Determining risk markers for gonorrhea and chlamydial infection and reinfection among adolescents in public high schools.

Abstract

In response to high adolescent rates of Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (GC), Philadelphia began screening in all public high schools in 2003.
Data from 14,862 students who tested more than once in the Philadelphia High School STD Screening Program (PHSSSP) during the 2002-2006 school years were analyzed for factors associated with CT and GC infection. Multivariable Cox proportional hazards models and logistic regression models were constructed to identify characteristics associated with measured STD rates. A secondary analysis assessed short-term reinfection rates among participants retesting within the same school year.
In the primary analysis, over multiple years, the unadjusted female CT/GC rate was more than double that in males (6.0 vs. 2.4 cases per 100 person-years, respectively). Among students with a baseline positive, males had a higher rate than females (19.9 vs. 17.7 cases per 100 person-years, respectively). Among students with a positive test result, 13.6% were reinfected within the same school year. Females with named partners not treated had a higher reinfection rate than all others (85.5 vs. 40.1-45.2 cases per 100 person-years, respectively).
Clinicians and screening programs that offer STD testing to urban high school students, regardless of gender, should encourage those with a prior STD history to test more frequently. Clinicians should work with infected patients, especially females, to ensure their partners are treated.

Full text

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Determining Risk Markers for Gonorrhea and Chlamydial Infection
and Reinfection Among Adolescents in Public High Schools
GRETA L. ANSCHUETZ, MPH,* JENNIFER N. BECK, MPH,*† LENORE ASBEL, MD,*‡ MARTIN GOLDBERG,*
MELINDA E. SALMON,*§ AND C. VICTOR SPAIN, DVM, PHD,*
Background:
trachomatis (CT) and Neisseria gonorrhoeae (GC), Philadelphia began
screening in all public high schools in 2003.
Methods: Data from 14,862 students who tested more than once in
the Philadelphia High School STD Screening Program (PHSSSP) dur-
ing the 2002–2006 school years were analyzed for factors associated
with CT and GC infection. Multivariable Cox proportional hazards
models and logistic regression models were constructed to identify
characteristics associated with measured STD rates. A secondary anal-
ysis assessed short-term reinfection rates among participants retesting
within the same school year.
Results:
In the primary analysis, over multiple years, the unad-
justed female CT/GC rate was more than double that in males (6.0 vs.
2.4 cases per 100 person-years, respectively). Among students with a
baseline positive, males had a higher rate than females (19.9 vs. 17.7 cases
per 100 person-years, respectively). Among students with a positive test
result, 13.6% were reinfected within the same school year. Females with
named partners not treated had a higher reinfection rate than all others
(85.5 vs. 40.1–45.2 cases per 100 person-years, respectively).
Conclusions:
Clinicians and screening programs that offer STD
testing to urban high school students, regardless of gender, should
encourage those with a prior STD history to test more frequently.
Clinicians should work with infected patients, especially females, to
ensure their partners are treated.
In response to high adolescent rates of Chlamydia
TRADITIONAL SCREENING PROGRAMS for Chlamydia tra-
chomatis (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 ne-
glected testing male adolescents, who serve as an important res-
ervoir of infection for females.1,2Knowledge 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.3–7More recently, males from the general population
have been screened for CT/GC either through school screening
programs8–10or venues which traditionally only offered screening
to females.11Current recommendations to clinicians include
screening all women under 25 years with no similar recommen-
dation 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.
Methods
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 stu-
dents. 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; Gen-
probe Inc., San Diego, CA). A clinician returns to the school to
Correspondence: Greta L. Anschuetz, Philadelphia Department of Public
Health, Division of Disease Control (DDC), 500 S Broad St, Philadelphia, PA
19146. E-mail: greta.anschuetz@phila.gov.
Received for publication April 9, 2008, and accepted July 8, 2008.
From the *Philadelphia Department of Public Health, Philadelphia,
Pennsylvania; †Drexel University School of Public Health,
Philadelphia, Pennsylvania‡Drexel University College of Medicine,
Philadelphia, Pennsylvania; and §Centers for Disease Control and
Prevention, NCHHSTP, Philadelphia, Pennsylvania
Sexually Transmitted Diseases, January 2009, Vol. 36, No. 1, p.4–8
DOI: 10.1097/OLQ.0b013e3181860108
Copyright © 2008, American Sexually Transmitted Diseases Association
All rights reserved.
4

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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.13In 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 docu-
mented 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 dis-
ease-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 ad-
mission 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 ad-
mission 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 inter-
viewed by public health staff. During public health interviews,
information on sexual contacts was collected in order to con-
duct 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).14The final model provided adjusted hazard
ratios (AHR) with 95% confidence intervals for variables associ-
ated 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 covari-
ance matrix.15Selected 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.16Because 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 Re-
view Board.
Results
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 resi-
dential 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 obser-
vations (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.
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
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5 RISK MARKERS FOR GONORRHEA AND CHLAMYDIAL INFECTION

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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 com-
pared 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 dis-
ciplinary 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).
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 be-
cause 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) com-
pared 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 candi-
date 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 associa-
tion 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).
Discussion
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 reinfec-
tion 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
TABLE 1. Characteristics Associated with Measured Gonorrhea and Chlamydial Rates Among High School Students
Males Females
N*
%
Positive
#
Days†
CT/GC
Rate‡
AHR§
95% CIN*
%
Positive
#
Days†
CT/GC
Rate‡
AHR§
95% CI
Baseline test result
Negative
Positive
p-value
Age at endpoint
12–15 y
16–17 y
18–20 y
p-value
Race/ethnicity
Other
Non-Hispanic
black
p-value
School type at
endpoint
Magnet
NEI/CIT
Alternative
p-value
10244
150
2.4
18.7
371
302
2.2
19.9
1.0
8.7
8,461
452
6.0
18.1
368
334
5.5
17.7
1.0
3.35.5–13.8
?0.01
2.5–4.2
?0.01
1,803
7,066
1,525
1.5
2.6
4.3
335
371
392
1.6
2.3
3.5
1.0
1.0
1.1
1,669
6,198
1,046
6.2
6.7
7.3
332
371
394
6.8
5.9
5.8
1.0
0.6
0.4
0.7–1.5
0.7–1.8
0.68
0.5–0.7
0.3–0.6
?0.01
2,793
7,601
1.2
3.2
376
365
1.1
2.9
1.0
2.1
2,413
6,500
3.8
7.7
374
360
3.4
7.0
1.0
1.71.4–3.1 1.4–2.2
?0.01
?0.01
1999
8,039
356
1.0
2.9
6.5
378
369
338
0.9
2.6
6.0
1.0
2.3
4.6
2,717
6,030
166
4.2
7.5
15.1
364
365
370
3.9
6.8
13.1
1.0
1.5
2.5
1.4–3.6
2.3–9.2
?0.01
1.2–1.8
1.5–4.0
?0.01
*Number of testing events, not the number of unique individuals.
†Median number of days between baseline and event test.
‡Number of events per 100 person years.
§Adjusted Hazard Ratios (AHR) are adjusted for baseline test result, age, race/ethnicity, school type at endpoint and home ZIP code reported adolescent Chlamydial
morbidity.
6
Sexually Transmitted Diseases ● January 2009
ANSCHUETZ ET AL.

Page 4

studies recruited males from high risk populations, such as STD
clinics6,7or 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 rein-
fections, 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.18–21In a recent
study, Niccolai et al.1reported 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 part-
ner 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 treat-
ment of partners may reduce the measured CT/GC reinfection
rates, especially for females. More studies are needed to under-
stand 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. Ex-
pedited 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.
Fig. 1.Measured CT/GC Rates for selected risk factor profiles based on gender and 2 other risk factorsa
0
5
10
15
20
25
#1#2 #3#4#5 #6#7
Measured CT/GC rate
(per 100 person-years)

% population
CT/GC rate
Gender
Age Group
School type Magnet Alternative
Baseline
diagnosis
Any
#1
7.4%
1.0
M
16-17y
#2
1.3%
6.2
M
16-17y
#3
7.9%
3.5
M
18-20y
Any
#4
10.1%
3.9
F
16-17y
Magnet
#5 #6
1.6%
16.9
F
16-17y
Any
#7
5.1%
5.0
F
18-20y
Any




21.5%
6.7
F
16-17y
NEI/CIT
LEGEND
b

Any Any Any Any Pos. Neg.
aThe above figure represents selected subgroups with a measured CT/GC rate above the sex-specific average representing ?1% (N ? 193)
of the population. For comparison, some low CT/GC rate subgroups have been included.
bRate per 100 person-years.
TABLE 2.Association between Partner(s) Treatment Status and Reinfection within the Same School Year
Student’s Gender & Partner(s) Treatment StatusN% PositiveCT/GC Rate* OR95% CI
p-Value
Females w/named Partner(s) none treated
Males w/named Partner(s) none treated
Males w/other status for partners†
Females w/other status for partners†
66
15
132
363
24.2
13.3
12.9
11.9
85.5
45.2
40.8
40.1
2.5
1.2
1.1
1.0
1.3–4.7
0.3–5.72
0.6–2.0
ref.
?0.01
0.79
0.77
*Number of events per 100 person years.
†Other treatment status is the combination of adolescents who refused to name partners, those who had some partners’ treated and those who had all partners’
treated.
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All age groups, with the exception of the youngest males,
demonstrated sufficient prevalence of CT/GC infections to jus-
tify 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
20yearsolds.Moreanalysesareneededtounderstandtherelationship
between age group and measured CT/GC rates among females.
Our findings are consistent with others3,4showing that disci-
plinary 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,22suggesting that infection and rein-
fection rates may be lower in many suburban and rural high
school populations. Of the 33,036 students excluded from anal-
ysis 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. Mea-
sured 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 screen-
ing, 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 reg-
ular 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 part-
ners are treated. Local public health agencies can often assist clini-
cians with partner notification and treatment.
Community based screening programs, such as PHSSSP, are
important for detecting and treating asymptomatic CT/GC in-
fections 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 his-
tory is not verifiable.
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