Determining Risk Markers for Gonorrhea and Chlamydial Infection and Reinfection Among Adolescents in Public High Schools : Sexually Transmitted Diseases

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Determining Risk Markers for Gonorrhea and Chlamydial Infection and Reinfection Among Adolescents in Public High Schools

Anschuetz, Greta L. MPH*; Beck, Jennifer N. MPH*†; Asbel, Lenore MD*‡; Goldberg, Martin*; Salmon, Melinda E.; Spain, C Victor DVM, PhD*

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Sexually Transmitted Diseases 36(1):p 4-8, January 2009. | DOI: 10.1097/OLQ.0b013e3181860108
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TRADITIONAL SCREENING PROGRAMS for Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (GC) infections among adolescents (those aged 15–19 years) from the general population have yielded little information about reinfection; many have neglected testing male adolescents, who serve as an important reservoir of infection for females.1,2 Knowledge is limited about infection, reinfection, and risk factors among adolescent males as screening has centered on juvenile detention centers or sexually transmitted disease (STD) clinics limiting the generalizability of the results.3–7 More recently, males from the general population have been screened for CT/GC either through school screening programs8–10 or venues which traditionally only offered screening to females.11 Current recommendations to clinicians include screening all women under 25 years with no similar recommendation for men.12

The Philadelphia High School STD Screening Program (PHSSSP) began in January 2003 as a means to identify and treat adolescents infected with CT/GC, and thereby reduce transmission and the sequelae of undiagnosed and untreated infections.8 PHSSSP provides longitudinal data on a general population of adolescents who potentially may receive 4 screening opportunities during their high school career, with additional testing available for those who test positive.

The objective of our analysis was to measure the rate of CT/GC infection and reinfection in a general population of urban high school students who participated at least twice in the PHSSSP. We identified demographic and personal characteristics associated with higher measured STD rates within the PHSSSP as well as characteristics associated with increased risk of reinfection within the same school year. By establishing characteristics of students at high-risk for infection and reinfection, school based programs can tailor their screening efforts to assure that the most appropriate student populations are reached and guide decision making for prospective testers. Furthermore, clinicians can identify groups with a higher measured STD rate that are likely to benefit from more frequent screening, even when asymptomatic.


Source of Data

Detailed methods of the PHSSSP have been previously reported.8 In brief, the Philadelphia Department of Public Health (PDPH), STD Control Program began offering urine tests for CT/GC in the 2002–2003 school year and currently reaches 69 of the 71 public high schools (grades 9–12) in Philadelphia County. The two high schools excluded include one operated within the prison system, which screens their students for CT/GC upon intake and a special education high school. Staff visit the public high schools yearly and provide educational sessions on STDs. Following the brief educational session, confidential screening is offered to all students. Each student is given a paper bag that contains a form to collect demographic information, a urine cup, and a card with information on how to get test results. All students complete the demographic form, and then are escorted to a bathroom. There they make the decision whether to provide a urine specimen for testing. Specimens submitted are tested for CT and GC by a nucleic acid amplification test (APTIMA Combo 2 Assay; Genprobe Inc., San Diego, CA). A clinician returns to the school to provide treatment for students testing positive, typically one week following testing.

Beginning in the 2003–2004 school year, PDPH staff have actively contacted students testing positive during the annual school screening for retesting 3 to 4 months following their treatment, in accordance with CDC guidelines for females positive for CT.13 In order to protect confidentiality, students are contacted for retesting only if they can be located in the school where they were originally tested. Students tested after March 1 are ineligible for retesting, as schools are closed before 3 months have passed.

Two sets of analyses were conducted. The primary analysis focused on students (regardless of infection status) who retested over 2 or more school years, whereas the secondary analysis focused on students who tested positive and retested within the same year.

CT/GC Infection Rates Over Multiple Years

The primary analysis being presented used successive pairs of tests on Philadelphia students with at least 2 valid PHSSSP tests collected from different school years between 2002 and 2006. The analysis was limited to students between the ages of 12 and 20 years with ≤3 years between successive testing, and with documented treatment from all infections detected.

For each successive pair of tests, the follow-up time was defined as the time between the first (“baseline”) and the second test (“endpoint”). If a student was positive at baseline, time was calculated from treatment date to endpoint. The outcome variable was the result for CT and/or GC at the endpoint test. Candidate risk factors/markers were baseline test result (categorized as STD disease-free or of having a positive STD test), age group at endpoint (12–15 years, 16–17 years, or 18–20 years), race/ethnicity (self-identification as non-Hispanic black or any other race/ethnicity), and school type at endpoint (magnet, neighborhood/city-wide admission and disciplinary schools). Adolescents in the 12 to 15 year age group were primarily over 14 years of age (97.8%). As infection patterns were similar, neighborhood and city-wide admission schools types were combined. Adolescent Home ZIP code reported morbidity was a continuous variable calculated from the 2006 reported morbidity of CT cases among adolescents aged 15 to 19 years from the students’ home ZIP codes. This variable was used as a proxy for the students’ level of CT exposure in their neighborhood. Students who failed to provide a home ZIP code, but attended a neighborhood school (<1% of subjects), were assigned the most commonly reported ZIP code of residence from all the students attending that school.

CT/GC Reinfection Within the Same School Year

In a secondary analysis, we identified risk factors/markers associated with reinfection rates among students who tested positive for CT and/or GC and retested within the same school year. Students were eligible for this analysis if they had a positive screening test with confirmed treatment in the regular PHSSSP within the 2003–2006 school years and were interviewed by public health staff. During public health interviews, information on sexual contacts was collected in order to conduct partner notification and treatment.

The outcome variable of the secondary analysis was the retest result for CT and/or GC. Time between treatment of baseline infection and retest was categorized at ≤4 months or >4 months. Partners treatment status categorized students as those who named partners who PDPH could not locate or confirm treatment or as those with other partners treatment statuses. The other partners’ treatment statuses group combined students who refused to name partners and students who had some or all of their named partners treated. The other partners’ treatment statuses were combined because of similarities in reinfection rates. Also, age group (at time of initial test for subset analysis), race/ethnicity, school type, and home ZIP code adolescent reported morbidity were evaluated as candidate risk factors as described above.

Data Analysis

Data on PHSSSP participants are stored in a person-centered database at PDPH. All analyses used SAS version 9.1 (SAS Institute, Inc, Cary, NC). In the primary analysis, associations were evaluated using multivariable survival analysis (Cox proportional hazards modeling).14 The final model provided adjusted hazard ratios (AHR) with 95% confidence intervals for variables associated with measured CT/GC rates. We controlled for the lack of independence among repeated observations on the same person using the robust sandwich estimate of Lin and Wei for the covariance matrix.15 Selected profiles were constructed by combining gender and ≥ 2 risk factors/markers to identify high-risk groups. Measured STD rates were calculated for demographic profiles which represented at least 1.5% of the population. In the secondary analysis, logistic regression provided adjusted odds ratios and 95% confidence intervals for variables associated with reinfection within the same school year.

Plausible interactions (effect modification) were evaluated one at a time using the likelihood ratio test.16 Because of interaction between gender and other risk factors, all final analyses were stratified by gender. In the model building process, we used best subsets modeling to determine which set of risk factors were the best predictors for the outcome.

These analyses were approved by the PDPH Institutional Review Board.


CT/GC Infection Rates Over Multiple Years

Approximately 30,000 (55%) of the close to 55,000 enrolled students attend the PHSSSP education session each year and are given the opportunity to test for CT and GC. From 69,029 tests from 49,871 individual students tested from 2002–2006 within the PHSSSP, 1,824 (3.7%) were ineligible for analysis because of missing date of birth, being ≥21 years of age, or having a residential ZIP code outside of Philadelphia County. An additional 33,036 students had only one valid test within the PHSSSP. From the remaining eligible screen results, 210 (1.1%) of 19,597 observations (paired tests) were ineligible for having >3 years between test dates or having the tests occur within the same school year. Overall, 19,307 observations (paired tests) from 14,862 students were included in the primary analysis. Positivity increased among students as the number of school years between tests increased: 4.3% (698/16,241) positive when the second test occurred in the next school year, 5.4% (149/2,737) positive when two school years lapsed between tests, and 5.8% (19/310) positive when three school years lapsed between tests. The population was predominantly black with the majority attending neighborhood schools (Table 1). More males than females were tested in PHSSSP.

Characteristics Associated with Measured Gonorrhea and Chlamydial Rates Among High School Students

Total positivity among those observations meeting inclusion criteria was 4.5% (866/19,307). CT infection alone was found most commonly(783) but an additional 50 infections were GC only, and 33 were dual infections with CT and GC. Among males, the unadjusted CT/GC rate was 2.4 cases per 100 person-years calculated from 274 infections among 10,394 observations. For females, the unadjusted CT/GC rate was 2.5 times as high (6.0 cases per 100 person-years) based on 592 infections among 8,913 observations. Median time between tests for both genders was 369 days with a range of 133 days to 1,095 days.

In multivariable analyses, both males and females with baseline positive tests had a higher measured CT/GC rate than those with baseline negative tests with the effect being stronger for males (Table 1). For males, a linear association between age group and measured CT/GC rate was detected, with older males having a higher rate compared to younger males. Females, aged 18 to 20, had a higher positivity compared to younger females, but when time was factored in they had the lowest CT/GC rates. Non-Hispanic black students had a higher measured CT/GC rate compared to all other reported race/ethnicity groups regardless of gender. Finally, students in disciplinary schools had the highest measured CT/GC rates among school types, with females from disciplinary schools having twice the measured CT/GC rates of males. These results are driven by CT as that is the more prevalent infection detected in the PHSSSP. Seven profiles were formed that represented combinations 3 or more risk factors/markers for higher risk (Fig. 1).

Fig. 1:
Measured CT/GC Rates for selected risk factor profiles based on gender and 2 other risk factors

CT/GC Reinfection Within the Same School Year

In the 2003–2006 school years (years in which active retesting of positives was conducted), 2,269 CT and/or GC infections were detected; 677 (29.8%) of these students were retested within the same school year. Most students (41.8%) were not retested because they had a positive test after March 1. Additionally, 28.4% of students were not in attendance at their original school on the days PHSSSP returned for retesting. Of those retested, 576 (85.1%) met the selection criteria for the reinfection analysis.

Among eligible students, 13.6% (78/576) were reinfected within the same school year. Among those reinfected, the median time until the second infection was detected was 127 days (range: 62–232 days). Most students (316/576 – 54.9%) did not name any sexual partners during interview, while 39.1% (225) named 1 partner and 6.1% (35) named 2 to 3 partners. Overall, adolescents who named partners who PDPH could not locate and/or confirm treatment for had a reinfection positivity of 22.2% (18/81) compared to 12.1% (60/495) among the other groups (refused to name partners: 13.3% (42/316)), some treated: 12.5% (2/16), and all treated: 9.8% (16/163). In multivariable analyses, only one candidate risk factor – Partners Treatment Status – remained significant and was retained; students who named partners who PDPH could not locate for treatment had the highest risk of reinfection (P = 0.05). Partners treatment status had a different effect for males and females (Table 2). Among males, we found only a weak association between partner treatment status and reinfection. However, if a female named partners and PDPH could not locate any of them for treatment, she was more than twice as likely as other females to become reinfected (OR = 2.5, 95% CI: 1.3–4.7). Measured reinfection rates within the same school year for females whose named partners were not treated was 85.5 cases per 100 person-years followed compared to 40.1 to 45.2 cases per 100 person-years for all other groups (Table 2).

Association between Partner(s) Treatment Status and Reinfection within the Same School Year


Across multiple years, the highest measured CT/GC rates in PHSSSP was a subsequent infection among those with a baseline positive test result in PHSSSP. Among those with a baseline positive test, males had an even higher measured CT/GC reinfection rates than females. Our results show that retesting adolescents with a prior positive is important for both males and females. We are not aware of any reinfection studies conducted with general adolescent populations that included males. Published reinfection studies recruited males from high risk populations, such as STD clinics6,7 or juvenile detention centers.4,5

Within the same school year, we found that females whose named partners are not treated appear to be a subgroup particularly vulnerable to reinfection over the first 4 months, on average, following treatment. The lower measured reinfection rate in other groups suggests that partner notification and treatment may reduce the risk of reinfection, especially in females. Based on published data, we expect that if any treatment failure exists, it would be <5%; persistent infections are difficult to distinguish from reinfections, however, as risk factors, such as resuming sex with an untreated partner, do not always change after infection.17

Most previous reinfection studies have focused on women and have reported reinfection rates that vary by the STD infections included, time followed, and population included.18–21 In a recent study, Niccolai et al.1 reported a CT reinfection rate for adolescent females of 50.5 cases per 100 person-years (reported as 42.1 cases per 1,000 person-months) from 1998–2001 among females in urban Connecticut. The population recruited by Niccolai is fairly high risk with half pregnant at enrollment and 52.6% reporting a CT infection before enrollment. In the current study, the measured CT/GC rate among females whose named partners could not be located for treatment (85.5 cases per 100 person-years) was higher than that reported by Niccolai. However, females with other partner treatment status (40.1 cases per 100 person-years) and males, regardless of partner treatment status (40.8–45.2 cases per 100 person-years) had lower rates. The measured CT/GC reinfection rates reported over multiple school years (19.0 cases in males and 17.7 cases in females) are most likely underestimates as the time to rescreening overestimates the time to infection, and will lower the calculated CT/GC rates. Current guidelines recommend that only females with CT/GC infection be retested approximately 3 months following treatment, but males may benefit equally from a similar recommendation. Our results also show that ensuring treatment of partners may reduce the measured CT/GC reinfection rates, especially for females. More studies are needed to understand why reinfection is similar for those who do not name partners, whose named partners have confirmed treatment, or whose named partners are not all treated and why reinfection is still greater than 40 cases per 100 person-years even among adolescents whose named partners have confirmed treatment. Expedited partner therapy (EPT) could potentially reduce reinfection rates. Local guidelines, however, such as those that govern PHSSSP, may not allow for EPT in some communities.

All age groups, with the exception of the youngest males, demonstrated sufficient prevalence of CT/GC infections to justify making screening opportunities available in high schools. The measured CT/GC rates among females showed a decreasing trend as age increases, whereas the positivity was positively associated with age at testing. Potentially, the measured CT/GC rate is being influenced by the longer time between tests among 18 to 20 years olds. More analyses are needed to understand the relationship between age group and measured CT/GC rates among females.

Our findings are consistent with others3,4 showing that disciplinary school students have higher measured STD rates than other adolescents. When time and funds permit, testing and treating in disciplinary schools more frequently (i.e., more than once a year) may aid in reducing the measured STD rates in adolescents.

We expect our results are generalizable to similar urban high school populations. CT/GC rates in urban areas, based on reported CT/GC morbidity, is typically higher than in the United States as a whole,22 suggesting that infection and reinfection rates may be lower in many suburban and rural high school populations. Of the 33,036 students excluded from analysis because they had only 1 test in the PHSSSP, an estimated 16,451 (49.7%) tested for the first time as seniors and/or had their first test in Year 4 limiting their opportunity to test again in PHSSSP during the years covered by the analysis. Students self select to screen each year allowing those who do not perceive themselves to be at risk to opt out or those who have recently tested outside of the PHSSSP to forgo testing. Measured CT/GC rates in the PHSSSP may overestimate that from the general high school student population if low risk students elect not to be tested. Conversely, high-risk students may be absent or choose not to retest leading to an underestimation of the true STD rate. Of note, within Philadelphia public high schools approximately 20% of students are absent daily.23 PHSSSP did not locate >50% of students eligible for retesting within the same school year increasing the risk of a selection bias in our reinfection rate estimates. If students who are chronically absent from school are at higher risk for contracting STDs, then our results would underestimate the true short-term reinfection risk in this population. Including test results from other venues is not possible as only positive test results are reportable to the health department. Finally, because we have interval-censored data, (i.e., we do not have the exact date that a student became infected) we are overestimating the time to infection for most students. Therefore, our measured CT/GC rates will usually underestimate the true CT/GC rate.

Strengths of this analysis include the fact that the PHSSSP reaches all public high schools in Philadelphia and tests between 15,000 to 20,000 students a year, making it the largest school STD screening program in the United States and allows for the most comprehensive look at STD rates within an urban high school population, to date.

When prioritizing asymptomatic individuals for CT screening, clinicians should place a higher priority on adolescents with a previous STD. Although prior testing history is not always available, knowledge of other risk factors may be enough to determine which adolescents may benefit from regular CT/GC screening. Our results suggest that clinicians should offer CT/GC testing regularly to those patients at higher risk, even if the patient is asymptomatic (Fig. 1). Also, to decrease the risk of reinfection, clinicians should work with patients, especially females, infected with CT/GC to ensure their sexual partners are treated. Local public health agencies can often assist clinicians with partner notification and treatment.

Community based screening programs, such as PHSSSP, are important for detecting and treating asymptomatic CT/GC infections missed in other venues. These screening programs should ensure that adolescents with a prior positive infection are strongly encouraged to retest. Active follow-up is important for students, especially females, whose partners’ treatment history is not verifiable.


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