquisition of chlamydia in a well-defined cohort of young, nonhealth-care seeking sexually active women from their entry into recruit training through their first year of military service in the United States Marine Corps. Like civilian populations, chlamydial prevalence rates among US military personnel are unacceptably high also, ranging from 3% to 12%.3,12,13,20–22 Some of these military rates reflect “community acquired” chlamydia diagnosed at entry into military training.3,21,22 This unique cohort of female United States Marines was universally screened and treated for STIs at baseline (within 2 weeks of recruit training entry), had subsequent predictable STI risk exposure periods, and periodic STD risk assessments including microbiologic STI screening coupled with self-report surveys during an approximate 12-month period from the end of recruit training through their first year of military service. Consequently, the design of this study should provide a more accurate assessment of chlamydial acquisition in a young female cohort over time.
Materials and Methods
Between June 1999 and June 2000 all women enrolled in recruit training for the United States Marine Corps at Parris Island, SC (the sole recruit training site for women Marine recruits) were approached during the first week of their 13-week recruit training program by 2 trained civilian research assistants to participate voluntarily in a cognitive-behavioral intervention to prevent STIs and unintended pregnancies during their first year of active duty (experimental intervention) or an intervention focusing upon nutrition and physical injury prevention (control intervention). No military personnel were present during study recruitment and all recruits who agreed to participate in the study signed informed written consent forms and were also given the Human Subjects Bill of Rights statement in accordance with the institutional review boards (IRBs) for the University of California, San Francisco and the Naval Hospital Beaufort, Beaufort, SC in accordance with the guidelines of the US Department of Health and Human Services. The evaluation of the original intervention study is published elsewhere and contains a more detailed description of the overall study.6
Study Design and Assessments
Before the intervention, participants completed a baseline self-administered health survey and were screened for C. trachomatis, Neisseria gonorrhoeae, and Trichomonas vaginalis. (All female Marine Corps recruits are screened for pregnancy and HIV before the beginning of recruit training. Either condition precludes admission to the Marine Corps.) Two postintervention assessments were conducted, which also consisted of a self-administered health survey and laboratory rescreening for the same 3 microorganisms. The postintervention assessments occurred, on average, 4 weeks after graduation from recruit training (median = 34.5 days, range = 11–146 days) and, again on average 11.4 months (median = 10.3 months, range = 1.2–29.2 months) after graduation. The first follow-up assessment took place after the participants had a postgraduation vacation (mean = 13.3 days, median = 10 days reported by 64.9% of respondents, range = 7–90 days) at the end of a 3-week follow-on training period, and the second follow-up assessment took place during the participants' first duty assignment period. The sample disposition, STD exposure periods, and assessment periods are outlined in Figure 1.
Based on prior tracking data of Marines Corps personnel, approximately half of all female Marines are stationed in regions of southern California, eastern North Carolina, and southern Japan during their first year of military service. Given limited resources and the need to have biologic specimens collected, stored, and transported, the study was designed to conduct biologic screenings only in these 3 key geographic regions for the second follow-up assessment.
At baseline (T1), during a reproductive health examination that is required of all entering female Marines Corps recruits, endocervical specimens were collected by a clinician during a pelvic examination. First-void urine samples and self-administered vaginal swabs were also obtained to screen for C. trachomatis and N. gonorrhoeae. At follow-up collections (T2, T3), no pelvic exams were done and only first-void urine samples and self-administered vaginal swabs were obtained to screen for C. trachomatis. Specimens were transported routinely to the Naval Hospital laboratory for processing within 6 hours of collection while maintaining the cold chain. The first-void urine samples and self-administered vaginal swabs for C. trachomatis and N. gonorrhoeae were frozen to −70°C within 24 hours of collection and transported to our university-based research laboratory while maintaining the cold chain. The endocervical and first-void urine samples for C. trachomatis were processed using LCx (Abbott Laboratories, Abbott Park, IL) in accordance with manufacturer's guidelines.23 Although not an FDA cleared specimen for C. trachomatis at the time of the study, vaginal specimens were utilized since they were proven efficacious in prior research.24 The vaginal samples were processed according to the endocervical specimen protocol. A second self-administered vaginal swab for T. vaginalis was immediately inoculated, on collection site, into the In-Pouch TV (Biomed Diagnostics Laboratories, San Jose, CA) according to the manufacturer's instructions. Specifically, the specimens were incubated in pouches immediately after collection at 37°C and were read by trained research assistants for the presence of T. vaginalis at 2 and 5 days after inoculation by microscopy in accordance with manufacturer's guidelines. The same procedures used at baseline for collection and processing of the first-void urine and self-administered vaginal swabs specimens were used at both follow-up assessments. Any woman with a positive STI identified during the course of the study was referred to the base's health clinic where she received treatment and preventive counseling in accordance with guidelines set by the Centers for Disease Control and Prevention.25
It is important to note that female Marine Corps recruits are restricted to base and segregated from their male counterparts during the entire 13-week recruit training period. Consequently, given the screening and treatment procedures described for the baseline assessment, it is reasonable to assume that all female Marines who were followed in our study at T2 were free of STIs when they graduated from recruit training (Fig. 1, Study Design for STI exposure periods).
Self-Administered Health Surveys.
Data on sociodemographic factors, including participants' age, race/ethnicity, education, marital status, region of residence (Northeast, Midwest, South, and West as defined by the Centers for Disease Control and Prevention), and geographic location of residence (metropolitan vs. nonmetropolitan as defined by the US Department of Agriculture for the 1990 Census and based on respondent's home zip code) are drawn from responses to the baseline health survey. At the second follow-up assessment, the health survey assessed the participants' self-reported history of STIs since graduation from recruit training. Specifically, they were asked, “Since graduating from Recruit Training, have you been told by a medical provider (doctor or corpsman) that you had an STD?”, and “If yes, what was the name of the STD(s)?” The response set for the latter question was chlamydia, gonorrhea, trichomonas, herpes, warts, syphilis, and other. Self-reported STIs have been found to have high reliability and comparable sensitivity compared with medical record and state STD reports.26
Follow-Up Assessments and Study Attrition
An overview of the disposition of the study population by risk and assessment periods is outlined in Figure 1. Two thousand one hundred fifty-seven (97%) of 2228 women were eligible for the study and 2157 women gave informed written consent to participate in the study. To determine STI acquisition rates, only those ongoing participants who had been sexually active since graduation from recruit training were included (n = 1192) for further analyses. A comparison between the subsample of women who self-identified as sexually active and those who self-identified as not being sexually active revealed that the sexually active women were slightly less likely to be white (54.7% vs. 57.4%, P = 0.033) and slightly more likely to be single (94.3% vs. 91.9%, P = 0.029) than the nonsexually active women. No differences with regards to age, region, and geographic location of residence were found. To insure comparability of acquisition rates defined by varying sources of data and assessment periods, it was necessary to limit the data analyses to only those women who had complete STI biologic specimen data at T2 and T3 and self-report survey data at T3 (n = 648). The only significant demographic difference identified with this selection again revealed that women with complete data were less likely to be white compared with women with incomplete data (49.8% vs. 60.5%, P = 0.001). Finally, since the overall study subsumed an intervention to prevent unintended pregnancy and acquisition of STIs during the first year of active service, the final analytic subsample for this evaluation of acquisition was restricted to the control group (N = 332), thus excluding those women exposed to the STI prevention intervention. The control group and the intervention group did not statistically differ on any demographic characteristics.
Overall, women participating in the study were young (mean = 18.9 years of age at baseline, median = 18 with 49.7% of the sample at this age, range = 17–30), ethnically diverse (44% ethnic and racial minorities), overwhelmingly single, and resided primarily in urban settings before recruit training entry (Table 1).
Acquisition of STIs
The baseline (T1) overall prevalence rate at entry into recruit training for any of the 3 microorganisms measured was 14% (249/1769), including C. trachomatis 11% (209/1813), N. gonorrhoeae 2% (43/1813), and T. vaginalis 2% (30/1766). All women had documented appropriate treatment for all infections before completion of recruit training. The acquisition rates after recruit training for any of the 3 microorganisms by microbiologic tests were 5% (16/332) at T2, 11% (36/332) at T3, and 15% (50/332) when T2 and T3 biologic results were combined. Since the majority of infections identified at all study periods were C. trachomatis, all further analyses will focus solely on acquisition of that microorganism.
Acquisition of C. trachomatis by Assessment Period
Microbiologic laboratory testing at T2 assessed acquisition from exposure during a short vacation period (median 10 days) that immediately follows graduation from recruit training (3.6% positive). This vacation leave was followed by 3 weeks of follow-on training during which the women faced the same social restrictions encountered during their initial recruit training (i.e., they had no social contact with males). After completion of the follow-on training, they immediately commenced to occupational specialty training where there were opportunities for social contact with male peers. Microbiologic laboratory testing at T3 detected new untreated infections (9.9%) acquired between the completion of their follow-on training and the T3 assessment, approximately 9 to 12 month window of exposure. Self-reports of diagnosis and treatment of C. trachomatis infection since graduation from recruit training attempted to capture infections that were acquired and treated between the 2 microbiologic laboratory testing periods (8.1%), i.e., outside of the study protocol. Table 2 reports the acquisition rate defined by each of these data sources and relevant combinations of data sources, i.e., microbiologic specimen screenings at specific time periods (T1, T2, and T3), self-report STIs (reported in the health survey at T3 covering the period since graduation from recruit training), and combining the microbiologic screening results with self-reports.
All reports of acquisition rates were based on individuals, i.e., the number of women who acquired C. trachomatis divided by the total number of women (N = 332). Specifically, when sources of data are combined, an infected woman was counted only once to determine the acquisition rate, even if she had multiple infections during the study assessment period. However, there was little evidence of multiple infections in the same women as the acquisition rate for the T2 and T3 biologic tests combined (13.0%) is only slightly lower than summing the individual rates T2 plus T3 (13.5%). Similarly, the addition of the self-reported data yielded a rate (19.9%) only slightly lower than what would be obtained if the combined biologic test rate and the health survey rate were added together.
This study is the first report of chlamydial acquisition by an ethnically and geographically diverse cohort of nonhealth-care seeking, sexually active young women with known STD risk exposure periods who were prospectively followed and evaluated at defined assessment periods with both microbiologic laboratory and health survey screening tools. Specifically, at the beginning of 13 weeks of recruit training, these women Marine recruits were screened for C. trachomatis infection through microbiologic laboratory testing applying nucleic acid amplification tests technology on 3 different specimens (urine, vaginal, endocervical). All women who tested positive were treated and counseled. Restriction to base and sexual segregation during recruit training precluded exposure to infection until after graduation from recruit training. We found that the laboratory confirmed acquisition rate of C. trachomatis in this cohort ranged from 3.6% after a brief 10-day vacation leave to 13% based on the combined results of the 2 microbiologic laboratory screening periods (T2, T3) over the first year of active duty. This is consistent with 2 other prospective studies employing nucleic acid amplification tests technology. A multicenter study of chlamydia infected young women aged 14 to 34 years old who were retested at 1 and 4 months showed a recurrence rate of 6%.19 In a second study, a cohort of women under 25 years old were shown to have an acquisition rate of 11%.16,17 However, in the current study, given the 9- to 12-month gap between T2 and T3, it is likely that our 13% acquisition rate is an underestimation of the actual rate. This conclusion of underreporting is supported by the findings from the Add Health national sample of young women aged 18 to 26 years, which found that these young women underreported the C. trachomatis infections by a ratio of 1.41 laboratory confirmed to self-reported infections in the previous year.27 By adding in the unique self-reported chlamydial infections (additional 8%) from the health survey at T3 in our current study, the summed acquisition rate increased to 19.9%.
The findings from this prospective study also emphasizes the fact that the chlamydial epidemic continues to be “alive and well” among healthy young women who are not seeking health care services. We have shown that our cohort of women entered military service with a high rate of infection (11% at T1) reflecting high community-based infection rates. We also know that this same cohort of women continued to acquire chlamydia over their first year of duty with rates as high as 20% when both microbiologic laboratory and health survey assessments are summed. But most striking, these epidemic rates are occurring among healthy young women who have had access to the largest universal “HMO health coverage” system in the United States (military health) during the entire 12 months study period. The laboratory-verified infections were only discovered among these nonhealth-care seeking women by the active screening intervention of the research project over a 1-year period.
On a national level, efforts to achieve the recommended policy of universal screening among sexually active young women have fallen short of the goal as reflected in the available data from both commercial and Medicaid plans. For example, in 2001 among 16- to 26-year-old sexually active females only 26% and 38% were screened by commercial and Medicaid plans, respectively.28 To begin to address this discrepancy between universal and actual screening rates among young women, effective systems level interventions have been implemented by our group and others. Specifically, 2 such systems interventions have been shown to markedly increase chlamydial screening rates from 5% to 65%29 in an adolescent population, and from 52% to 72% among adolescent and young adult women.30 Furthermore, to address the high rate of acquisition/recurrence presented here and elsewhere, it is obvious there is a need for more frequent active chlamydial screening during a given year, especially among at risk groups like young military women.2,21
To accomplish increased active screening among young, at risk women, we need to promote and actively support research and public health policies, programs, and interventions that focus on increasing active screening of young women not only within traditional clinical settings, but also outside of such settings in order to identify and target those young women who are not seeking health care services. This is especially true in the military setting where a 20% annual acquisition rate represents a significant resource burden on the military health care system including the possible threat to military readiness that serious reproductive health sequelae to untreated STI's could pose. Finally, this study shows that the acquisition rates of STI's such as chlamydia may vary widely depending upon the source of the information (e.g., self-report vs. laboratory verified), which becomes particularly important in applying the findings from surveillance and intervention studies in the development of research and clinical programs and policy.
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