Adolescent HIV Prevalence, Sexual Risk, and Willingness to Participate in HIV Vaccine Trials

Article Outline

• Abstract
• Methods
• Results
• Discussion
• Acknowledgment
• References
• Copyright

Abstract 

Purpose

To determine human immunodeficiency virus (HIV) prevalence, sexual risk behaviors, and attitudes toward HIV vaccine trials among 11–19 year-olds in a peri-urban community near Cape Town, South Africa.

Methods

We performed HIV antibody testing on oral transudate, and assessed sexual risk behaviors and willingness to participate in HIV vaccine trials using self-administered questionnaires.

Results

Of the 510 adolescents selected, 356 (73%) participated. The HIV prevalence of the group was 10.6% (95% confidence interval [CI] 7.5–14.4). One-third of adolescents had experienced sexual debut, with a mean age of 14.6 years. Number of lifetime sexual partners was independently associated with HIV infection (odds ratio [OR] = 1.62; 95% CI 1.1–2.3). In a multivariate analysis, increasing age, female gender, and attending school were independently associated with having had sex. The majority of adolescents (79%) were willing to participate in an HIV vaccine trial. Increasing age and length of residence in the community were significantly associated with willingness to participate (OR = 1.19; 95% CI 1.01–1.4 and OR = 1.14; 95% CI 1.03–1.26, respectively).

Conclusions

The prevalence of HIV and risk behavior among adolescents in this community is high. HIV vaccines are required that target preadolescents. HIV vaccine trials in adolescents in this setting will be facilitated by their willingness to participate.

Keywords: Adolescents, HIV vaccine trials, HIV prevalence, HIV risk, South Africa

There are more human immunodeficiency virus (HIV)-infected people living in South Africa than in any other country in the world, with a national HIV prevalence of 11.4% [1]. Worldwide, the fastest growing age group of HIV-infected people is youth. HIV prevalence from the South African Department of Health’s annual antenatal survey showed that in 2003, the rates of HIV seropositivity at antenatal testing for 15-, 16- and 17-year-olds were 8.5%, 9.4%, and 12.5%, respectively [2]. The 2004 data showed that the prevalence among 15-year-olds had risen to 10% [3].

There have been two large, cross-sectional studies with nationally representative samples that provide data regarding HIV prevalence and risk in children and young adults in South Africa. The prevalence rates in the 15- to 24-year age group ranged from 10.2% to 13% [1], [4] with as many as three times more females infected than males. These and other surveys also reported unprotected sex and coercive sex, with approximately 10% of the adolescent girls reporting sex against their will [1], [4], [5].

Although HIV infection rates of adolescents and young adults vary between countries, it is apparent that youth in most cultures are at risk for HIV infection. Therefore, it is critically important that adolescents and preadolescents are prioritized for primary immunization should a preventive HIV vaccine become available. The immunology and physiology of adolescents differ from those of adults, and it cannot be assumed that the response to vaccine candidates will be the same [6], [7]. A delay in implementing HIV vaccine trials in this vulnerable population may result in excluding youth from early pivotal efficacy trials. This would result in extended time to vaccine licensure for adolescents, with a consequent loss of many lives.

Enrollment of adolescents in HIV vaccine trials requires (a) the identification of potential communities willing to allow HIV vaccine trials to include their adolescents, (b) evaluation of the HIV incidence and prevalence of adolescents in these communities, and (c) evaluation of the risk of HIV exposure among potential trial participants. In general, HIV vaccine efficacy trials require large numbers of high-risk individuals. Knowledge of HIV risk among preteens and younger teens is required to identify high-risk cohorts.

Most data published about the sexual behavior of South Africa youth excludes adolescents below 15 years of age [5], and these studies have confined themselves to school settings [8], [9], [10]. This is possibly due to the challenges that accompany such research in young teens. Knowledge is lacking in a number of other important areas. Firstly, little, if anything, is known about the adolescent HIV risks in the specific settings where HIV vaccine trials are being conducted. Secondly, there are few data on whether adolescents and their parents or guardians in developing world settings would be willing to participate in HIV vaccine trials. Adults from at-risk communities in the United States and from other developed countries report varying degrees of willingness to take part in trials, and willingness has, in some instances, been associated with education level, knowledge of vaccines, and HIV risk [11], [12], [13]. Lastly, although some data from adolescents in the developed world point to the possibility that HIV vaccines may not be universally accepted by adolescents [14], [15], no parallel data from adolescents in developing countries exists.

In preparation for the inclusion of adolescents in HIV vaccine trials, we conducted a cross-sectional study of HIV prevalence, sexual behaviors, and attitudes to HIV vaccines and vaccine trials among randomly selected 11–19-year-olds in a peri-urban community. This study aims to explore issues regarding HIV risk, HIV vaccine acceptability, and willingness to participate in HIV vaccine trials identified through research done largely among adults in developed countries, among high-risk adolescents living in sub-Saharan Africa where most HIV vaccine efficacy trials are likely to take place.

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Methods 

The study was conducted between August 2004 and March 2005 in a peri-urban, Xhosa-speaking community near Cape Town. Following an established approach to approximate simple random sampling based on incomplete enumeration data [16], we used 2002 census information to randomly select 781 adolescents on 385 of the 864 plots in the community that contained at least one adolescent between the ages of 11 and 19 years, with probability of household selection proportional to the number of adolescents living within the home. Then, within each home, fieldworkers used a random number scheme to select eligible adolescents, the number of which was determined by the number of adolescents that were selected from that plot as described above. A smaller, second random selection was performed, following the same methods to replace those plots that were found not to have eligible adolescents due to population changes since the initial census (n = 271). Overall, 510 adolescents were selected to participate, representing approximately one-third of individuals in the eligible age range living in the community.

Ethics approval was obtained from the University of Cape Town Health Sciences Research Ethics Committee. Written informed consent or assent was obtained from the adolescents and from a parent or guardian of participants under 18 years. The only eligibility criteria were age 11 to 19 years, and the ability and willingness to provide written consent from relevant parties.

After consent was obtained from adolescents and parents in the homes, the adolescents were invited to the local clinic where the study was conducted. Saliva samples were obtained using the OraSure HIV-1 oral specimen device, and were analyzed for HIV-1 using the Vironostika uniform II oral fluid assay (Organon Technika, Boxtel, Netherlands). Results were anonymous, labeled with participant identification number only for linkage to the questionnaires. At no time were participant names recorded. Participants wishing to know their HIV status were referred to the HIV testing service operated on site by the local clinic (although because of anonymity, the number of adolescents who sought their HIV results separately is unknown).

Data on participant demographic characteristics and sexual behaviors were collected using either a self-administered paper-based instrument or direct data entry using Palm™ Pilot handheld devices. The method of data collection was assigned at random as part of a separate reliability study that demonstrated good intermethod reliability of sexual behavior reporting (unpublished observation). The survey instrument contained 71 questions, covering the following domains: demographics, sexually transmitted infection symptoms and treatment, sexual history (including partner history), condom use, transactional sex, and coerced sex. Additional items investigated willingness to participate in HIV vaccine trials. All responses were multiple choice, with the option to refuse to answer. Both methods of data collection presented the identical items with the same phrasing, options, and question order in both English and the local language, isiXhosa. Participants received instruction in the use of handheld devices before completion. Although the literacy rate among youth in this community is high, the study coordinator was available to assist adolescents who needed help in reading the study questions. All data collection was anonymous and confidential. Participants received transport reimbursement and a snack for their attendance to study visits.

Paper questionnaires were manually entered and verified in Questionnaire Development System™ (QDS). The data from the Palm™ Pilot questionnaires were transmitted via modem and captured in Microsoft Excel. Data were then analyzed using Stata Version 9.0 (StataCorp LP, College Station, Texas). Bivariate analyses using chi-square, Fisher’s exact and t-tests were performed to examine the associations between participant demographic characteristics, sexual risk behaviors, and HIV status. Odds ratios and 95% confidence intervals were calculated for HIV status and willingness to participate. Separate multiple logistic regression models predicting HIV status, sexual behavior, willingness to participate, and HIV vaccine acceptability were developed to examine associations after multiple statistical adjustments. Variables were included in the models if they demonstrated appreciable bivariate associations, and were removed from models if their associations did not persist and their removal did not affect associations involving other covariates. The results of logistic regression models are presented as odds ratios (OR) with 95% confidence intervals (CI). All statistical tests are two-sided at α = .05.

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Results 

Of the 510 adolescents selected to participate in the survey, consent was obtained from 356 of the adolescents and their parents or legal guardians, where appropriate, and therefore, a total of 356 adolescents were enrolled. Of the 154 that did not enroll, 35 were nontraceable; one died, 15 were not at home despite multiple visits, and 19 moved due to relocation or shack fires. The remaining 119 were refusals; 42 (35%) were documented as parental refusal; for the remainder, either the adolescent refused (n = 18, 15%) or this was not documented (n = 59, 50%). After excluding relocated adolescents, the response rate was 73%.

Participant demographic characteristics and sexual risk behaviors are shown in Table 1. The median age of the participants was 15 years. The median level of education was eighth grade, and 68% (242) of participants were female. The median duration of residence in the community was 5 years (range 1–18 years); 87% (286) of the adolescents lived with either their mother or father, and 45% (149) lived with both their parents.

Table 1. Participant demographic characteristics and sexual risk behaviors, overall and by HIV status, with odds ratios for HIV infection; all cells are n (%) unless otherwise noted

Variable	Overall n = 356a	HIV negativebc (n = 296)	HIV positive (n = 35)	Odds ratio for HIV infection (95% CI)
Demographics
Female	227/329(64%)	190/281(68%)	23/30(77%)	1.6(.7–3.8)
Age 11–13 years	133/329(40%)	122/281	5/30(3.9%)	1.0
Age 14–16 years	96/329(29%)	80/281	11/30(12%)	3.4(1.1–10.0)
Age 17–19 years	100/329(30%)	79/281	14/30(15%)	4.3(1.2–3.1)
Mean grade (SD)	7.4 SD 2.7	7.3 n = 238	8.9 n = 25	1.3(1.5–12.5)
Sexual behaviors
Ever had sex	99/308(32%)	81/265(31%)	14/29(48%)	2.1(1.0–4.5)
Mean number of lifetime partners (SD)d	2.62 SD 2.03	.7(n=255)	1.8(n=29)	1.3(1.0–1.7)
Partner at first sex more than 5 years olderd	25/96(26%)	19/82(23%)	6/14(43%)	2.5(.8–8.1)
Ever received gift for sexd	13/96(13%)	9/76(12%)	3/14(21%)	2.0(.5–8.7)
Ever used condom–maled	14/22(64%)	13/20(65%)	1/2(50%)	.54(.03–10.0)
Ever used condom–femaled	41/76(54%)	32/63(51%)	9/13(69%)	2.17(.6–7.8)
Boyfriend ever forced sex (females only)d	11/70(15%)	7/58(12%)	4/12(33%)	3.6(.9–15)

HIV results were available from 332 adolescents, one of which was indeterminate. Of the remaining 331, the HIV prevalence was 10.6% (95% CI 7.5–14.4%) (Table 1). Gender stratification is not shown, as the number of HIV-positive males was small. Although females were more likely to be HIV positive, this was not statistically significant. Older age was associated with HIV positivity, as was grade. The HIV-positive adolescents had had a significantly larger number of lifetime partners than HIV-negative adolescents. In addition, females who had experienced coercive sex were three times more likely to be HIV infected. There was no correlation between HIV status and other risk behaviors such as condom use. In a model adjusting for age, gender, and school attendance, number of lifetime sexual partners was significantly associated with HIV status (OR 1.6; 95% CI 1.1–2.3).

The average age of sexual debut was 14.6 years (SD 2.0, range 7–19 years) for the 99 (32%) adolescents that reported having ever had sex. Of all sexually active adolescents, 25% reported experiencing their sexual debut with someone who was more than 5 years older (n = 26, 24 of whom were female). The average number of partners for sexually active participants was 2.6. In a logistic regression model of lifetime intercourse adjusting for age, gender, school attendance and living with parents, increasing age (OR 1.9; 95% CI 1.6–2.2), female gender (OR 2.3; 95% CI 1.2–4.7), and attending school (OR 3.1; 95% CI 1.1–9.0) were independently associated with having had sex. Fifty percent of the HIV-positive adolescents claimed to never have had sex (n = 15).

Sexual behavior stratified by age group demonstrated that high-risk activity was occurring in the 11–13-year age group. Five (3.9%) of this age group were HIV positive. Two (2%) reported having been raped, two (2%) had had oral sex, and six (5%) had had anal sex. Three (38%) of the sexually active 11- to 13-year-olds reported receiving gifts, money or food in exchange for sex.

Overall, 205 (79%) of the adolescents said that they would either definitely or probably be willing to participate in an HIV vaccine trial. Table 2 shows willingness to participate in an HIV vaccine trial vs. demographics and selected sexual behaviors. There was no difference in willingness to participate according to gender; however, willingness was strongly associated with increasing age, grade, and length of time of residence in the community. Sexually active adolescents were significantly more likely to be willing to participate, but HIV status was not associated with willingness. No other risk behaviors were associated with willingness to participate. In a multivariate analysis adjusting for sexual activity and school attendance, increasing age and length of residence in the community were significantly associated with willingness to participate (OR 1.2; 95% CI 1.0–1.4 and OR 1.1; 95% CI 1.0–1.3, respectively).

Table 2. Adolescents’ willingness to participate versus demographics and risk behaviors; all cells are n (%) unless otherwise noted

	If there was an HIV vaccine that needed to be tested in people, do you think you would take part in the research study and receive an experimental vaccine? (In other words, would you take a vaccine to help test if it is safe or prevents HIV?)
	Yes/maybe n = 205a	Probably not/no n = 54a	OR (95% CI)
Female	146/205(71%)	34/54(63%)	1.46(.78–2.73)
Mean age (SD)	15 SD 2.6	13.9 SD 2.7	1.16(1.03–1.31)
Years in community	6.6 SD 4.1	4.9 SD 3.0	1.13(1.03–1.24)
Mean grade (SD)	7.7 SD 2.7	6.9 SD 2.7	1.14(1.01–1.28)
Ever had sex	71/196(36%)	10/49(20%)	2.2(1.04–4.71)
Mean age of first sex (SD)b	15 SD 1.9	13.9 SD 2.8	1.25(.93–1.68)
Mean number of partners (SD)b	2.6 SD 2	2.6 SD 1.67	.99(.73–1.36)
Ever used condomb	51/57(89%)	6/13(46%)	2.98(.89–9.94)
Boyfriend forced sexb	7/53(13%)	1/8(13%)	1.06(.11–10.0)
HIV positive	13/18(72%)	5/18(28%)	2.33(.67–8.09)

Reasons for and barriers to participation are shown in Table 3. The most common reasons for willingness were to help find a vaccine to protect their loved ones and the rest of the world, but also, hope that the study vaccine would protect them from HIV. In addition, 12% hoped the vaccine would cure them of HIV. The most common perceived barrier to participation was fear of unknown side effects, but 23% were afraid the vaccine could give them HIV.

Table 3. Adolescents’ reasons for willingness or barriers to participation in an HIV vaccine trial

	Percentagea
Motivating factor for participation
To help find a vaccine against HIV to protect their loved ones and the rest of the world	33
Hope that the study vaccine would stop them from getting HIV	33
To get free medical care	16
Hope that the vaccine would cure them from AIDS	12
To get money	11
Barriers to participation
Fear of unknown side effects	27
Fear that the vaccine could give them HIV	23
Afraid of needles	20
Don’t have enough time	11
Fear of what people might think	8

Participants also answered questions about their willingness to receive a safe and effective vaccine if one were available. There were 108 (42%) who stated they would accept it, 21 (8%) claimed they would not want to receive an HIV vaccine, and the remaining 50% were unsure or wanted more information. No demographic or sexual behavior factors were significantly associated with vaccine acceptance or refusal, including age (p = .12), gender (p = .18), and sexual activity (p = .10).

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Discussion 

This is the first study to explore HIV prevalence, sexual risk behaviors, and willingness to participate in HIV vaccine trials of adolescents in a potential vaccine trial site. Our study demonstrates that adolescents as young as 11 to 13 years are already at risk for HIV infection, and therefore would be potential beneficiaries for a preventative HIV vaccine and, consequently, HIV vaccine trials. Our data also show that adolescents are willing to participate in HIV vaccine trials. Their willingness and the high prevalence and risk make this community a suitable setting for adolescent phase III HIV vaccine trials.

This study highlights that HIV prevalence among adolescents in this community is high, including among young adolescents. Although older adolescents were more likely to be HIV infected in this study, the 14- to 16-year-old age category had a 12% HIV prevalence, and already 3.8% were infected in the 11–13-year age group. These infections are unlikely to represent mother-to-child transmission in a setting where 60% of vertically infected infants die by the age of two years, and where antiretrovirals had been available for less than one year. The increase in prevalence between age groups also indicates a high incidence in these young ages. Additionally, we found high-risk behavior already occurring in the 11- to 13-year-olds. The HIV prevalence and the presence of high-risk behavior in this young age group confirms that early adolescence is a critical time point for HIV prevention interventions.

These results should be interpreted carefully for several reasons. Our relatively small sample size means that the estimates of HIV prevalence within the different age categories are somewhat imprecise. Although our response rate (73%) was relatively high for this type of research, we cannot rule out the possibility of participation biases, although the impact of such biases (to increase or decrease the observed prevalence of HIV and high-risk sexual behaviors) is unclear. Similarly, response biases in the collection of high-risk sexual behaviors exist, although this concern is common to all studies of self-reported behaviors. Finally, hypothetical questions regarding HIV vaccine trials should be considered with caution, as they may be an overestimation of true enrollment [17].

The sexual risk of these adolescents is similar to that found in other African settings as well as in some developed countries. We found a higher number of HIV infections in those who had exchanged sex for gifts, and who had their first sexual encounter with a partner more than five years their senior. These findings are consistent with other data from African settings in which sexual relationships borne out of economic and age asymmetries are associated with poor condom use and higher HIV transmission [18]. A number of the younger age group (11 to 13 years) reported having had anal and oral sex, raising concerns of misconceptions in these youth around risk associated with such sex, as in other adolescents internationally [19], [20]. School attendance was positively associated with having reached sexual debut. In a study by Magnani et al performed in Zambia, school attendance was associated with lower levels of sexual activity [21]. This difference may be due to quality or quantity of HIV education in schools, or the environment of the adolescents when outside of school [21], [22]. Flisher at al found that having had sex in eighth grade, and having engaged in risky sex (as opposed to safer sex or not having had intercourse) strongly predicted dropout by grade 12 [23].

The adolescents in this community seemed willing to participate in HIV vaccine trials. In contrast to studies in other risk groups such as adult intravenous drug users [24], these adolescents reported mostly altruistic reasons for their willingness to participate. Willingness to participate may correlate with perceived risk for HIV, because those who are sexually active are more willing to participate in HIV vaccine trials. Indeed, Kiwanuka et al found an association between perceived risk and willingness to participate among 15–49-year-old Ugandans [25]. This same motivation was expressed by Thai army recruits [26] and Canadian men who have sex with men [27]. In microbicide studies, women’s motivations for the use of microbicides included protection against potential rape situations [28]. However, in our study, rape and sexual coercion do not correlate with willingness to participate, although the numbers in each group were small. Those adolescents who had lived in the community longer were more willing to participate; this could be due to more exposure to intense HIV vaccine education campaigns in the community. HIV vaccine awareness has correlated with willingness to participate in a number of settings, including among adults from India [13].

Our study did not examine the willingness of parents and guardians to allow their adolescents to participate in HIV vaccine trials, nor their attitudes around this subject. For adolescent participation to occur, researchers will need parental consent. Our data show that the majority of adolescents in this community were living with parents, making them accessible for proxy consent for intervention trials. In addition, our study, which included a noninvasive HIV test, did require parental consent to participate and this was obtained without difficulty. Adolescents in an “intervention trial” such as an HIV vaccine trial should be explored further.

Our findings support the inclusion of adolescents in HIV vaccine trials in this community. It is argued that at-risk adolescents may be difficult to recruit and obtain consent from for HIV vaccine trials, and that their understanding of difficult concepts may be limited. Although this study was observational, we found these adolescents were easily and rapidly recruited. The adolescents were willing to participate in HIV vaccine trials, and their reasons were altruistic. However, fewer adolescents were willing to accept a safe and effective vaccine than would be willing to participate in the vaccine trials themselves. This implies that the adolescents might not understand what the trials involve. In addition, there were misconceptions about HIV vaccines themselves in this group of adolescents, such as hope that the study vaccine would protect them from or cure them of HIV. HIV vaccine education has been occurring in this community for more than two years, and has targeted both youth and adults. Although we did not test HIV vaccine knowledge in this study, in Uganda, Kiwanuka et al found that, in general, the adolescents had poorer knowledge of HIV and HIV vaccines than the adults [25]. This implies more intense or more adolescent-appropriate education may have to take place before enrolling adolescents.

The adolescents in this community were reportedly less likely to accept a safe and effective vaccine against HIV than they were to participate in HIV vaccine trials. Among the data collected, we did not identify variables that were predictive of vaccine acceptance. Zimet et al found that certain health beliefs were predictive of HIV vaccine acceptability among 13–18-year-olds in the United States [29]. Our study did not specifically explore health beliefs of these adolescents. Others have found that vaccine characteristics are important in vaccine acceptability [11].

The HIV prevalence and sexual behavior of adolescents in South Africa and around the world demonstrates the importance of HIV vaccines for adolescent health. A delay in inclusion of adolescents in trials will result in a delay in licensure of a vaccine for this group. To achieve this, adolescent recruitment and retention strategies should be developed. Age-appropriate tools for both ensuring and assessing understanding should be developed. Assessment of true HIV incidence from adolescents in communities in which HIV vaccine efficacy trials are planned may be necessary. Although there are challenges specific to the inclusion of adolescents in HIV vaccine trials, these must be overcome as quickly as possible to ensure the rapid assessment of safety and efficacy of promising vaccine candidates in this important target group.

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Acknowledgment 

This work was supported by Elizabeth Glaser Pediatric AIDS Foundation Grant #22148PS and the South African AIDS Vaccine Initiative.

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