Overall prevalences for chlamydia for unduplicated females from years 1996 to 2003 were over 15% each year. Trends have not decreased by year; the lowest prevalence was in 1999 at 15.1% and the highest prevalence was in 2002 at 19.5% (Table 1). Reasons for this are unclear; except that the cohorts are continually changing as students leave and new students come. The high prevalence may just reflect high community prevalence and the opportunity for transmission from unscreened males in both the schools and community. Fewer males are traditionally tested for chlamydia in our schools, but the prevalences are usually only slightly lower (8–10%) than for females (personal communication, Gerry Waterfield). The reasons for fewer males being tested in schools may include the fact that females more often seek reproductive health services, and adolescent males do not routinely seek health care unless they are symptomatic or are identified as a sexual contact to an infected female.15–17 Provision of sports physicals by SBHCs may provide another venue that could provide opportunistic screening of both females and males for STIs.18
A significant limitation of this analysis is that the measure of incidence of reinfection presented is likely to be an overestimate of the true reinfection rate because it is limited to individuals who were positive once and then were retested subsequently. Since individuals are potentially more likely to have come back for a second test if they were symptomatic or suspected they were infected again, our estimate of reinfection is likely to be biased upward. Although this limitation exists, this approach to measuring incidence of reinfection has been employed by others.11,19 Longitudinal cohort studies, which insure that all infected individuals get retested, would be required to determine the precise reinfection rate, however such studies are expensive and are potentially limited to small numbers of individuals. If one were to take the extreme case, where none of our remaining cohort was reinfected, the overall estimate of the incidence of reinfection would be 236/1920 or 12.3%. The true estimate is likely to lie somewhere between 26.3% and 12.3%. There is no way to correct for the bias in this analysis, but insight into what makes a student report for rescreening within 1 year may be instructive. As reported by the clinicians, students appear to be more likely to seek rescreening when they report having a new partner, which would put them at increased risk. It is also standard SBHC procedure that students are told to return for rescreening every 6 months and if they are infected, they are instructed to return for rescreening in 3 months. However there is no definitive method to know what prompted rescreening in this analysis.
We analyzed the data to ascertain repeat unique, individual infections in order to identify trends and reinfection incidence by age and school. The chlamydia incidence of reinfection rate in students from the 8 high and 3 middle schools in Baltimore was very high (26.3%) and not dissimilar from other earlier analyses of reinfection rates for females in some of these same schools.3 Our reinfection rates in Baltimore appeared to be much higher than those reported in earlier studies in other cities.11,19–21 However, our methodology differed from that of other studies in that we looked at reinfection within 1 year, rather than the shorter time periods of 3 to 4 months or longer time periods of 3.4 years used by others.11,21 Xu et al.,11 using passive surveillance similar to that of our method, reported that among 32,698 women, 15% developed 1 or more repeat infections during a mean follow-up time of 3.4 years, while in those less than age 20 years, 6% were reinfected in 6 months, 11% by 1 year, and 17% by 2 years.11 Whittington et al.21 detected a reinfection rate of 7.1% at 1 month and 13.4% at 4 months. Additionally, a summary of published reinfection rates for chlamydia for 1- and 4-month periods reported a range from 5% to 13%.22 Thus, comparisons of reinfection across studies are problematic with regard to timing of retesting. It has also been noted that studies relying on passive retrospective cohorts developed from health services data provide somewhat upwardly biased estimates of incidence of reinfection of STIs.23 However, allowing for the lack of perfect cohort studies, the CDC recommends rescreening women who have a positive test in approximately 3 months in the latest treatment guidelines.24
Our trends for reinfection incidence in females, as measured by this analysis, have varied little over time; reinfection rates for 1 year ranged from 24.5% in 1996 to 21.6% in 2003. Participation in the school screening program in New Orleans demonstrated an incidence rate per 1000 person-months in students that were tested more than once during 3 years of screening of 4.3% (2.2, males; 7.1, females).19 The differences from our analysis may be due to differences in timing of measurement of reinfection. Compared with our high reinfection incidence, their lower rate may also be due to the lower starting prevalences in these schools of 7.7% for females and 1.8% for males.19 High-risk teens who were followed in adolescent clinics in Indianapolis over 3 years demonstrated initially high chlamydia rates (28.4%) and reinfection rates of 18% at visit 2 in 3 months, while at visit 3 in 9 months the reinfection rate for chlamydia was 20%, a rate not too dissimilar from our reinfection incidence of 25%, although it is difficult to compare results across studies.8 The high reinfection incidence in our schools and in other cities requires more intense prevention interventions to lower these reinfection rates.
Screening during sports physicals in SBHCs may present an additional opportunity to test more asymptomatic students.26 In 1 study, 93% of athletes were asymptomatic; prevalence was 6.5% among females and 2.8% for males.27 Not all high school screening studies have reported high chlamydia prevalences; of 283 female and 381 male asymptomatic students screened in San Francisco, a prevalence of 3.9% for females and 0.8% for males was demonstrated.28 An example of high prevalence from screening in high schools was demonstrated in a comprehensive school screening program in Philadelphia, which reported an initial prevalence of 8.1% for females and 2.5% for males among 19,394 public high school students.29
The high reinfection rate among female school students in our analysis supports a local recommendation to screen adolescents frequently,3 and especially if there is a history of a previous chlamydia infection, as recommended by the CDC.24 Screening by urine-based tests makes rescreening easier to accomplish than obtaining cervical swabs. Young age of <20 years for both males and females has been reported to be significantly associated with risk of STI reinfection in a large study of 64,463 patients attending sexually transmitted diseases clinics from 4 cities, indicating that emphasis for rescreening should be focused on adolescents.30 Young age at first infection as detected in our study was also significantly associated with increased risk of reinfection; it may suggest that younger females may require more intensive interventions. Use of self-collected samples, such as urine and self- obtained vaginal swabs, which can be collected at home and mailed to a testing site, has been widely used in Europe to improve screening and rescreening.31,32
Future approval by the Food and Drug Administration for use of vaginal swabs collected at home may offer another way to encourage adolescent females to sample themselves more frequently, after initial screening in schools. Frequent rescreening appears to be urgently needed for adolescents, especially since teens often change sex partners and may have more than 1 partner.33 Self-obtained vaginal swabs are highly accurate if tested by NAATs, are acceptable to women, and can be recommended as feasible for retesting adolescents for chlamydia.34–39 Whether urines or self-obtained vaginal swabs are used, self-sampling may provide an optimal intervention to affect the epidemic of chlamydia in the United States. However, ways to improve rescreening of infected adolescents are needed and may include making advanced appointments, offering reminders through the school mail services, and providing home collection kits.
In summary, adolescent females attending SBHCs are at increased risk for reinfection with up to approximately 26% in Baltimore becoming reinfected with chlamydia within 1 year of their first documented infection. Intensive behavioral and educational interventions should be offered to adolescents. Our nurse practitioners are now providing single dose treatment at diagnosis, individualized risk reduction counseling, condoms with education, partner notification, and recommending rescreening of infected individuals at 3 months. Schools represent a logical forum for students to access health services. The installation of additional SBHCs should be encouraged, along with school-wide screening programs for sexually active students.29
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