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Associations Between Sexually Transmitted Disease Diagnosis and Subsequent Sexual Risk and Sexually Transmitted Disease Incidence Among Adolescents

Crosby, Richard A. PhD*†; DiClemente, Ralph J. PhD*†‡§; Wingood, Gina M. ScD, MPH*†; Salazar, Laura F. PhD*†; Rose, Eve MPH*; Levine, David MD, FAAP∥; Brown, Larry MD¶; Lescano, Celia PhD¶; Pugatch, David MD**; Flanigan, Timothy MD††; Fernandez, Isa PhD‡‡; Schlenger, William PhD§§; Silver, Barabra J. PhD∥∥

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*Department of Behavioral Sciences and Health Education, Rollins School of Public Health, Atlanta, Georgia; Emory Center for AIDS Research, Atlanta, Georgia; the Departments of Pediatrics and §Medicine, Emory University School of Medicine, Atlanta, Georgia; the Department of Pediatrics, Morehouse School of Medicine, Atlanta, Georgia; the Departments of Psychiatry, **Pediatrics, and ††Medicine, Brown University School of Medicine, Providence, Rhode Island; the ‡‡Department of Epidemiology and Public Health, University of Miami, Miami, Florida; §§Research Triangle Institute, Research Triangle Park, North Carolina; and the ∥∥Center for Mental Health Services, SAMHSA, Rockville, Maryland

This study was supported by a grant from the Center for Mental Health Services, Substance Abuse and Mental Health Services Administration, Department of Health and Human Services.

Correspondence: Richard A. Crosby, PhD, Rollins School of Public Health, 1518 Clifton Road, NE, Room 542, Atlanta, GA 30322. E-mail: rcrosby@sph.emory.edu

Received for publication September 16, 2003,

revised November 4, 2003, and accepted November 5, 2003.

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Abstract

Background: Empiric evidence is lacking in regard to the subsequent sexually transmitted disease (STD)-associated risk behaviors of adolescents diagnosed and treated for an STD.

Goal: The goal of this study was to prospectively identify associations between STD diagnosis and subsequent sexual risk and STD incidence among a sample of U.S. adolescents.

Study Design: A cohort of 455 adolescents (age 15–21 years) was followed for 3 months. Adolescents were recruited from primary care clinics and through outreach activities.

Results: A total of 10.8% were initially diagnosed with at least one STD. After adjusting for observed covariates, these adolescents (compared with those testing negative) were 2.8 times (P = 0.0001) more likely to be abstinent from sex and 2.2 times more likely to report always using condoms (P = 0.04). However, during the ensuing 3 months, they were approximately 2.4 times more likely to report having sex with multiple partners (P = 0.01), 8.9 times more likely to test positive for trichomonas (P = 0.009), and 3.0 times more likely to test positive for chlamydia (P = 0.04).

Conclusions: Compared with those testing negative, adolescents diagnosed with an STD may subsequently adopt safer sex behaviors, including abstinence. However, perhaps in part as a result of having sex with multiple partners, they might fail to practice safer sex behaviors stringently enough to avoid subsequent STD acquisition.

IN THE UNITED STATES, sexually transmitted diseases (STDs) disproportionately affect adolescents, and prevalence rates among some subgroups have reached epidemic proportions. 1 Although the literature addressing factors that predispose adolescents to STD acquisition is well-developed and embodies a wide scope, 1–6 the body of evidence pertaining to responses after infection is quite limited. However, this limited evidence is important because it provides a starting point for further investigation. For example, in a study of 14 to 21 year olds, approximately one fifth of those diagnosed with an STD practiced abstinence during the ensuing 3 months. Increased condom use was reported among those who remained sexually active. 7 Another study compared adolescents with and without a history of STD infection, and observed that rates of current sexual risk behaviors and subsequent STD acquisition were significantly greater among those reporting a history of STDs. 8 Similar findings, about greater rates of sexual risk behaviors, have been reported among adolescents diagnosed with HIV. 9

Given that STD reinfection (or the acquisition of an STD diagnosed after previously being treated for a different STD) is common among U.S. adolescents, 10–12 observational studies that assess adolescents’ sexual risk and protective behaviors after their receipt of their results from STD testing are warranted. Accordingly, the purpose of this study was to prospectively identify associations between STD diagnosis and subsequent sexual risk and STD incidence among a sample of U.S. adolescents.

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Methods

Study Sample and Design

Study participants were adolescents enrolled in a multisite, randomized trial of a brief HIV prevention program. A waitlist control group was used. The study recruited adolescents (15–21 years of age) from primary care clinics and through outreach activities (eg, street outreach, posters, flyers, referral from friends) in 3 U.S. cities: Atlanta, Georgia, Providence, Rhode Island, and Miami, Florida. Inclusion criterion was sexual activity (vaginal or anal intercourse) within the past 90 days. Adolescents who were currently pregnant, attempting to become pregnant, or who had delivered a baby within the past 90 days were excluded. Adolescents with known HIV-positive serostatus were also excluded.

Eligible adolescents (n = 1867) were invited to participate in the study. Adolescents listened to a standardized brief overview of the study, including requirements of participation and amount of compensation provided. Informed consent was obtained from adolescents 18 years of age or older. Assent and parental consent were obtained for adolescents 15 to 17 years of age. The University Institutional Review Board, at the respective institutions, approved all study protocols. A total of 1412 adolescents enrolled in the study and completed baseline assessments, yielding a participation rate of 76%.

A prospective cohort design, with a 3-month observation period, was used. The predictor variable was STD diagnosis at baseline, and the outcomes measures were assessed at follow up. To ensure that effects of the behavioral intervention would not confound the current observational study, adolescents assigned to the intervention group were not included in the analyses. Thus, only data collected from adolescents randomized (by computer-generated concealment of allocation procedures) to the waitlist control group were used for these analyses. These adolescents completed an assessment at baseline and 3 months but did not receive any form of behavioral intervention beyond the standard-of-care clinical counseling provided if they were diagnosed (and therefore treated) with a nonviral STD. Furthermore, because the outcomes of interest were sexual risk behaviors and STD incidence, adolescents reporting they did not have sex during the observation period were excluded from the analysis (one important exception was the inclusion of adolescents to determine associations between abstinence and STD diagnosis at baseline). Of 706 adolescents completing baseline assessments, 602 (85%) returned for the planned 3-month follow-up assessment. Of these 602 adolescents, 88 did not complete the follow-up assessment and 59 indicated they did not have sex between the baseline and follow-up periods. Thus, the analytic sample was comprised of 455 adolescents who completed baseline and follow-up assessments (including urines) and indicated sexual activity during the observation period.

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Data Collection

Adolescents completed a 30-minute questionnaire using audio computer-assisted self-interviewing (A-CASI) technology. Many of the questions pertained to adolescents’ sexual risk behavior, and these items were used in the current analysis. Evidence suggests that A-CASI technology could facilitate adolescents’ disclosure of personal information such as their sexual risk behaviors. 14,15 Questions asked adolescents about their sexual risk behaviors during the past 90 days. The inherent nature of such questions created a need for the use of multiple skip patterns. Fortunately, the use of A-CASI technology obviates problems following these patterns because the computer program automatically “skips” adolescents to the appropriate sections. To facilitate recall, adolescents were given a 90-day calendar; a standardized script was used to help adolescents document memorable events during the recall period. Subsequently, adolescents were trained to use the laptop computers, eg, they were shown how to enter responses using the number and letter keys, function keys were defined, and 3 questions were used for practice. Research staff remained in the testing room to answer any questions and assist with operation of the computers. Adolescents were compensated $50 for their participation.

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Measures
Predictor Variable.

Participants were instructed to collect the first part of the stream of urine. Collection tubes were immediately refrigerated and shipped to Indiana University for assay within 96 hours of collection. The Abbott LCx Probe System (Abbot Park, IL) was used to test for Chlamydia trachomatis and Neisseria gonorrhoeae DNA. 13,14 Urine was also tested for trichomonas by polymerase chain reaction (PCR) using a primer set previously described. 15 This assay method for trichomonas has been evaluated (against wet mount and another PCR assay) and demonstrated high levels of sensitivity and specificity. 16,17 Adolescents testing positive for an STD were provided with single oral-dose therapy (400 mg Suprax (Lederle Pharmaceutical) for gonorrhea, 1 g Zithromax (Pfizer Pharmaceutical) for chlamydia, or 2 g Flagyl (Pharmacia Corp.) for trichomonas).

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Outcome Measures.

Throughout the questionnaire, sex was defined as including both penile–vaginal sex (defined to adolescents as “when a man inserts his penis into a woman’s vagina”) and anal sex (defined to adolescents as “when a man puts his penis into a man’s or woman’s anus or butt”). Assessed outcomes used a 90-day recall period. Two measures of condom use were assessed: 1) whether adolescents always used condoms (ie, 100% use) and 2) frequency of condom use (assessed on a 5-point scale ranging from never to always). Number of sex partners, frequency of sex (reported by adolescents) for an average week, and whether adolescents had sex with someone they would consider a “casual” partner were also assessed. The number of unprotected sexual episodes reported by adolescents was also assessed. Finally, urine specimens were collected and all laboratory tests were repeated at the follow-up assessment.

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Data Analysis

First, continuous-level measures were evaluated for normality by determining if skewness or kurtosis ratios exceeded an absolute value of 2.0. Because these measures were not normally distributed, they were dichotomized by performing a median split. The use of a median split was deemed preferable to a log transformation because log-transformed outcomes are not readily amenable to practical interpretation of the study findings.

Significance of bivariate associations between STD diagnosis (baseline) and the assessed outcome measures was determined by chi-squared tests. Outcomes achieving a screening level of significance (P <0.15) were subsequently tested in a series of logistic regression models (one model for each outcome) that included adolescents’ gender and race (minority vs. white) as covariates. In addition, a series of bivariate tests were conducted to determine whether site differences might confound the analyses. Site differences were observed for 2 outcome measures (not having sex and frequency of unprotected sex). Thus, site was entered as a covariate in the models predicting these 2 outcomes. Finally, models of sexual risk behavior outcomes also included adolescents’ baseline report of the behavior being predicted. Forward stepwise entry was used in each model. Adjusted odds ratios (AORs), their 95% confidence intervals, and respective P values were calculated for outcomes achieving significance defined by an alpha of 0.05.

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Results

Characteristics of the Sample

Average age of the adolescents was 18.3 years (standard deviation, 1.8). Females comprised 59.6% of the sample. Nearly one half (48.5%) self-identified as black, 23.6% identified as Hispanic, 22.7% identified as white, and 5.2% identified as a member of an “other” race. Approximately one sixth (15.6%) reported being diagnosed with an STD before enrolling in the study. At baseline, chlamydia was diagnosed for 7.5% of the adolescents, gonorrhea for 1.3%, and trichomoniasis for 4.0%. Approximately one tenth of the adolescents (10.8%) were diagnosed with at least one STD.

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Bivariate Associations

Table 1 displays bivariate associations between STD diagnosis (baseline) and selected outcomes assessed 3 months later. Table 1 also provides descriptive information relative to the assessed outcomes. For example, approximately 43% of those diagnosed with an STD reported engaging in sex with multiple partners in the next 90 days compared with approximately 32% among those testing negative (note, this difference achieved only a screening level of significance). Only 3 outcomes failed to achieve a screening level of significance (ie, P <0.15). Adolescents did not differ about engaging in sex more than once a week. Approximately 30% of the adolescents subsequently engaged in sex with a casual partner, regardless of whether they were diagnosed with an STD. Finally, the incidence of gonorrhea was quite low and this outcome did not achieve significance.

Table 1
Table 1
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Adjusted Analyses

Table 2 displays odds ratios adjusted for the influence of the observed covariates. Because a forward stepwise entry procedure was used, only significant AORs were calculated. For clarity, significant AORs for gender or race are also displayed in Table 2.

Table 2
Table 2
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As shown, 5 of the outcome measures retained a significant association with STD diagnosis at baseline. Adolescents diagnosed with an STD at baseline were nearly 3 times more likely than their counterparts who tested negative to report (at the subsequent 3-month follow-up assessment) that they had not had sex in the past 3 months. Similarly, those diagnosed with an STD were more than twice as likely to report using condoms all of the time during the subsequent 3 months. Conversely, those diagnosed with an STD were more than twice as likely to report having multiple partners in the subsequent 3 months.

Being diagnosed with an STD at baseline predicted subsequent infection with both trichomonas and chlamydia. Adolescents diagnosed with an STD at baseline were approximately 9 times and 3 times more likely to test positive for trichomonas and chlamydia, respectively.

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Discussion

The findings support and extend previous findings reported by Fortenberry and colleagues. 7 Our findings support their work (a within-subject analysis) by indicating that adolescents diagnosed with STDs are more likely (as a group) to subsequently practice safer sex (or abstinence) than those not diagnosed with an STD. Also, our findings extend their work by suggesting that the protective behaviors of those diagnosed with an STD are inadequate to lower subsequent STD incidence to a follow-up level observed for adolescents who were not initially diagnosed with an STD.

Specifically, prospective findings from controlled analyses suggest that adolescents diagnosed with an STD could be more likely to subsequently abstain from sex or use condoms than their counterparts who tested negative for STDs. These findings support the notion that testing and the process of diagnosis and treatment could confer a protective effect against subsequent STD-associated risk behaviors among adolescents. However, the findings also suggest that (among those not adopting abstinence) adolescents testing positive could be more likely to have sex with multiple partners and could be more likely to subsequently acquire an STD. These latter 2 findings are clearly related in that risk of STD acquisition increases with each additional partner (given that condoms are not used correctly and consistently). Although approximately 37% of those diagnosed with an STD at baseline reported using condoms consistently over the 3-month period of observation, evidence from other studies strongly suggests that condoms might not have been used correctly. 18–21

Despite what appears to be relatively safer sexual practices among adolescents initially diagnosed with an STD, finding that these adolescents were more likely to subsequently acquire an STD is critically important. Although a greater tendency toward having sex with multiple partners could explain this discrepancy, several alternative explanations are also warranted. For example, the association could also be attributable to sexual network factors, ie, seroprevalence of STDs within adolescents’ sexual networks could be the underlying cause of the observed association. 22 Previous research also suggests that adolescents reporting they engage in risky behaviors (of any kind) tend to affiliate with others who also engage in these risky behaviors. 23–25 The observed association could also be attributable to having sex with untreated partners after adolescents received their initial diagnosis and treatment. 7

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Limitations

Despite the use of A-CASI technology, the findings are limited by the use of self-reported measures. In addition, our use of a nonprobability sample precludes generalization. Furthermore, the participation rate of 76% could indicate a sampling bias, thus further limiting the generalizability of the findings. Conceivably, higher-risk adolescents could have been less likely to participate in the study, although this rate is within the range of similar studies. Finally, it should be noted that adolescents testing positive were treated, for free, with single oral-dose therapy. Unlike care provided outside the context of a study, treatment did not involve appointment-making, waiting in crowded clinics, or adherence to medication. To the extent that these clinical experiences could contribute to the adoption of safer sex practices, the effects observed could underestimate effects that would occur in the context of routine care.

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Conclusion

Controlled findings suggest that adolescents diagnosed with an STD (compared with those being tested and learning they did not have an STD) may subsequently adopt safer sex behaviors, including abstinence. Thus, the findings suggest that diagnosis of STDs in asymptomatic adolescents could be an effective trigger to behavior change. However, perhaps in part as a result of having sex with multiple partners, adolescents diagnosed with an STD may fail to practice safer sex behaviors stringently enough to avoid subsequent STD acquisition.

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References

1. Eng TR, Butler WT, eds. The Hidden Epidemic: Confronting Sexually Transmitted Diseases. Washington, DC: National Academy Press, 1997.

2. Crosby RA, Miller KS. The pivotal role of the family on adolescent females’ sexual health. In: Wingood GM, DiClemente RJ, eds. Handbook of Women’s Sexual and Reproductive Health. New York: Kluwer Academic/Plenum Publishers, 2002: 113–128.

3. DiClemente RJ, Crosby RA. Sexually transmitted diseases among adolescents: Risk factors, antecedents, and prevention strategies. In: Adams GR, Berzonsky M, eds. Blackwell Handbook of Adolescence. Oxford, UK: Blackwell Publishers Ltd, 2003: 573–605.

4. Santelli JS, DiClemente RJ, Miller KS, Kirby D. Sexually transmitted diseases, unintended pregnancy, and adolescent health promotion. Adolesc Med 1999; 10: 87–108.

5. Crosby RA, DiClemente RJ, Wingood GM, et al. Correlates of unprotected vaginal sex among African American female teens: The importance of relationship dynamics. Arch Pediatr Adolesc Med 2002; 154: 893–899.

6. Berman SM, Hein K. Adolescents and STDs. In: Holmes KK, Sparling PF, Mardh P, et al., eds. Sexually Transmitted Diseases. New York: McGraw-Hill, 1999: 129–142.

7. Fortenberry JD, Brizendine EJ, Katz BP, Orr DP. Post-treatment sexual and prevention behaviours of adolescents with sexually transmitted infections. Sex Transm Infect 2002; 78: 365–368.

8. DiClemente RJ, Wingood GM, Sionean C, et al. Association of adolescents’ STD history and their current high-risk behavior and STD status: A case for intensifying clinic-based prevention efforts. Sex Transm Dis 2002; 29: 503–509.

9. Diamond C, Buskin S. Continued risky behavior in HIV-infected youth. Am J Public Health 2000; 90: 115–118.

10. Orr DP, Johnston K, Brizendine EJ, et al. Subsequent sexually transmitted infection in urban adolescents and young adults. Arch Pediatr Adolesc Med 2001; 155: 947–953.

11. Fortenberry JD, Brizendine EJ, Katz BP, et al. Subsequent sexually transmitted infections among adolescent women with genital infection due to Chlamydia trachomatis, Neisseria gonorrhoeae, or Trichomonas vaginalis. Sex Transm Dis 1999; 26: 26–32.

12. Kamb ML, Fishbein M, Douglas JM, et al. Efficacy of risk-reduction counseling to prevent human immunodeficiency virus and sexually transmitted diseases: A randomized controlled trial. JAMA 1998; 280: 1161–1167.

13. Hook EW III, Ching SF, Stephens J, et al. Diagnosis of Neisseria gonorrhoeae infection in women by using ligase chain reaction on patient-obtained vaginal swabs. J Clin Microbiol 1997; 35: 2129–2132.

14. Hook EW III, Smith K, Mullen C, Stephens J, et al. Diagnosis of genitourinary Chlamydia trachomatis infections in women by using ligase chain reaction on patient-obtained vaginal swabs. J Clin Microbiol 1997; 35: 2133–2135.

15. Kengne P, Veas F, Vidal N, Rey JL, Cuny G. Trichomonas vaginalis: Repeated DNA target for highly sensitive and specific polymerase chain reaction diagnosis. Cell Mol Biol Lett 1994; 40: 819–831.

16. Kendrick CS, Williams JA, Van Der Pol B. Evaluation of a modified Amplicor PCR assay for the detection of Trichomonas vaginalis DNA using female endocervical and urine specimens. 14th meeting of the International Society for Sexually Transmitted Disease Research, Berlin, Germany, June 2001.

17. Madico G, Quinn TC, Rompalo A, McKee KT Jr, Gaydos CA. Diagnosis of Trichomonas vaginalis infection by PCR using vaginal swab samples. J Clin Microbiol 1998; 36: 3205–3210.

18. Crosby RA, DiClemente RJ, Wingood GM, et al. Correct condom application among African American adolescent females: The relationship to perceived self-efficacy and the association with confirmed STDs. J Adolesc Health 2001; 29: 194–199.

19. Crosby RA, Yarber WL. Perceived versus actual knowledge about correct condom use among US adolescents: Results from a national study. J Adolesc Health 2001; 28: 415–420.

20. Crosby RA, Sanders S, Yarber WL, et al. Condom use errors and problems among college men. Sex Transm Dis 2002; 29: 552–557.

21. Sanders SA, Graham CA, Yarber WL, Crosby RA. Condom use errors and problems among young women who apply put condoms on their male partners. J Am Women Med Assoc 2003; 58: 95–98.

22. Laumann EO, Youm Y. Racial/ethnic group differences in the prevalence of sexually transmitted diseases in the United States: A network explanation. Sex Transm Dis 1999; 26: 250–261.

23. Wingood GM, DiClemente RJ, Crosby RA, et al. Gang involvement and the health of African-American female adolescents. Pediatrics 2002; 110: e57.

24. Prinstein MJ, Boergers J, Spirito A. Adolescents’ and their friends health-risk behavior: Factors that alter or add to peer influence. J Pediatr Psychol 2001; 26: 287–298.

25. La Greca AM, Prinstein MJ, Fetter MD. Adolescent peer crowd affiliation: Linkages with health-risk behaviors and close friendships. J Pediatr Psychol 2001; 26: 131–143.

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