ORIGINAL STUDY
Associations Between Psychosocial Factors and Incidence of Sexually Transmitted Disease Among South African Adolescents Ann O'Leary, PhD,* John B. Jemmott III, PhD,† Loretta S. Jemmott, PhD,† Anne Teitelman, PhD,† G. Anita Heeren, MD,† Zolani Ngwane, PhD,‡ Larry D. Icard, PhD,§ and David A. Lewis, PhD¶║
Background: Adolescents living in South Africa are at high risk for HIV and other sexually transmitted diseases (STDs). The present study sought to identify correlates of curable STD incidence among a cohort of adolescents in Eastern Cape Province, South Africa. Methods: Data were collected in conjunction with an HIV/STD prevention intervention randomized controlled trial.1 At 54 months postintervention, curable STD incidence (gonorrhea, chlamydial infection, and trichomoniasis) was assayed and self-report measures of potential correlates of STD incidence were collected. Results: Participants were adolescents reporting at least 1 sexual partner in the past 3 months (n = 659). As expected, univariate analyses revealed that girls were more likely than boys to have an STD. In addition, intimate partner violence, unprotected sex, and having older partners were associated with incident STD. In Poisson multiple regression analyses, sex (risk ratio [RR], 4.00; 95% confidence interval [CI], 2.51–6.39), intimate partner violence (RR, 1.23; 95% CI, 1.12–1.35), unprotected sex (RR, 1.42; 95% CI, 1.09–2.01), and multiple partners (RR, 1.70; 95% CI, 1.11–2.61), but not partner's age (RR, 1.00; 95% CI, 0.94–1.07) were associated with incident STD, adjusting for 42-month STD prevalence. Binge drinking, forced sex, and age were unrelated to STD incidence in both analyses. Interactions between sex and the hypothesized correlates were nonsignificant, suggesting that sex did not modify these relationships. Conclusions: Interventions to reduce HIV/STD incidence among adolescents in South Africa should address the risk associated with sex, unprotected sex, intimate partner violence, and multiple partnerships.
From the *Centers for Disease Control and Prevention, Atlanta GA; †University of Pennsylvania, Philadelphia, PA; ‡Haverford College, Haverford, PA; Temple University, Philadelphia, PA; and ¶Centre for HIV and Sexually Transmitted Infections, National Institute for Communicable Diseases, Johannesburg, South Africa; and ║Centre for Infectious Diseases and Microbiology & Marie Bashir Institute for Infectious Diseases and Biosecurity, Westmead Clinical School, University of Sydney, Sydney, Australia Conflicts of interest and funding: No authors declare any conflicts of interest. Correspondence: Ann O'Leary, PhD, Division of HIV/AIDS, Centers for Disease Control and Prevention, 1600 Clifton Rd, MS E-37, Atlanta GA 30329. E-mail: [email protected]. Received for publication August 26, 2014, and accepted December 26, 2014. Author notes: This study was funded by Research Grant R01 MH065867 from the National Institute of Mental Health. The National Institute of Mental Health had no role in the design and conduct of the study, preparation, review, or approval of the manuscript. The findings and conclusions are those of the authors and do not represent the views of the Centers for Disease Control and Prevention. DOI: 10.1097/OLQ.0000000000000247 Copyright © 2015 American Sexually Transmitted Diseases Association All rights reserved.
Sexually Transmitted Diseases
•
S
exually transmitted disease (STD) represents a significant health problem for South African adolescents. The World Health Organization has estimated that of a population of 384.4 million, 92.6 million curable STIs occurred in the African Region in 2008.2 Although correlates of STD have been identified for a variety of populations, few such studies have been conducted among adolescents in Sub-Saharan Africa.3–5 In one study,4 a sexual risk reduction intervention produced a significant reduction in incidence of herpes simplex virus-2. Studies on other populations, however, have revealed some general correlates. One of these is sex, with females more susceptible to STD due to biological, economic, and social factors.6 Another is having a much older sexual partner, which is common among women in Sub-Saharan Africa7 and puts women, especially, at risk for STD,8–10 including HIV. It should be noted, however, that although very few studies have examined effects of age disparity on boys' STD risk, there is some evidence suggesting that boys are more likely to be infected with HIV when their most recent female partner was older.11 Binge drinking has also been shown to be predictive of STD incidence.12,13 A study by Boden and colleagues,12 which was conducted among men and women aged 15 to 30 years in New Zealand, showed an alcohol dose effect with higher levels of alcohol consumption and more symptoms of dependence, related to more STD. In South Africa, shabeens—casual houses where beer is sold and consumed—are ubiquitous. It is understood that if a man buys a girl a beer, she is expected to have sex with him. Intimate partner violence has been found to be correlated with STD among US women and male perpetrators of violence14,15 and with HIV infection in South Africa.16 South Africa has high rates of rape,17 and forced sex has been shown to be associated with STD both in the United States18,19 and in South Africa.20 Self-reported sexual behavior has been an inconsistent correlate of STD. Having multiple sex partners has been shown to predict STD21 and HIV22 in some studies, but not others.23 Condom use has also been examined as an STD predictor. In an early study,24 condom use was found to be unrelated to STD incidence, probably because contracting a STD requires that the person be exposed to an infected partner. Thus, people who have unprotected sex with partners who do not have an STD will not contract an STD, diminishing the relation between self-reported behavior and STD.25 The present study was designed to identify correlates of curable STD at 54 months postintervention in the “Let Us Protect Our Future” trial.1,26 No STD assessment was done at baseline, but as only 3% of participants were sexually active at that time, it can be assumed that the overwhelming preponderance of infections happened after the 8-day intervention. At 42 months, all identified STD was treated, so that curable STD at 54 months can be taken as an incidence measure. We hypothesized that curable STD incidence would be predicted by older age, female sex, risk reduction intervention arm,
Volume 42, Number 3, March 2015
135
Copyright © 2015 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
O'Leary et al.
binge drinking, having experienced intimate partner violence, having been raped, having had condom-unprotected sex, multiple partners, and having older partners. We examined these relationships in bivariate analyses as well as in Poisson multiple regression.
METHODS The institutional review board (IRB) no. 8 at the University of Pennsylvania, which was the designated institutional review board under the federal-wide assurances of the University of Pennsylvania and the University of Fort Hare, approved the study. The laboratory testing was additionally approved by the Human Research Ethics Committee (Medical) of the University of the Witwatersrand, South Africa. We conducted the study in Mdantsane, an urban township, and Berlin, a neighboring rural settlement, in Eastern Cape Province, South Africa, where isiXhosa is the first language of 95.1% of the population. The participants were adolescents who enrolled in a schoolbased cluster-randomized controlled trial of an HIV/STD riskreduction intervention. Schools that taught sixth-grade learners and served the general population were eligible. All 35 eligible schools (26 in Mdantsane, 9 in Berlin) agreed to participate. From 17 matched pairs of schools similar in numbers of sixth-grade learners, numbers of classrooms, and whose classrooms had electricity, we randomly selected 9 and randomized within pairs 1 school to the HIV/STD risk-reduction intervention and one to the health-promotion-control intervention. Methods for the intervention study are described in detail elsewhere.26 We enrolled 18 schools for 13 months beginning in October 2004. The initial informed-consent process covered activities through the 12month follow-up. Accordingly, we located the original participants who were now dispersed to more than 100 secondary schools and gave them parent/guardian consent forms and cover letters explaining the continuation of the trial and inviting their parents or guardians to a meeting where they could receive additional information and ask questions about the follow-up study. This article is based on the 54-month follow-up data. The 42-month follow-up data were collected beginning in April 2008, and the 54-month data collection was completed by June 2010.
Measures Incident STD. At the 42- and 54-month follow-up assessments, participants provided a urine specimen after completing
the self-report questionnaire. First-pass urine specimens were delivered to the Centre for HIV and STIs at the National Institute for Communicable Diseases, Johannesburg, South Africa, and assayed for Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (NG) using the Gen-Probe APTIMA Combo 2 Assay (Gen-Probe, Inc, San Diego, CA) and for Trichomonas vaginalis (TV) using the APTIMA TV assay (Gen-Probe, Inc). All participants with a positive curable STD (CT, NG, or TV) test received directly observable single-dose antimicrobial treatment and risk-reduction counseling per Centers for Disease Control and Prevention recommendations. The outcome variable in the present analysis is the incidence of any of these STDs at 54 months. Participants received a binary code based on whether they had any STD or not. The predictor variables included age, sex, study arm, binge drinking, intimate partner violence, history of forced sex, any unprotected sex, multiple partners, and participants' report of age of sexual partner assessed at 54-month follow-up. Unprotected Vaginal Intercourse. Participants were coded as having unprotected vaginal intercourse if they reported having vaginal intercourse without using a condom in the previous 3 months. Multiple Partners. Participants reporting 2 or more sexual partners in the previous three months were coded as having multiple partners. Forced Sex. History of forced sex was assessed with a single item: “Have you ever been forced to have vaginal intercourse against your will?” Intervention Condition. Intervention condition was a dichotomous variable indicating whether the participant had been in the sexual risk reduction intervention or the health promotion control intervention. Binge Drinking. Respondents were asked how many times in the past month they had had 5 or more drinks of alcohol. Participants were coded as having had a binge drinking episode if they reported having 5 or more drinks of alcohol on a single occasion in the past month. Intimate Partner Violence. This was assessed with the physical abuse subscale of the Conflict in Adolescent Dating Relationships Inventory.27 We averaged 4 items to create a scale. The items assessed estimates of the number of times each event had occurred during the preceding year, with responses ranging from “0” to “6 or more.” The item stem was “In the last year,
TABLE 1. Characteristics of Learners Reporting at Least 1 Sexual Partner in the Past 3 Months, by Intervention Condition, Mdantsane and Berlin, South Africa
Characteristic
All Learners
Boys
Girls
n Rural resident, no. (%) Age, y, mean (SD) Partner's age, y, mean (SD) Ever forced sex to have, no. (%) Intimate partner violence, mean (SD) Unprotected intercourse, no. (%) Multiple sexual partners, no. (%) Binge drinking, no. (%) HIV/STD intervention, no. (%) Any STD, no. (%) Chlamydia, no. (%) Gonorrhea, no. (%) Trichomoniasis, no. (%)
659 50 (7.59) 16.91 (1.21) 18.08 (2.55) 127 (19.27) 0.44 (0.87) 242 (36.89) 139 (21.55) 222 (34.31) 362 (54.93) 131 (19.88) 103 (15.53) 41 (6.22) 19 (2.88)
330 26 (7.93) 17.20 (1.26) 16.8 (1.93) 91 (27.74) 0.31 (0.60) 126 (38.53) 114 (35.29) 142 (44.38) 183 (55.79) 29 (8.84) 27 (8.23) 6 (1.83) 0 (0.00)
329 24 (7.32) 16.62 (1.08)* 19.3 (2.49)* 36 (10.98)* 0.57 (1.06)* 115 (35.17) 25 (7.79)* 80 (24.54)* 177 (53.96) 102 (31.10)* 76 (23.17)* 35 (10.67)* 19 (5.79)*
Unprotected intercourse and multiple sexual partners were reported over the past 3 months. Binge drinking was reported over the past month. Intimate partner violence is mean of 4 items regarding the frequency (0–6 or more times) of such victimization in the past year. *P < 0.001.
136
Sexually Transmitted Diseases
•
Volume 42, Number 3, March 2015
Copyright © 2015 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Sexually Transmitted Diseases
•
Volume 42, Number 3, March 2015
Unprotected intercourse and multiple sexual partners were reported over the past 3 months. Binge drinking was reported over the past month. Intimate partner violence is mean of 4 items regarding the frequency (0–6 or more times) of such victimization in the past year.
1.00 0.01 (0.839) 1.00 0.02 (0.636) 0.00 (0.935) 1.00 0.24 (
Associations Between Psychosocial Factors and Incidence of Sexually Transmitted Disease Among South African Adolescents Ann O'Leary, PhD,* John B. Jemmott III, PhD,† Loretta S. Jemmott, PhD,† Anne Teitelman, PhD,† G. Anita Heeren, MD,† Zolani Ngwane, PhD,‡ Larry D. Icard, PhD,§ and David A. Lewis, PhD¶║
Background: Adolescents living in South Africa are at high risk for HIV and other sexually transmitted diseases (STDs). The present study sought to identify correlates of curable STD incidence among a cohort of adolescents in Eastern Cape Province, South Africa. Methods: Data were collected in conjunction with an HIV/STD prevention intervention randomized controlled trial.1 At 54 months postintervention, curable STD incidence (gonorrhea, chlamydial infection, and trichomoniasis) was assayed and self-report measures of potential correlates of STD incidence were collected. Results: Participants were adolescents reporting at least 1 sexual partner in the past 3 months (n = 659). As expected, univariate analyses revealed that girls were more likely than boys to have an STD. In addition, intimate partner violence, unprotected sex, and having older partners were associated with incident STD. In Poisson multiple regression analyses, sex (risk ratio [RR], 4.00; 95% confidence interval [CI], 2.51–6.39), intimate partner violence (RR, 1.23; 95% CI, 1.12–1.35), unprotected sex (RR, 1.42; 95% CI, 1.09–2.01), and multiple partners (RR, 1.70; 95% CI, 1.11–2.61), but not partner's age (RR, 1.00; 95% CI, 0.94–1.07) were associated with incident STD, adjusting for 42-month STD prevalence. Binge drinking, forced sex, and age were unrelated to STD incidence in both analyses. Interactions between sex and the hypothesized correlates were nonsignificant, suggesting that sex did not modify these relationships. Conclusions: Interventions to reduce HIV/STD incidence among adolescents in South Africa should address the risk associated with sex, unprotected sex, intimate partner violence, and multiple partnerships.
From the *Centers for Disease Control and Prevention, Atlanta GA; †University of Pennsylvania, Philadelphia, PA; ‡Haverford College, Haverford, PA; Temple University, Philadelphia, PA; and ¶Centre for HIV and Sexually Transmitted Infections, National Institute for Communicable Diseases, Johannesburg, South Africa; and ║Centre for Infectious Diseases and Microbiology & Marie Bashir Institute for Infectious Diseases and Biosecurity, Westmead Clinical School, University of Sydney, Sydney, Australia Conflicts of interest and funding: No authors declare any conflicts of interest. Correspondence: Ann O'Leary, PhD, Division of HIV/AIDS, Centers for Disease Control and Prevention, 1600 Clifton Rd, MS E-37, Atlanta GA 30329. E-mail: [email protected]. Received for publication August 26, 2014, and accepted December 26, 2014. Author notes: This study was funded by Research Grant R01 MH065867 from the National Institute of Mental Health. The National Institute of Mental Health had no role in the design and conduct of the study, preparation, review, or approval of the manuscript. The findings and conclusions are those of the authors and do not represent the views of the Centers for Disease Control and Prevention. DOI: 10.1097/OLQ.0000000000000247 Copyright © 2015 American Sexually Transmitted Diseases Association All rights reserved.
Sexually Transmitted Diseases
•
S
exually transmitted disease (STD) represents a significant health problem for South African adolescents. The World Health Organization has estimated that of a population of 384.4 million, 92.6 million curable STIs occurred in the African Region in 2008.2 Although correlates of STD have been identified for a variety of populations, few such studies have been conducted among adolescents in Sub-Saharan Africa.3–5 In one study,4 a sexual risk reduction intervention produced a significant reduction in incidence of herpes simplex virus-2. Studies on other populations, however, have revealed some general correlates. One of these is sex, with females more susceptible to STD due to biological, economic, and social factors.6 Another is having a much older sexual partner, which is common among women in Sub-Saharan Africa7 and puts women, especially, at risk for STD,8–10 including HIV. It should be noted, however, that although very few studies have examined effects of age disparity on boys' STD risk, there is some evidence suggesting that boys are more likely to be infected with HIV when their most recent female partner was older.11 Binge drinking has also been shown to be predictive of STD incidence.12,13 A study by Boden and colleagues,12 which was conducted among men and women aged 15 to 30 years in New Zealand, showed an alcohol dose effect with higher levels of alcohol consumption and more symptoms of dependence, related to more STD. In South Africa, shabeens—casual houses where beer is sold and consumed—are ubiquitous. It is understood that if a man buys a girl a beer, she is expected to have sex with him. Intimate partner violence has been found to be correlated with STD among US women and male perpetrators of violence14,15 and with HIV infection in South Africa.16 South Africa has high rates of rape,17 and forced sex has been shown to be associated with STD both in the United States18,19 and in South Africa.20 Self-reported sexual behavior has been an inconsistent correlate of STD. Having multiple sex partners has been shown to predict STD21 and HIV22 in some studies, but not others.23 Condom use has also been examined as an STD predictor. In an early study,24 condom use was found to be unrelated to STD incidence, probably because contracting a STD requires that the person be exposed to an infected partner. Thus, people who have unprotected sex with partners who do not have an STD will not contract an STD, diminishing the relation between self-reported behavior and STD.25 The present study was designed to identify correlates of curable STD at 54 months postintervention in the “Let Us Protect Our Future” trial.1,26 No STD assessment was done at baseline, but as only 3% of participants were sexually active at that time, it can be assumed that the overwhelming preponderance of infections happened after the 8-day intervention. At 42 months, all identified STD was treated, so that curable STD at 54 months can be taken as an incidence measure. We hypothesized that curable STD incidence would be predicted by older age, female sex, risk reduction intervention arm,
Volume 42, Number 3, March 2015
135
Copyright © 2015 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
O'Leary et al.
binge drinking, having experienced intimate partner violence, having been raped, having had condom-unprotected sex, multiple partners, and having older partners. We examined these relationships in bivariate analyses as well as in Poisson multiple regression.
METHODS The institutional review board (IRB) no. 8 at the University of Pennsylvania, which was the designated institutional review board under the federal-wide assurances of the University of Pennsylvania and the University of Fort Hare, approved the study. The laboratory testing was additionally approved by the Human Research Ethics Committee (Medical) of the University of the Witwatersrand, South Africa. We conducted the study in Mdantsane, an urban township, and Berlin, a neighboring rural settlement, in Eastern Cape Province, South Africa, where isiXhosa is the first language of 95.1% of the population. The participants were adolescents who enrolled in a schoolbased cluster-randomized controlled trial of an HIV/STD riskreduction intervention. Schools that taught sixth-grade learners and served the general population were eligible. All 35 eligible schools (26 in Mdantsane, 9 in Berlin) agreed to participate. From 17 matched pairs of schools similar in numbers of sixth-grade learners, numbers of classrooms, and whose classrooms had electricity, we randomly selected 9 and randomized within pairs 1 school to the HIV/STD risk-reduction intervention and one to the health-promotion-control intervention. Methods for the intervention study are described in detail elsewhere.26 We enrolled 18 schools for 13 months beginning in October 2004. The initial informed-consent process covered activities through the 12month follow-up. Accordingly, we located the original participants who were now dispersed to more than 100 secondary schools and gave them parent/guardian consent forms and cover letters explaining the continuation of the trial and inviting their parents or guardians to a meeting where they could receive additional information and ask questions about the follow-up study. This article is based on the 54-month follow-up data. The 42-month follow-up data were collected beginning in April 2008, and the 54-month data collection was completed by June 2010.
Measures Incident STD. At the 42- and 54-month follow-up assessments, participants provided a urine specimen after completing
the self-report questionnaire. First-pass urine specimens were delivered to the Centre for HIV and STIs at the National Institute for Communicable Diseases, Johannesburg, South Africa, and assayed for Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (NG) using the Gen-Probe APTIMA Combo 2 Assay (Gen-Probe, Inc, San Diego, CA) and for Trichomonas vaginalis (TV) using the APTIMA TV assay (Gen-Probe, Inc). All participants with a positive curable STD (CT, NG, or TV) test received directly observable single-dose antimicrobial treatment and risk-reduction counseling per Centers for Disease Control and Prevention recommendations. The outcome variable in the present analysis is the incidence of any of these STDs at 54 months. Participants received a binary code based on whether they had any STD or not. The predictor variables included age, sex, study arm, binge drinking, intimate partner violence, history of forced sex, any unprotected sex, multiple partners, and participants' report of age of sexual partner assessed at 54-month follow-up. Unprotected Vaginal Intercourse. Participants were coded as having unprotected vaginal intercourse if they reported having vaginal intercourse without using a condom in the previous 3 months. Multiple Partners. Participants reporting 2 or more sexual partners in the previous three months were coded as having multiple partners. Forced Sex. History of forced sex was assessed with a single item: “Have you ever been forced to have vaginal intercourse against your will?” Intervention Condition. Intervention condition was a dichotomous variable indicating whether the participant had been in the sexual risk reduction intervention or the health promotion control intervention. Binge Drinking. Respondents were asked how many times in the past month they had had 5 or more drinks of alcohol. Participants were coded as having had a binge drinking episode if they reported having 5 or more drinks of alcohol on a single occasion in the past month. Intimate Partner Violence. This was assessed with the physical abuse subscale of the Conflict in Adolescent Dating Relationships Inventory.27 We averaged 4 items to create a scale. The items assessed estimates of the number of times each event had occurred during the preceding year, with responses ranging from “0” to “6 or more.” The item stem was “In the last year,
TABLE 1. Characteristics of Learners Reporting at Least 1 Sexual Partner in the Past 3 Months, by Intervention Condition, Mdantsane and Berlin, South Africa
Characteristic
All Learners
Boys
Girls
n Rural resident, no. (%) Age, y, mean (SD) Partner's age, y, mean (SD) Ever forced sex to have, no. (%) Intimate partner violence, mean (SD) Unprotected intercourse, no. (%) Multiple sexual partners, no. (%) Binge drinking, no. (%) HIV/STD intervention, no. (%) Any STD, no. (%) Chlamydia, no. (%) Gonorrhea, no. (%) Trichomoniasis, no. (%)
659 50 (7.59) 16.91 (1.21) 18.08 (2.55) 127 (19.27) 0.44 (0.87) 242 (36.89) 139 (21.55) 222 (34.31) 362 (54.93) 131 (19.88) 103 (15.53) 41 (6.22) 19 (2.88)
330 26 (7.93) 17.20 (1.26) 16.8 (1.93) 91 (27.74) 0.31 (0.60) 126 (38.53) 114 (35.29) 142 (44.38) 183 (55.79) 29 (8.84) 27 (8.23) 6 (1.83) 0 (0.00)
329 24 (7.32) 16.62 (1.08)* 19.3 (2.49)* 36 (10.98)* 0.57 (1.06)* 115 (35.17) 25 (7.79)* 80 (24.54)* 177 (53.96) 102 (31.10)* 76 (23.17)* 35 (10.67)* 19 (5.79)*
Unprotected intercourse and multiple sexual partners were reported over the past 3 months. Binge drinking was reported over the past month. Intimate partner violence is mean of 4 items regarding the frequency (0–6 or more times) of such victimization in the past year. *P < 0.001.
136
Sexually Transmitted Diseases
•
Volume 42, Number 3, March 2015
Copyright © 2015 by the American Sexually Transmitted Diseases Association. Unauthorized reproduction of this article is prohibited.
Sexually Transmitted Diseases
•
Volume 42, Number 3, March 2015
Unprotected intercourse and multiple sexual partners were reported over the past 3 months. Binge drinking was reported over the past month. Intimate partner violence is mean of 4 items regarding the frequency (0–6 or more times) of such victimization in the past year.
1.00 0.01 (0.839) 1.00 0.02 (0.636) 0.00 (0.935) 1.00 0.24 (
