CHLAMYDIA TRACHOMATIS (CT) AND NEISSERIA GONORRHOEAE (GC) infections are the most commonly reported sexually transmitted diseases (STDs) in the United States with an estimated 3 million CT and 650,000 GC infections occurring each year.1 Adolescents and young adults are disproportionately affected by these STDs. In 2003, 634,916 (72%) of the 877,478 reported cases of CT and 197,270 (58%) of the 335,104 reported cases of GC were among persons aged 15 to 24 years.2 Nationally, the estimated costs associated with the multiple complications of CT infections exceed $1.88 billion annually.3 Because most chlamydial infections are asymptomatic,4–6 active screening and treatment programs are critical for the prevention of these complications.7 With the second highest CT rate (1189.3 per 100,000 persons) of large U.S. cities (>200,000 residents) in 2003 and a predominance of these infections among 15 to 19 year olds,2 Philadelphia has a critical need for STD reduction among adolescents.
Given that adolescents are less likely than others to seek or receive appropriate preventive health services and STD screening,8–10 school-based screening and treatment programs may be an acceptable and cost-effective alternative mechanism to identify infections among this population.6,11–13 When school-based health clinics (SBHCs) exist, they can provide general medical care, including STD testing and education on sexual health issues to enrolled students; however, SBHCs are present in less than 6.5% of U.S. public schools.14 The availability of urine-based nucleic acid amplification testing (NAAT) facilitates testing, making screening for CT and GC possible in nonclinical settings, including schools without SBHCs.
The Philadelphia Department of Public Health (PDPH), with the support of the School District of Philadelphia (SDP), initiated a voluntary school-based education and screening program to identify and treat CT and GC infections among the adolescents attending Philadelphia public high schools.
The SDP is the seventh largest public school system in the nation15 with 55,832 students enrolled in grades 9 through 12 during the 2002–2003 school year. On January 6, 2003, the PDPH initiated the High School STD Screening Program (PHSSSP).
Before the implementation of PHSSSP, the SDP sent a letter to parents or guardians of high school students describing the risks of chlamydial infections, the high rates of infection in Philadelphia, and the nature of the voluntary screening program. In the letter, parents were encouraged to discuss the problem of STDs with their children; however, parental consent was not sought in accordance with Pennsylvania regulations.16
For the PHSSSP, groups of approximately 60 students attended an educational and screening session. PDPH staff met with individual school administrators to set up screening in each high school. Over a 5-month period, sessions were conducted at every school. Each high school's sessions were scheduled to ensure that each child enrolled in the high school was scheduled to attend a session for one period during the school day. Although every child was scheduled to attend a session, some students were missed because of absence or truancy. Placing students in groups of 60 allowed for control of the class while ensuring that the PDPH was able to schedule screening for all students over the school year.
The 25-minute educational portion was interactive and included an overview of common STDs and risk factors for STDs with an emphasis on CT and GC. Specially trained disease intervention specialists (DIS) and STD educators led the education and screening sessions. During the sessions, the confidential and voluntary nature of screening was emphasized, and students were informed that free and confidential treatment would be made available for those who tested positive. Screening was available for all students who attended the educational sessions; however, the importance of screening for those who had ever engaged in sexual intercourse was emphasized.
Every student was given a testing kit, consisting of a brown paper bag with: 1) a form to be completed by the students that requested name, date of birth, address, phone number, racial identification (including Hispanic as a category), their preferred method for PDPH staff to contact them, and a self-selected secret code; 2) a urine collection cup; and 3) a card with a PDPH telephone number to call for test results. Students were instructed to provide urine specimens if they wanted to be tested. Small groups of students, approximately equal to the number of stalls in the restrooms, were then accompanied to the restrooms by PDPH staff who collected testing kits as students exited the restrooms whether (or not) a urine specimen was provided. Submitted urine specimens were aliquotted into transport tubes and brought to the PDPH Public Health Laboratory (PHL) for testing.
Submitted urine specimens were tested for N. gonorrhoeae and C. trachomatis at the PDPH PHL by nucleic acid amplification testing (APTIMA Combo 2 Assay; Genprobe Inc., San Diego, CA) according to the manufacturer's instructions. All positive specimens underwent repeat testing using the same method. Per PDPH-PHL protocol, only specimens that tested positive on both tests were reported out as positive.
Students who telephoned PDPH were given their test results after confirmation of their secret code. Students with positive test results were informed when PDPH staff would be present at their school to provide treatment, were instructed to abstain from sex until completing treatment, and were encouraged to ensure that their partners received treatment. Those with partners in the same school were told that partners could come to “in-school” treatment sessions. The staff at each school established procedures to assure confidential attendance of treatment sessions for students. PDPH staff attempted to confidentially inform all students with positive results who did not call for results about the treatment session at their school.
When students with positive test results reported to “in-school” treatment sessions, a PDPH clinician provided a single-dose observed therapy: 1 g azithromycin, orally for the treatment of chlamydial infection and/or 400 mg cefixime orally for the treatment of gonococcal infection. Students reporting an allergy or other contraindication to these regimens were referred to a public health center or to their private physician for an appropriate alternative treatment. All students who obtained treatment through the PDPH, either at school treatment sessions or at PDPH clinics, were provided STD risk avoidance counseling, were referred to a PDPH clinic or outside/independent family planning clinics for complete STD and HIV testing, and were provided referral cards listing PDPH clinic sites for their sexual partners. Students with symptoms of pelvic inflammatory disease or epididymitis were treated and referred to an STD clinic, family planning clinic, or provider of their choice for immediate evaluation.
PDPH DIS staff actively followed up with those students who had positive test results but did not attend the school-based treatment sessions. Assistance, including transportation, was offered to students to facilitate evaluation and treatment either at a PDPH clinic or a healthcare provider of choice. DIS staff contacted healthcare providers to confirm appropriate treatment had been given.
Test results, treatment information, and data collected from information forms completed by students were entered into the PDPH Disease Control Management System (DCMS) database, which is used to track reportable STDs in the city of Philadelphia.
Analyses were limited to students with valid dates of birth who were between the ages of 12 and 20 years at the time of screening. If a student submitted a specimen at more than one educational session, only the first specimen was included in the current analyses. Thirty-one students provided 2 specimens for testing. Second tests occurred when students changed schools (n = 15), were present in 2 classes that attended sessions (n = 7), or requested repeat testing to verify positive test results (n = 9). The results were the same for both specimens for all but 3 students. For 2 students, the first specimen was positive for CT, and both were treated before second specimen collection. The third student tested positive for GC only on the second specimen, which was collected 2 weeks after the initial negative specimen.
The overall prevalence, as well as sex-, age-, race-, school type-, and residential CT morbidity area-specific prevalences were calculated by dividing the number of positive tests by the total number tested in each group. Residential CT morbidity areas, which are not necessarily geographically contiguous, are zip code groupings based on 2002 rates of reported chlamydial infections among all 12- to 20-year-old Philadelphia residents. The residential CT morbidity areas were categorized as high (>3800 per 100,000 12–20 year olds), medium (1500–3799 per 100,000), or low (<1500 per 100,000). To assess the association between CT and GC outcomes and factors of interest, crude prevalence ratios (PRs) and 95% confidence intervals (95% CIs) were calculated in SAS 8.2.17 Within-group correlations were accounted for in school type and residential morbidity area analyses.
Of the approximately 30,000 students who attended the PHSSSP, 19,701 (>65%) individuals submitted specimens adequate for testing; approximately 40 specimens were rejected because of insufficient quantity in transport tube. The current analyses comprise 19,394 students between 12 and 20 years old (Table 1), excluding 259 (1.3%) individuals with missing birth dates and 48 (0.2%) persons over the age of 20 (excluding 2 positive individuals from the analysis). Students who submitted specimens were generally similar to the approximately 55,800 Philadelphia public high school students in grades 9 to 12 regarding race (65% black, 16% white, 11% Hispanic, and 6% Asian) and sex (49.8% male). Most screened students attended neighborhood public high schools (59.1%), 16.0% attended magnet schools, 8.2% attended schools with special entry requirements, 13.4% attended vocational schools, and the remaining 3.3% were at alternative disciplinary schools. A majority of students screened (52.8%) resided in areas with high CT morbidity, 28.8% lived in areas with moderate CT morbidity, and the remaining 17.9% of those with valid zip codes were from areas with low CT morbidity.
Among the students who submitted adequate specimens for testing, 1012 (5.2%) students tested positive for CT, 93 (0.5%) for GC, and 55 (0.3%) for both infections. Nearly 60% (55 of 93) of the screened students identified with GC infections also had CT coinfections.
Females had higher prevalence of infections than males. Among screened female students, the prevalence of CT was 8.1% and GC was 0.8% (Table 1), which are 3.3 and 5.1 times higher than the prevalence of CT (2.5%) and GC (0.2%) among male students, respectively. In addition, CT-GC coinfections were 7.3 times more common among females compared with males.
Generally, the prevalences of CT and GC were higher among older students. Compared with female students aged 12 to 14 years, females in the 2 older age groups had nearly one and a half times higher prevalence of CT and GC infections (Table 2). Among male students, this trend was even more pronounced. Compared with male students aged 12 to 14 years, the prevalence of CT was nearly 5 times higher among those aged 15 to 17 years and 8 times higher among those aged 18 to 20 years. Gonococcal infections were also more prevalent among older male students compared with those aged 12 to 14 years. Prevalences among the older adolescent groups were statistically significantly higher only for CT infections (Table 2). Among the females tested, over 20% of the 13 year olds had positive tests for CT, whereas no 20 year olds were positive for GC; however, small numbers of students in these age groups limit the interpretability of these findings.
Regardless of sex, the prevalence of CT was lowest among students who identified as white (females: 2.4% and males: 0.1%) and were highest among those who identified as black, 10.5% and 3.4%, respectively (Table 1). In sex-specific comparisons with white students as the referent group, CT infections were significantly higher for certain groups: 4.4 times higher for black females, 24.4 times for black males, 1.5 times for Hispanic females, and 8 times for Hispanic males (Table 2). In these comparisons, only GC and CT-GC coinfections were significantly more common among black females (Table 2). Infections were also more common among male and female students in the “other” racial category compared with white students.
Compared with students attending magnet schools, those attending all other types of schools had at least a 2-fold higher prevalence of CT with the highest CT prevalence (19.7%) among female students attending alternative disciplinary schools. Among female students, the prevalence of GC and dual infections among disciplinary school attendees were significantly higher (10.7–4.7) than the prevalence of these infections in female students at all other school types, except those at special admission schools (Table 2). Despite the variability in prevalence by school type, there was at least one positive result in each individual school.
Female students living in high CT morbidity areas had the highest prevalence of CT (9.9%), GC (1.1%), and dual infection (0. 7%), whereas those living in the lowest morbidity areas had the lowest prevalences of these infections (3.7%, 0.1%, and 0.1%, respectively) (Table 1). Male students living in high CT morbidity areas also had the highest prevalence of CT (3.1%); however, GC and dual infections were low for males in all areas.
Treatment Provided to Students With Positive Test Results
Nearly all (99.9%) of 1052 infected students were appropriately treated. Of those treated, 739 (70.3%) received treatment at “in-school” treatment sessions, whereas 235 (22.4%) were managed in PDPH categorical STD clinics, 35 (3.3%) in family planning clinics, and 42 (3.9%) in private doctors' offices or other PDPH clinics. The median time between testing and treatment was 5 days shorter for students who were treated during school treatment sessions (8 days) than for those treated in other settings (13 days, P <0.0001).
As the largest school-based GC/CT screening program in the United States to date, the PDPH educated over 30,000 students, tested over 19,700 individuals, and identified 1052 infected students, of which 1051 received treatment. We found that a broad-based screening program in schools, although labor-intensive, was readily acceptable to students and staff, and was not only feasible, but also successful for case finding and treatment. Our ability to test such a large number of students and treat those with positive test results demonstrates that local health departments and school districts can successfully collaborate to provide screening and treatment to large groups of adolescents.
The prevalence of either CT or GC infections (5.4%) among screened Philadelphia high school students is similar to those from other school-based screening initiatives, which ranged from 2.4% to 11%.11,12,18 Because sexually inexperienced or inactive students were not excluded from PHSSSP, the prevalences we found certainly underestimate the infection rates among sexually active students. Risk behavior and symptom histories were not collected; therefore, we could not better evaluate STD risks of students submitting specimens or the influence of factors such as sex, peer pressure, or sexual history on specimen submission.
We found large differences in CT and GC prevalence by sex, similar to those seen in other screening efforts—school-based or not.11–13,19 These differences may be explained by factors that have been previously described, including physiological/anatomic differences—the presence of columnar epithelial cells on the cervix—that make young women more susceptible to CT,20 males are more likely to be symptomatic and thus seek treatment,21 and partnership-related factors such as the propensity for younger women to have older partners and differences in partnership concurrency between males and females.22 There are also the unexamined possibilities that men may have a shorter duration of infection if left untreated or that current testing methodology may not detect infection harbored in sites other than the urethra.
Racial differences in the prevalence of infections were also identified, with black students having significantly higher prevalences than white students. Racial disparities in STDs among adolescents and young adults have been previously described.23,24 Higher prevalences among certain racial groups of adolescents have been attributed to higher prevalence of risk behaviors,25 increased risk associated with decreased socioeconomic status,26 and involvement in higher-risk sexual networks.27,28 Because race is a complicated construct, which represents a myriad of underlying differences between groups, including socioeconomic status,29–31 historical pressures,32 racism,33 and access/use of medical care,34 the role of race in the assessment of health disparities needs to be recognized as a marker rather than as a causal factor. Notably, in PHSSSP, the racial disparity was much greater among males than females; how gender and racial factors interact needs further study.
The associations for both school type and residential morbidity area were in the anticipated direction. School type-specific chlamydial prevalences in PHSSSP were similar to those found in the 1998–1999 school-based screening program in New Orleans, which found a low prevalence (0.7%) in the only academic magnet school and higher prevalences (4.1–13.4%) in the other 11 high schools.35 In the PHSSSP, students residing in areas with high CT morbidity were more likely to be infected than students residing in areas with low CT morbidity.
These “community-level” factors are quite complicated and undoubtedly comprise many influences on STD risk. Students may be more likely to choose their sexual partners from the area in which they reside or the schools they attend; therefore, sexual networks formed in areas of high morbidity are likely to sustain high STD morbidity.27,28,36 Additionally, people who reside in the same area may have shared beliefs, attitudes, and knowledge regarding sexual activity and STD prevention37; distinct patterns of medical care utilization (availability, access, and stigmatization)34; and similar experiences of social inequities such as income inequality38–43 and segregation.44 Differences by school types may be influenced by many of these same factors; students enrolled in the different types of schools are certainly not evenly distributed geographically across the city. Further assessment of school-level risk factors for high STD prevalence such as the ones currently assessed—school type and STD morbidity area—will improve the ability to target CT-GC screening efforts more effectively.
Given that the goal of screening programs is to prevent sequelae and decrease transmission, the success of any program is dependent not only on the ability to screen the at-risk population, but also on the ability to ensure the treatment of those who test positive. In the few instances in which treatment rates were reported from school-based screening programs, the rates ranged from 88% to 100%.11,13 In PHSSSP, our ability to provide single-dose therapy in the schools was a key element for successful treatment. Without SBHCs to provide treatment at various times during the school day, follow up with students absent from school during the treatment sessions was challenging.
In addition to preventing complications of asymptomatic infections, another goal of large-scale STD screening programs is to eliminate prevalent cases that allow for infection to be sustained in a sexual network. A few large-scale nonschool-based screening programs that have been in place for several years have led to decreases in prevalence.45,46 One longitudinal school-based program showed a decrease in the prevalence of chlamydial infections over time, although the decrease was only significant in males.47 We anticipate a reduction in the prevalence of chlamydial and gonococcal infections in the Philadelphia high school population as well as in the community at large as a result of continued annual screening and treatment in Philadelphia high schools. To further these efforts, we plan to enhance identification and treatment of infected persons by implementing active partner notification and repeat testing of infected students 3 months after treatment.
Although the students treated in the schools or PDPH STD clinics were counseled to have their sexual partners receive treatment, we only know about the few partners who attended the school treatment sessions as a result of our limited ability to track partners treated elsewhere. The feasibility and effectiveness of providing active partner notification for high school students who test positive in school-based screenings has not been previously evaluated. During the second academic year of screening, active partner notification services were added to the PHSSSP to try to eliminate these infections and for evaluation of such service provision.
Over 65% of the students who attended educational sessions in the schools provided a urine specimen for screening; however, those screened represent less than 40% of the students enrolled in these grades in the Philadelphia public school system. Participants in PHSSSP had similar demographics to the overall student body. Students who did not attend the educational sessions could also have been infected with either of these bacterial STDs. According to the 2003 Youth Risk Behavior Survey, 63.9% of Philadelphia public high school students report a history of sexual intercourse at least once.48 With a liberal assumption that all students who submitted specimens had engaged in sexual intercourse, we failed to screen approximately 15,000 sexually active students. If the nonscreened student population had STD prevalences similar to those who were screened, then we missed approximately 780 infections. In future years of PHSSSP, we will work to engage a larger portion of Philadelphia high school students.
A concern that has been raised regarding urine-based screening for CT and GC in nontraditional settings is that screening for HIV, syphilis, and other STDs may be precluded for those at increased risk for other infections, particularly those infected with CT or GC.49 Additional STD testing, that requires examination or more invasive procedures, may not be feasible in nonclinical high school settings. In PHSSSP, all infected students were counseled to seek follow up for comprehensive STD care. Given the high CT and GC rates among adolescents and the availability of noninvasive screening methods, school-based screenings can provide the essential initial link into traditional clinic-based health care for those adolescents at highest risk for other STDs.
In conclusion, we found and treated a large number of chlamydial and gonococcal infections among Philadelphia public school students residing in a city with one of the highest rates of chlamydial infections in the country. These infections were not found to be equally distributed across this school population. Both CT and GC infections were far more common in female students than in male students. When stratified by sex, the same factors were associated with higher levels of CT infections in both females and males: black racial identification, alternatively disciplinary school attendance, and living in an area with a high underlying prevalence of CT. However, the majority of CT and GC infections in both males and females were found in neighborhood schools, which rules against targeting interventions at “high-risk” schools. Although targeted interventions, aimed at residents of certain high morbidity areas or racial groups, may be shown to be more cost-effective in the future, it is likely to be more difficult to implement such programs while ensuring confidential testing.
As the largest school-based screening effort to date, this project should demonstrate to others in STD prevention that it is not only possible to undertake such screening programs in public high schools, but that these efforts can also lead to the identification and treatment of STDs that might otherwise go undetected. Hopefully, by sustaining this large school-based program, we will be able to demonstrate a decrease in the prevalence of these STDs not only in high school students, but in the community at large as well.
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