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Subsequent Sexually Transmitted Infection in Urban Adolescents and Young Adults
Donald P. Orr, MD;
Krystal Johnston, MD;
Edward Brizendine, MS;
Barry Katz, MD;
J. Dennis Fortenberry, MD, MS
Arch Pediatr Adolesc Med. 2001;155:947-953.
ABSTRACT
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Objective To compare the rates of subsequent infection with Chlamydia trachomatis, Neisseria gonorrhoeae,
or Trichomonas vaginalis in a group of high-risk
adolescents and young adults.
Methods At the time of treatment, 444 unmarried teenagers and young adults aged
13 to 25 years were enrolled from an urban sexually transmitted disease clinic
and 3 community-based primary care clinics. Subjects were infected with C trachomatis, N gonorrhoeae,
or T vaginalis, were diagnosed as having nongonococcal
urethritis (in men), or were uninfected sexual contacts with one of these
infections. Subjects returned at 1, 3, 5, and 7 months.
Results The rate of subsequent infection was substantial. Forty percent of men
and 53% of women who were uninfected contacts at enrollment were estimated
to be infected within 7 months; 60% of men and 73% of women infected at enrollment
were estimated to be reinfected. Among women, subjects who were infected at
enrollment had a shorter time to subsequent infection (median, 140 days) compared
with uninfected contacts (median, 209 days) (P =
.04). Among men, findings were similar, but the difference in median time
to subsequent infection was not significant (P =
.08). Baseline characteristics that predicted shorter time to reinfection
were female sex and infection at enrollment. When sexual behaviors in the
2 months preceding each subsequent data collection visit were included in
the model, only being female and reporting at least one new interval sexual
partner were significant predictors of subsequent sexually transmitted infections.
Conclusions These data support recent research that has found high rates of subsequent
infection among high-risk adolescents and young adults. Contacts of a sexually
transmitted infection appear to be at equally high risk for subsequent infection
as those with a personal history of infection. Our data suggest that more
frequent than annual screening for N gonorrhoeae, C trachomatis, and T vaginalis
would be appropriate in at-risk adolescent and young adult populations, including
individuals who are uninfected sexual contacts to a sexually transmitted infection.
INTRODUCTION
IN 1995, there were approximately 12 million new cases of sexually transmitted
infections (STIs) in the United States; two thirds of these occurred in individuals
younger than 25 years.1 There are significant
long-term consequences to untreated bacterial infection, including pelvic
inflammatory disease, infertility, increased risk for ectopic pregnancy, complications
of pregnancy, and chronic pelvic pain. Having one STI increases the risk of
acquiring others, including human immunodeficiency virus.2
Estimated direct and indirect costs of these infections reached $10 billion
in 1995.3
Although many infections (chlamydia, gonorrhea, and trichomonas) are
curable with appropriate antibiotic treatment, recurrent infection is common.
As many as 40% of annual chlamydial and gonorrheal infections occur in people
previously infected with those organisms4, 5, 6, 7;
little is known about recurrent infection with trichomonas.8
Most data on subsequent STI probably underestimate the disease burden, because
they focus only on recurrence of the original infectious organism. Because
these infections all have similar means of acquisition, and the presence of
multiple simultaneous infections is not uncommon,7
it is important to broaden the scope of analysis for recurrent STIs.
Current recommendations include annual screening for chlamydia and gonorrhea
among sexually active adolescents and young adults.9, 10, 11
Recent studies1, 12 suggest that
screening for STI on a more frequent basis (vs annual screening) may be indicated
for certain of these populations. Little information is available to guide
the clinician in screening other similar populations. The purpose of the present
study is to determine rates and predictors of subsequent infection with Chlamydia trachomatis, Neisseria gonorrhoeae, or Trichomonas vaginalis among adolescents
and young adults diagnosed as having an STI and those known to be uninfected
contacts of STI.
SUBJECTS AND METHODS
SUBJECTS
Unmarried adolescents and young adults aged 14 to 21 years were recruited
from a sexually transmitted disease (STD) clinic and 3 urban adolescent community
clinics at the time of treatment for chlamydia, gonorrhea, or trichomonas
infection or as a contact of a documented infection from March 1, 1996, through
November 30, 1998. Contacts who presented for treatment concurrent with a
subject who was enrolled because of a documented STI were eligible regardless
of age. These clinics serve a predominantly urban, African American, and low
to middle income population. Individuals were excluded from the study who
did not plan to continue residence in the area for the next 3 months or who
were pregnant. All eligible subjects were invited to participate. No information
was collected from persons who declined to participate.
Diagnostic criteria for infection at enrollment in women included culture
of endocervical secretions indicating the presence of C
trachomatis or N gonorrhoeae, and microscopic
examination of saline vaginal secretions revealing motile organisms consistent
with T vaginalis. In men, endourethral swabs were
cultured for chlamydia, and gram stain was performed to test for polymorphonuclear
leukocytes and intracellular diplococci (if results were negative, a culture
was performed). Nongonococcal urethritis was diagnosed in men when 10 or more
polymorphonuclear leukocytes were observed per high-power field under light
microscopy in the absence of gram-negative intracellular diplococci. Men were
not screened for trichomonas. Women found to have trichomonas based on findings
of the wet mount and men diagnosed as having gonorrhea or nongonococcal urethritis
based on the results of the gram stain were enrolled at this visit. The remainder
of subjects were enrolled at the time of antibiotic treatment based on the
above diagnostic test results or when presenting for treatment as a sexual
contact with one of these organisms. Contacts underwent a genital examination,
and specimens were obtained before treatment. All subjects, including contacts,
were treated with appropriate observed single-dose antibiotic therapy (1 g
of azithromycin, 400 mg of cefixime, and/or 2 g of metronidazole) according
to Centers for Disease Control and Prevention guidelines.9
Individuals with gonorrhea were also treated for chlamydia, regardless of
the results of the chlamydia culture. As part of standard clinic policy, all
subjects were informed that they required treatment either for an STI or because
they were a contact to an unnamed individual who had been treated for an STI.
Following treatment, subjects completed a questionnaire and structured interview
about sexual behaviors, condom use, substance use, and sociodemographic characteristics.
The study was approved by the Indiana University and Purdue University (Indianapolis)
institutional review board; written informed consent was obtained from all
subjects.
Subjects were asked to return 1, 3, 5, and 7 months after treatment.
At each visit, STI screening was performed. Chlamydia and gonorrhea were screened
by urine sample, using polymerase chain reaction (Amplicor PCR test kit; Roche
Diagnostic Corp, Indianapolis, Ind)13, 14;
women provided a self-obtained vaginal swab to culture for trichomonas, using
modified Diamond medium.15 A preliminary study
demonstrated that self-obtained vaginal swabs identified 25 of 25 vaginal
infections with T vaginalis compared with provider-obtained
vaginal swabs (D.P.O., oral communication, February 1996). The sensitivity
and specificity of polymerase chain reaction for N gonorrhoeae in urine samples were 89.5% and 99.7%, respectively, for women, and
96.4% and 99.1%, respectively, for men. The sensitivity and specificity for C trachomatis were 87.2% and 97.5%, respectively, in women,
and 94% and 98%, respectively, in men (B. Van Der Pol, BS, written communication,
March 30, 2001).
Subjects completed a questionnaire regarding activity and behaviors
in the preceding period. Subjects found to have an STI at return visits were
treated with appropriate observed single-dose oral antibiotics. They were
informed that their partners required similar treatment and that it was the
policy of the county health department to contact and treat all sexual partners.
STATISTICAL METHODS
Summary statistics for continuous data are presented as mean ±
SD, or as median (range) for skewed data. Categorical data are presented as
frequencies and percentages. t Tests and Wilcoxon
rank sum tests were used to compare means and medians between groups, respectively.
Pearson product moment correlation was used to compare categorical data between
groups. The median time to reinfection was estimated using the Kaplan-Meier
product-limit method. Log-rank tests were used to compare the reinfection
curves between those who were originally infected and those who were STI contacts
at enrollment.
One of the objectives of this study was to determine risk factors for
reinfection using baseline and interval sexual behavior data. Demographic
variables included in the model were age at enrollment, ethnicity, sex, and
initial infection status (infected vs contact). Data collected during the
study captured interim sexual behaviors in the 2 months before each follow-up
visit and included the number of partners, the number of events, the number
of unprotected events, and whether the subject had acquired a new partner.
For subjects who reported no sexual contacts during the interval 2 months,
the numbers of partners, events, and unprotected events were set at zero.
For analysis purposes, the numbers of partners, events, and unprotected events
were each categorized into 3 groups: none, 1, or 2 or more.
Cox proportional hazards regression models were used to model the time
to the first reinfection, using baseline predictors as the independent variables.
We chose not to treat the time to reinfection as interval-censored data. Instead,
we used a right-censoring approach and determined the total elapsed time from
enrollment to subsequent infection or to the last known visit with negative
test results. We defined the date of reinfection
as the date of the visit on which the subject tested positive for an STI.
If a subject never tested positive or was unavailable for follow-up, the subject
was censored at his or her last known visit. This gives the most conservative
time to subsequent infection by overestimating the actual time to reinfection.
We explored using different time points as estimates for date of reinfection.
We used the day after the last known visit with negative test results and
the midpoint between the last known visit with negative test results and the
visit with positive test results. Both of these definitions yielded the same
results as the more conservative definition. The proportional hazards assumption
was verified for each predictor variable using graphical methods. To assess
the effect of sexual behavior during the follow-up, multiple logistic regression
analysis was used to model the probability of infection at each subsequent
visit as a function of baseline predictors and interim behavioral factors.
Generalized estimating equations were used to account for the correlation
between visits on the same subject. All available visits for each subject
were included in the analysis. Commercially available statistical software
(SAS version 8.0; SAS Institute, Cary, NC) was used to perform the analyses.
RESULTS
Four hundred forty-four subjects were enrolled. Seventy-five percent
were women; 77% were African American. Men were older (mean ± SD, 18.3
± 2.0 years) than women (17.1 ± 1.9 years) (P<.001). About half of the subjects attended school (49%) and were
unemployed (47%). One hundred ten (25%) were enrolled as uninfected contacts
of STI, 200 (45%) were infected with C trachomatis,
97 (22%) with N gonorrhoeae, 59 (13%) with T vaginalis, and 25 (6%) had nongonococcal urethritis.
Simultaneous infection with more than one organism was observed: 29 subjects
(7%) were coinfected with chlamydia and gonorrhea, 7 women (2%) with chlamydia
and trichomonas, and 3 women (1%) with gonorrhea and trichomonas.
The group was at high risk for STI; overall, 62% reported a prior STI.
Men were at higher risk than were women, reporting a younger age at their
first episode of sexual intercourse (13.3 vs 14.2 years; P<.001) and more lifetime sexual partners (median, 12 [range, 1-100]
vs 5 [range, 1-350]; P<.001) and partners in the
2 months before enrollment (median, 1.5 [range, 0-15] vs 1.0 [range, 0-12]; P<.001).
At enrollment, women and African Americans were more likely to be infected.
Compared with uninfected contacts, adolescents and young adults with an STI
were younger, more likely to be enrolled in school, reported fewer sexual
partners in the 2 months before enrollment, and were more likely to have used
a condom at their last sexual encounter. There were no significant differences
between infected and contact groups in age at first intercourse or in number
of lifetime partners (Table 1).
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Table 1. Characteristics of Infected and Contact Groups
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Compared with subjects enrolled from the STD clinic, those recruited
from the adolescent clinics were more likely to be female, African American,
in school, to have used a condom at last coitus, and to have reported fewer
sexual partners in the 2 months before enrollment (data not shown).
Overall, 80% of subjects (n = 355) had at least one follow-up visit.
Three hundred thirty-seven subjects (76%) returned at 1 month, 262 (59%) at
3 months, 225 (51%) at 5 months, and 222 (50%) at 7 months. Compared with
those who were unavailable for follow-up, those who returned were more likely
to be female, African American, enrolled in school, infected with an STI at
enrollment, and to report more sexual partners in the 2 months before enrollment.
There were no significant differences in mean age at first intercourse, number
of lifetime partners, or reported condom use at last sexual encounter (data
not shown).
Subsequent infections were common, irrespective of the enrollment status. Figure 1 and Figure 2 depict the Kaplan-Meier curves for the time to subsequent
infection for women and men, respectively. Among the women, the median time
to subsequent STI was significantly shorter for those who had an STI at enrollment
(140 days) compared with the group who were enrolled as contacts of an STI
(209 days) (P = .04). By 7 months, among women, an
estimated 53% of the contacts and 73% of those with an STI at enrollment had
subsequent STI. The same pattern was observed among men, although it was not
statistically significant (P<.09). For men, the
median time to infection was 161 days among those enrolled with an STI and
217 days among the contacts. The proportions of the subjects estimated to
have an STI at each of the periods, derived using the Kaplan-Meier product-limit
method, are shown in Table 2. The percentages of subjects infected are not prevalence-type estimates (ie,
number of infected/number of subjects). Results of the proportional hazards
regression analysis to estimate the time to subsequent infection as a function
of baseline predictor variables are shown in Table 3. Women and those infected at enrollment had a shorter time
to reinfection. The repeated-measures multiple regression model that included
sexual behaviors in the 2 months before each follow-up visit (Table 4) demonstrated that being female and having at least one
new sexual partner independently increased the likelihood of subsequent infection.
Original infection status no longer was a significant predictor of subsequent
STI (P = .05).
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Figure 1. Kaplan-Meier curves depicting
the proportion of women who remained infection-free following enrollment and
initial antibiotic treatment.
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Figure 2. Kaplan-Meier curves depicting
the proportion of men who remained infection-free following enrollment and
initial antibiotic treatment.
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Table 2. Percentage of Subjects Estimated to Be Infected at Subsequent
Visits Derived From the Kaplan-Meier Product-Limit Method
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Table 3. Results of Proportional Hazards Regression Analysis to Model
Time to Reinfection as a Function of Baseline Variables
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Table 4. Results of Repeated-Measures Logistic Regression Analysis
to Estimate the Probability of Reinfection at Each Visit
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COMMENT
Subsequent infections with C trachomatis, N gonorrhoeae, or T vaginalis
were common in this population of adolescents and young adults, despite adequate
treatment with supervised antibiotics. Although the time to the acquisition
of a subsequent infection was longer for men and for those enrolled as a contact
of STI compared with those who had an STI at enrollment, 40% to 73% of subjects
were estimated to have become infected within 7 months after treatment. These
data add to the growing body of evidence demonstrating the substantial risk
of subsequent infection within a few months of an initial infection. In addition,
uninfected but at-risk adolescents and young adults also have high rates of
subsequent infection. Previous research has demonstrated that subsequent infections
with the same species are common among adolescent women. Preliminary work
by Fortenberry and Evans16 indicated that early
reinfection with C trachomatis was common among adolescent
women. Blythe and colleagues6 found that 38%
of adolescent women receiving reproductive health care had recurrent chlamydial
infection following treatment; most were reinfected within 9 months of treatment.
Orr et al17 reported that 17% to 26% of women
were reinfected with chlamydia 6 months after treatment. More recently, Burstein
and coworkers18 demonstrated a high prevalence
of chlamydia infections among inner-city adolescent women, with a median time
to subsequent infection of 6.3 months.
Studies examining subsequent infection with more than the original species
are limited. Oh and colleagues19 followed up
a group of adolescent women for 24 months with periodic examinations for chlamydia
and gonorrhea (culture) and trichomoniasis (wet mount). Forty-seven percent
of the women were infected with one of the organisms at enrollment (N gonorrhoeae, 11.6%; C trachomatis,
23.2%; and T vaginalis, 23.4%). Nearly 21% of the
women had chlamydial and 17% had gonococcal cervicitis during the follow-up.
Burstein et al12 investigated subsequent infections
with chlamydia and gonorrhea among adolescents in urban school-based clinics.
The median times to subsequent infection with N gonorrhoeae and C trachomatis were 2.6 and 4.8 months,
respectively, among the adolescent women.
More recently, Fortenberry et al7 described
subsequent infections among adolescent women treated for C trachomatis, N gonorrhoeae, or T vaginalis. More than 40% of the women were subsequently infected
with one of these organisms within 12 months following treatment; reinfection
with the same species and different species organisms was common.
Among adult men treated in STD clinics, recurrent infection with gonorrhea
is common.4, 5 "Repeaters" are
more likely to be younger, poor, to report "casual" sexual contacts, fail
to use condoms, and be African American. Little information is available about
the risk for subsequent STI among adolescent men. Cohen and coworkers20 reported declining prevalence rates of chlamydia
among adolescent boys screened and treated in public school health settings,
suggesting that screening and treatment may be effective in reducing incident
disease; the prevalence of gonorrhea did not change over the several years
of study. Recurrence rates were not available. In a multicenter STD prevention
study, Kamb et al21 reported that 12.8% of
adolescent men developed an incident STD within 12 months. These limited data
suggest that subsequent STI is probably common among high-risk adolescent
men and that incident STI is unlikely to be limited to the original infecting
species.
Investigators have been unable to identify consistent predictors of
initial or subsequent infection among adolescents when multivariate analytic
techniques are used.6, 7, 12, 18, 19, 22
In our study, being female, being infected at enrollment, and reporting an
unprotected coital event were associated with a shorter time to subsequent
STI. However, multivariate analysis that included sexual behaviors that took
place before each visit demonstrated that only being female and having any
new interval sexual partner predicted diagnosis of an STI at that visit. The
confidence intervals were large for several of the risk variables, and interactions
could not be tested because of the sample size. Age was not a predictor of
subsequent STI in our study.
The inability to identify clinically important predictors of subsequent
infection has led several investigators to recommend screening sexually active
adolescents for STI on a more frequent basis vs annually. Expanding screening
for subsequent infections beyond the original species would also be important,
because subsequent infections are not limited to the original species and
are not predicted by characteristics available at the time of treatment.7, 19 Asymptomatic infection is common,
and the presence of one STI may increase the risk for another.23, 24, 25, 26
Recurrent infection with chlamydia increases the risk for hospitalization
for pelvic inflammatory disease and ectopic pregnancy.27
Considerable research indicates that chlamydia screening and control
programs decrease the prevalence of chlamydia in these populations and would
be cost-effective for sexually active women, primarily by decreasing complications
of short- and long-term sequelae.28, 29
One report,30 completed before the availability
of nucleic acid amplification tests, suggests that screening adolescent men
would also be cost-effective. We could find no information about the effectiveness
of screening adolescents for other STIs, nor do there appear to be consistent
useful predictors of reinfection.
There are limitations to our study. The diagnostic tests used at follow-up
visits were more sensitive than those used at enrollment, resulting in the
potential for misclassification bias at enrollment and an inflated rate of
incident infection at the 1-month visit. We would expect this error to be
demonstrated by observing an increased rate of incident infections at 1 month
among subjects who were not treated at enrollment for a specific organism,
because the less sensitive test did not identify an infection when truly present
(false-negative test results). This would inflate the rates of incident infection
at 1 month, because the more sensitive tests were used at all visits subsequent
to enrollment. To identify any misclassification bias, we reexamined the data,
looking for differential rates of incident STI at 1 month among subjects who
were classified as free of infection at enrollment. For example, subjects
who did not have evidence of chlamydia at enrollment or who were not contacts
to chlamydia or gonorrhea (and therefore did not receive azithromycin) were
no more likely to have chlamydia at 1 month than were those who were treated
with azithromycin at enrollment. The results were the same for N gonorrhoeae and T vaginalis, suggesting
that the use of more sensitive tests was not a serious problem.
We studied a population of adolescents and young adults at high risk
for STI because of personal sexual behaviors and residence in neighborhoods
with high STD prevalence. Although we enrolled subjects from 2 types of clinics,
there were no differences in the median time to subsequent infection based
on the type of clinic from which adolescents and young adults were enrolled
(data not shown). Although 80% of the subjects returned for at least one subsequent
visit, men, those not attending school, adolescents and young adults reporting
fewer sexual partners in the 2 months before enrollment, and uninfected contacts
were more likely to be unavailable for follow-up. The 2 groups did not differ
at enrollment in behaviors that have been associated with STI. The effects
of attrition on our findings remain unknown.
We believe that the increasing body of evidence supports more frequent
STI screening for high-risk, asymptomatic, sexually active adolescents and
young adults. Newer nucleic acid amplification tests using urine or self-obtained
vaginal swabs are more acceptable to this population than are those tests
that require urethral or endocervical samples.31, 32, 33
A single sample may be used to detect chlamydia and gonorrhea; nucleic acid
amplification tests for trichomonas are available for research purposes and
could be made available for public use. The number of men in our study is
small, limiting the power to detect statistical differences in the time to
second infections. However, the findings are similar to those observed among
women, suggesting that the failure to detect differences is related to inadequate
statistical power. We believe our data are consistent with and expand on those
of Burstein12, 18 and Fortenberry7 and their colleagues. Adolescents and young adults
are at substantial risk for subsequent STI if they present with a documented
infection or are a contact of an STI.
Several unanswered questions remain that will require additional prospective
research. What is the optimal frequency of testing? It appears that every
6 months would be sufficient, based on median times to reinfection of about
6 months in several studies. However, this would leave a substantial proportion
of infected individuals at risk for transmitting infection for several months.
How would testing best be accomplished? Given the availability of urine-based
and vaginal swab–based tests, it would be possible to screen adolescents
in nontraditional settings12 and independent
of contact with physicians.12, 33, 34, 35, 36, 37
Home-based testing has been demonstrated to be feasible and acceptable in
several smaller European studies.32, 38, 39
Although this is attractive in that it might overcome the stigma associated
with delay in seeking STI-related care,40 one
loses the opportunity for education if there is no contact with a health provider.
It is unclear how one would enlist the adolescent or young adult as an ally
in programs for more frequent screening, particularly if divorced from an
office or clinic visit.
Which organisms should screening detect? Given our and others' experience,
we believe that gonorrhea, chlamydia, and trichomonas are obvious candidates
based on prevalence, sequelae, and the availability of curative antibiotic
therapy. Who should be screened? Our and other investigators' research has
focused on adolescents and young adults at high risk for STI. Little is known
about other populations of sexually active youth. Limited national data suggest
that about 6% of older adolescent and young adult men have asymptomatic infection
with C trachomatis.41
Research using computer models suggests that it should be cost-effective to
screen at this level of prevalent infection. How will such screening be financed,
especially if one is to maintain confidentiality in these populations? Cooperation
of adolescents, parents, payers, and private and public providers of health
care will be required.42
Last, what is the desired outcome of more frequent screening? One hopes
to reduce transmission and complications (secondary prevention). When applied
to large populations, would this reduce complications, as demonstrated with
chlamydia? Would it decrease the incidence of other STIs, including human
immunodeficiency virus?43 Additional research
is required in each of these areas if we are to move forward in reducing STIs
among adolescents and young adults.
AUTHOR INFORMATION
What This Study Adds
Sexually active adolescents are at high risk for STIs. Current recommendations
include annual STI screening in this population. Previous research has largely
focused on organism-specific screening following an incident infection, ignoring
the common mode of acquisition of an STI.
This study demonstrates that incident STIs are common among high-risk
adolescents, independent of original organism and infection status. We believe
that our data support a recommendation to screen high-risk youth every 6 months
for C trachomatis, N gonorrhoeae, and T vaginalis.
Accepted for publication April 10, 2001.
This work was supported in part by grants U19AI31494 and U19AI43924
from the National Institute of Allergy and Infectious Diseases, Bethesda,
Md.
Presented in part at the biannual meeting of the International Society
for Sexually Transmitted Disease Research, Denver, Colo, July 13, 1999.
We thank Cathy Roberts, MA, and Patricia Brooks for their invaluable
assistance in collecting the data for this study.
From the Section of Adolescent Medicine, Department of Pediatrics (Drs
Orr, Johnston, and Fortenberry), and Division of Biostatistics, Department
of Medicine (Mr Brizendine and Dr Katz), Indiana University School of Medicine,
Indianapolis. Dr Johnston is now affiliated with Kalamazoo Center for Medical
Studies, Michigan State University, Kalamazoo.
Corresponding author and reprints: Donald P. Orr, MD, Section of
Adolescent Medicine, Department of Pediatrics, Indiana University School of
Medicine, Riley Outpatient Garage, Room 070, 575 N West Dr, Indianapolis,
IN 46202 (e-mail: dporr{at}iupui.edu).
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