Advertisement
Research Article

School Based Sex Education and HIV Prevention in Low- and Middle-Income Countries: A Systematic Review and Meta-Analysis

  • Virginia A. Fonner mail,

    vtedrow@jhsph.edu

    Affiliation: Johns Hopkins Bloomberg School of Public Health, International Health Department, Baltimore, Maryland, United States of America

    X
  • Kevin S. Armstrong,

    Affiliation: Medical University of South Carolina, Department of Psychiatry and Behavioral Sciences, Charleston, South Carolina, United States of America

    X
  • Caitlin E. Kennedy,

    Affiliation: Johns Hopkins Bloomberg School of Public Health, International Health Department, Baltimore, Maryland, United States of America

    X
  • Kevin R. O'Reilly,

    Affiliation: Medical University of South Carolina, Department of Psychiatry and Behavioral Sciences, Charleston, South Carolina, United States of America

    X
  • Michael D. Sweat

    Affiliation: Medical University of South Carolina, Department of Psychiatry and Behavioral Sciences, Charleston, South Carolina, United States of America

    X
  • Published: March 04, 2014
  • DOI: 10.1371/journal.pone.0089692

Abstract

Objectives

School-based sex education is a cornerstone of HIV prevention for adolescents who continue to bear a disproportionally high HIV burden globally. We systematically reviewed and meta-analyzed the existing evidence for school-based sex education interventions in low- and middle-income countries to determine the efficacy of these interventions in changing HIV-related knowledge and risk behaviors.

Methods

We searched five electronic databases, PubMed, Embase, PsycInfo, CINAHL, and Sociological Abstracts, for eligible articles. We also conducted hand-searching of key journals and secondary reference searching of included articles to identify potential studies. Intervention effects were synthesized through random effects meta-analysis for five outcomes: HIV knowledge, self-efficacy, sexual debut, condom use, and number of sexual partners.

Results

Of 6191 unique citations initially identified, 64 studies in 63 articles were included in the review. Nine interventions either focused exclusively on abstinence (abstinence-only) or emphasized abstinence (abstinence-plus), whereas the remaining 55 interventions provided comprehensive sex education. Thirty-three studies were able to be meta-analyzed across five HIV-related outcomes. Results from meta-analysis demonstrate that school-based sex education is an effective strategy for reducing HIV-related risk. Students who received school-based sex education interventions had significantly greater HIV knowledge (Hedges g = 0.63, 95% Confidence Interval (CI): 0.49–0.78, p<0.001), self-efficacy related to refusing sex or condom use (Hedges g = 0.25, 95% CI: 0.14–0.36, p<0.001), condom use (OR = 1.34, 95% CI: 1.18–1.52, p<0.001), fewer sexual partners (OR = 0.75, 95% CI:0.67–0.84, p<0.001) and less initiation of first sex during follow-up (OR = 0.66, 95% CI: 0.54–0.83, p<0.001).

Conclusions

The paucity of abstinence-only or abstinence-plus interventions identified during the review made comparisons between the predominant comprehensive and less common abstinence-focused programs difficult. Comprehensive school-based sex education interventions adapted from effective programs and those involving a range of school-based and community-based components had the largest impact on changing HIV-related behaviors.

Introduction

Worldwide, young people aged 15–24 accounted for almost half of all new HIV infections among individuals aged 15 and older in 2010 [1]. School-based sex education is an intervention that has been promoted to increase HIV-related knowledge and shape safer sexual behaviors to help prevent new infections among this vulnerable group. As sexual debut is common in adolescence, so are the associated risks of engaging in transactional sex, having multiple concurrent partnerships, and experiencing sexual violence and coercion, all of which increase HIV-related risk [2]. School-based interventions are logistically well-suited to educate youth about sexual activity given their ability to reach large numbers of young people in an environment already equipped to facilitate educational lessons and group learning [3].

Contentious debates have raged in the past decade regarding whether abstinence-only or comprehensive sexual education interventions are effective and appropriate. Abstinence-only interventions promote delaying sex until marriage with little to no information provided about contraceptives or condom use, whereas comprehensive sexual education provides information on abstinence as well as information on how to engage in safer sex and prevent pregnancies and sexually transmitted infections (STIs). In the 1990s various groups in the United States invested in abstinence-only education, and with the creation of the President's Emergency Plan for AIDS Relief (PEPFAR) in 2004, money was earmarked for “ABC” programs (abstain, be faithful, use condoms), with a heavy emphasis on the “A” component, to be implemented in low- and middle-income countries most impacted by HIV [4]. Critics of abstinence-only education claim that it violates human rights by withholding potentially life-saving information from people about other means to protect themselves from HIV, such as condom use [5]. Others argue that abstinence is only a viable option for those who are able to choose when, how, and with whom to have sex, which is not always the case for many young women [6]. Additionally, promoting abstinence until marriage excludes gay children and adolescents who have no option for marriage in most countries. As an alternative, comprehensive school-based sex education programs present participants with all prevention options, including condom use and partner reduction. Abstinence-plus interventions present prevention options as hierarchical with abstinence being presented as the only strategy that completely eliminates HIV/STI risk.

Previous research has been conducted on the effectiveness of youth-oriented HIV prevention and sex education interventions in school settings. A review of 35 school-based sex education programs by Kirby and Coyle [7] found that abstinence based programs had no significant effect on delaying sexual debut, while some comprehensive programs were effective in reducing certain sexual risk behaviors. Gallant and Maticka-Tyndale [3] reviewed 11 school-based HIV education programs in Africa and concluded that most studies had an effect on either increasing HIV-related knowledge or changing attitudes or behaviors relating to sexual risk. Paul-Ebhohimhen et al. [8] systematically reviewed 10 school-based sex education studies implemented in sub-Saharan Africa and noted that interventions were more likely to report changes in knowledge as opposed to changes in sexual behavior. Speizer et al. [9] reviewed 41 adolescent reproductive health interventions in developing countries, including 22 based in schools, and found that the majority of school-based interventions (17/21) demonstrated improved HIV-related knowledge. Chin et al. [10] conducted parallel systematic reviews and meta-analyses of comprehensive and abstinence-only educational interventions and found that comprehensive sex education programs significantly reduced HIV, STI, and unintended pregnancies, but results for the abstinence-only review were inconclusive.

However, few reviews have attempted to quantitatively synthesize the effects of school-based interventions on HIV-related risk behaviors across studies, and no review to date has attempted to compare the effectiveness of abstinence-only or abstinence plus interventions with comprehensive sex education in low- and middle-income countries. Therefore, the current review seeks to address this gap by conducting a systematic review and meta-analysis on the efficacy of school-based sex education interventions, including abstinence-only/abstinence-plus and comprehensive sex education programs, in changing HIV-related knowledge and risk behaviors in low- and middle-income countries. This review sought to answer the following research question: Does participating in school-based sex education vs. not participating in school-based sex education reduce HIV-related risk behaviors among youth in low- and middle-income countries?

Methods

This review is part of a large systematic review and meta-analysis project, called The Evidence Project, which is a joint collaboration between investigators at the Medical University of South Carolina and the Johns Hopkins Bloomberg School of Public Health. The Evidence Project reviews the efficacy of behavioral HIV prevention interventions in low- and middle-income countries. Other reviews published with this project include topics such as voluntary counseling and testing [11], [12], provider-initiated testing and counseling [13], condom social marketing [14], behavioral interventions for people living with HIV [15], peer education [16], psychosocial support [17], mass media [18], and treatment as prevention [19]. This review used standardized data abstraction forms and procedures that have been employed in all reviews published as part of The Evidence Project, although no standalone protocol has been published specifically for this review. Additionally, we followed standard systematic review and meta-analysis procedures set forth in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [20].

Definition and Inclusion Criteria

School-based sex education was defined as programs designed to encourage sexual risk reduction strategies for HIV prevention delivered in school settings. This definition allowed for the inclusion of abstinence-only, abstinence-plus, and comprehensive sex education programs. Studies included in the review had to meet the following criteria: conducted in a low- or middle-income country as defined by the World Bank [21]; published in a peer-reviewed journal from January 1, 1990 to June 16, 2010; presented results of pre-post or multi-arm experimental design and analysis of outcome(s) of interest; and involved an HIV prevention intervention administered in a school setting that encouraged one or more sexual risk reduction strategies, including abstinence, condom use, or partner reduction.

There were no restrictions on language; eligible non-English articles were translated by consultants fluent in English and the language in which the article was written. Participant age was also not restricted. Therefore, studies across a variety of educational settings, from primary schools through college and vocational schools, were included. Additionally, in order to include as many studies as possible, a wide range of study designs were eligible for inclusion: randomized controlled trials (both individual and cluster-randomized, i.e., school or classroom), non-randomized controlled trials, prospective or retrospective cohorts, time-series, before-after, case-control, cross-sectional, and serial cross-sectional studies.

Search strategy

Our search strategy involved three methods. First, five electronic databases, including PubMed, PsycInfo, EMBASE, CINAHL, and Sociological Abstracts, were searched using a combination of terms for sex education, schools/youth, and HIV or AIDS (full list available from the authors upon request). The search was limited to a date range of January 1, 1990 to June 16, 2010. We also searched the table of contents of AIDS, AIDS Care, AIDS and Behavior, and AIDS Education and Prevention for relevant citations. Finally, we searched the reference lists of all included studies for additional eligible studies. This process was iterative and continued until no additional studies were identified.

Trained research assistants conducted an initial screening of all citations and excluded studies clearly not relevant to school-based sex education. Two senior study staff members then independently screened all remaining citations and categorized studies as eligible for inclusion, not eligible for inclusion, or questionable. Discrepancies in categorization were resolved through consensus. Full article texts were obtained and discussed by senior researchers to ascertain eligibility if questionable. Articles were retained and included as background studies if they failed to meet the inclusion criteria but still contained information relevant to school-based sex education in low- and middle-income countries, including prior reviews, cost-effectiveness analyses, and qualitative studies.

Data Abstraction

The following data were abstracted from each eligible study using standardized forms: location, year(s) of study implementation, study setting, study population, sample size, study design, sampling frame and sampling methods, description of the intervention, composition of intervention and control groups (if applicable), length of follow-up, description of outcomes, effect sizes, confidence intervals, statistical tests employed, and study limitations. Two trained research assistants independently abstracted data from each study; any discrepancies were resolved through consensus. Data were double entered into EpiData version 3.1 (EpiData Association, Odense, Denmark) and later exported to an SPSS database (IBM SPSS Statistics for Windows, Version 20.0. Armonk, NY).

We also evaluated the methodological rigor of studies to assess risk of bias based on the following criteria: whether the study 1) included a cohort of participants, 2) had a control and experimental/intervention group, 3) compared baseline demographic equivalence of control and intervention groups, 4) compared outcome measures between control and intervention groups at baseline (if applicable), 5) contained both pre- and post-intervention data, 6) randomly selected participants for assessment (i.e. sampling strategy), 7) randomly assigned participants to the intervention, and 8) maintained a follow-up rate of greater than 80%.

Selection of outcomes

Outcomes were chosen for meta-analysis based on relevance to HIV prevention and frequency in available studies. The five most commonly reported outcomes across studies were: HIV knowledge, condom use, self-efficacy related to HIV prevention (e.g., confidence in refusing sex or confidence in using condoms during sex), initiation of first sex, and number of sexual partners. All outcomes were based on self-report. Studies containing at least one of these outcomes were included in meta-analysis if they met the following criteria:

  1. Provided an estimate of effect size and its variance, or provided statistics needed to calculate an effect size and variance. If enough information was not provided to calculate an effect size, study authors were contacted for clarification or additional statistics. If study authors did not provide this information after one month, the study was removed from the analysis.
  2. Presented pre-post or multi-arm results comparing either participants who received the intervention to those who did not, or comparing outcomes before and after the intervention. If results of a repeated measures analysis were reported, authors needed to provide the correlation between pre-post measurements or provide enough information to calculate the correlation between measurements. If these statistics were not available, either in publication or after request, and the study was a controlled design, an effect size was generated using post-intervention statistics provided groups were similar at baseline with respect to the outcome of interest and other relevant covariates.
  3. Presented an outcome of interest that was measured in such a way as to be comparable to outcomes assessed by other studies. In other words, outcomes needed to be similar enough to synthesize across studies.
  4. Presented data based on an individual unit of analysis (studies presenting classroom- or school-level data only were excluded from meta-analysis).

Meta-analysis

Using standard meta-analytic methods [22], we standardized effect sizes as either Hedges' g (for continuous outcomes) or odds ratios (for dichotomous outcomes). For several outcomes, including HIV knowledge, self-efficacy, and number of sexual partners, both continuous and dichotomous effect sizes were combined in meta-analysis. In these instances, Comprehensive Meta-Analysis (CMA) was used to either convert the standard mean difference into an odds ratio when transforming the effect size from continuous to dichotomous or vice versa using methods developed by Hasselblad and Hedges [23]. This transformation assumes that the outcome under study involves an underlying continuous trait with a logistic distribution [24] and that outcomes are measured in relatively similar terms, regardless of whether they are presented dichotomously or continuously. For example, several studies reported number of sexual partners as a dichotomous outcome, such as having two or more partners in the past 6 months, whereas others reported a mean number of partners. The same logic holds for outcomes such as knowledge, where some studies presented knowledge outcomes on a continuous scale whereas others created a cut-off for “high” and “low” knowledge scores and presented results as a proportion. Combining both dichotomous and continuous effect sizes allowed us to utilize all available data.

CMA V.2.2 was used for all analyses [25]. Random effects models were used as included studies contained considerable heterogeneity of effects, and the purpose of the analysis was to generate inferences beyond the set of included studies [26].

When possible, data were analyzed in several ways per outcome. Stratifications by age, gender, instructor (e.g., teacher, peer, or health care professional), intervention type (abstinence vs. comprehensive sex education), and length of follow-up were made when three or more studies could be retained per category. Additionally, when possible, we investigated the role of certain characteristics of the data itself, including comparing differences between continuous and dichotomous effect sizes and whether the effect size was based on data collected pre-post intervention or post-only. Mixed effects meta-regression techniques were used to compare effect sizes across strata when possible. The I2 statistic and its confidence interval were calculated for each meta-analysis to describe inconsistencies in effect sizes across studies [24], [27]. When possible adjusted effect sizes were used in the pooled analyses; however, outcomes were most frequently reported in unadjusted terms, thus the analyses contain both adjusted and unadjusted effect sizes. Potential bias across studies, such as publication bias and selective reporting, was assessed for the HIV-related knowledge outcome by constructing a funnel plot. Funnel plots were not constructed for the remaining meta-analyses because there were too few studies to interpret the dispersion of effect sizes across the range of standard errors.

Results

Description of studies

Of 6191 studies initially identified, 64 studies in 63 articles met the inclusion criteria for this review (Figure 1). In five cases, more than one article presented data from the same study [28][39]. If articles from the same study presented different outcomes or follow-up times, both articles were retained and included in the review as one study [30], [31], [37], [38]. If both articles presented similar data, such as by providing an update with longer follow-up, the most recent article or the article with the largest sample size was chosen for inclusion [28], [33], [36], [39].

thumbnail

Figure 1. Disposition of citations during the search and screening process.

doi:10.1371/journal.pone.0089692.g001

Table 1 provides descriptions of included studies. The majority of studies took place in sub-Saharan Africa (n = 29, 45.3%). Studies also took place in East Asia/Pacific (n = 15, 23.4%), Europe/Central Asia (n = 2, 3.1%), Latin American/Caribbean (n = 16, 25.0%), and South Asia (n = 4, 6.3%). The most commonly used study design was a group randomized trial (n = 21), with schools or classrooms as the unit of randomization. Other study designs included individual randomized controlled trials (n = 4), before-after studies (n = 14), non-randomized individual trials (n = 2), non-randomized group trials (n = 12), serial cross-sectional studies (n = 4), cross-sectional studies (n = 5), and two studies utilized a study design classified as “other” which involved a hybrid of eligible study designs.

thumbnail

Table 1. Description of studies included in the review.

doi:10.1371/journal.pone.0089692.t001

Table 2 presents the methodological rigor assessment for included studies. Regarding methodological rigor, forty-seven studies used a control group, but only 18 studies reported whether intervention and control groups were equivalent on socio-economic variables at baseline, and only 14 reported whether intervention and control groups were equivalent on outcome measures at baseline.

thumbnail

Table 2. Methodological rigor of included studies.

doi:10.1371/journal.pone.0089692.t002

Most studies included both male and female participants; three studies evaluated school based sex education for girls only [40], [42]. Most studies (n = 56) took place among primary or secondary school students, five studies were implemented among university students [43][47], two involved secondary and university students [36], [48], one study involved student nurses [49], and another involved teacher trainees [50]. Ages of study participants ranged from 9, for an intervention among 4th graders in Mexico [51], to 38, for an intervention among university students in Malaysia [44]. Of the 27 studies reporting a mean age of study participants, the average age was 16.5 (SD = 2.7). Many studies included study populations with a wide range of ages. The age range in six studies spanned 10 years or more [52][55]. Generally, in studies measuring sexual risk behaviors, only a small portion of students in the study population were sexually active, thus substantially reducing the sample size for these outcomes.

Content of interventions.

Nine studies either taught abstinence-only or emphasized abstinence or delay of sexual debut over other risk reduction strategies among in-school youth [29], [33], [40], [41], [55][60]. The remaining studies provided comprehensive sex education.

Many studies reported using a variety of instructional formats to convey information and generate discussion. For example, 35 studies used lectures, 34 employed interactive discussions, 30 incorporated role-plays, and 21 utilized skill-based sessions, such as learning the steps involved in correct condom use. Use of media such as videos and audio tapes was also common. Two studies relied on drama, including creating plays and skits, for the bulk of the intervention [61], [62] and one study used a comic book to impart information [63]. Two studies were internet-based [36], [64] and involved students completing online modules during school hours at their own pace. Thirty three interventions reported basing their intervention on theory. Theories commonly referenced were Social Cognitive Theory, Health Belief Model, and Theory of Reasoned Action.

Intervention content varied widely. Several interventions were adapted from curricula that had been developed and implemented elsewhere, such as the US-based “Focus on Kids” [31], [38], [43], “Making Proud Choices” [41], and WHO's “Responsible Behavior: Delaying Sex” [40]. Other interventions worked with local community members and health educators to develop appropriate curricula. Forty-one studies included some form of commnity involvement in the intervention, such as consulting with parents and communities about what content could and could not be included in the intervention [33], [55], [56], [58], [60], [65][68]. Many studies reported a reluctance by teachers, parents, and/or communities to discuss or allow discussion of condoms during the intervention [33], [55], [56], [65], [66], [68]. Interventions commonly addressed health-related issues in addition to HIV/AIDS prevention (n = 43), including reproductive biology (n = 22), pregnancy prevention (n = 16), STI prevention (n = 22), relationships (n = 10), violence (n = 5), and values clarification (n = 5).

Intervention duration, location, and instructor type.

Interventions ranged from 2 or 3 hours in total [69], [70] to spanning multiple years and involving community-based components such as the creation of a youth resource center, youth-led condom distribution [30], [37], and training healthcare workers how to provide youth-friendly health information [68]. Most studies took place during the regular school day, although several studies included alternate times for the school-based sex education, such as having sessions on Saturdays [40] or after school hours [31], [38], [60]. Interventions were facilitated by health professionals, teachers, or peer educators, although several studies involved a mix of facilitator types throughout the intervention. The majority of studies took place in urban (n = 34) or peri-urban settings (n = 2). Only 3 studies specified that interventions took place in rural areas, 14 studies were conducted in a mix of urban and rural settings, and 11 studies did not provide enough information to determine the type of setting in which the intervention took place.

Meta-analysis results

HIV/AIDS knowledge.

HIV-related knowledge was the most commonly reported study outcome. Of all included studies, 49 (76.6%) evaluated the effect of the intervention on HIV-related knowledge. The measures used to assess HIV-related knowledge varied by study but centered on aspects such as HIV biology, HIV transmission, and HIV prevention. Some studies measuring HIV-related knowledge were excluded from meta-analysis for not controlling for baseline differences in socio-demographics or outcome variables (n = 3) [29], [71], [72], not providing enough data to convert results into standardized effect sizes (n = 18) [36], [47][50], [56], [57], [62], [63], [65], [69], [73][78], presenting knowledge outcomes not specifically related to HIV (n = 2), such as asking students whether they knew about HIV/AIDS [58], and measuring how many STIs students correctly identified [66].

Twenty-six studies were included in the meta-analysis for knowledge; results are presented in Table 3 and Figure 2. Nineteen studies reported knowledge as a continuous outcome; seven reported it dichotomously. In meta-analysis, dichotomous outcomes were converted to standardized mean differences for comparison across all studies. Random effects meta-analysis suggests that students who were exposed to a sexual education intervention were more knowledgeable of HIV and related topics than youth who did not experience an intervention. The standardized mean difference (Hedges' g) was 0.63 with a 95% confidence interval of 0.49 to 0.78, p<0.001. Meta-regression indicated no significant standardized mean difference when comparing males and females (p = 0.194); however, only 3 studies reported data disaggregated by gender with two additional studies reporting on entirely female samples. Similarly there was no significant difference in standardized mean knowledge score differences comparing abstinence-focused to comprehensive sex education interventions (p = 0.501). When stratified by instructor type, interventions led by health professionals (e.g. doctors, nurses, or health educators), appeared to produce more knowledgeable students than those led by either teachers, peers, or a mix of different types of instructors (β = 0.65, p = 0.004). However, when the two interventions implemented among college students were removed [42], [43], this effect was no longer significant.

thumbnail

Figure 2. Forest plots from meta-analysis of (A) HIV-related knowledge, (B) condom use, (C) self-efficacy, (D) number of sexual partners, and (E) initiation of sex.

A: Effect of school-based sex education on HIV-related knowledge (random effects, Hedges' G). B: Effect of school-based sex education on condom use (random effects, odds ratio). C: Effect of school-based sex education on self-efficacy (random effects, Hedges' G). D: Effect of school-based sex education on number of sexual partners (random effects, odds ratio). E: Effect of school-based sex education on initiation of first sex (random effects, odds ratio). Note. Results from Diaz et al., 2005, Fiscian et al., 2009, Givauden et al., 2008, Klepp et al., 1997, Visser et al., 1996, Visser et al., 2005, Cartagena et al., 2006, Okonofua et al., 2003, and Li et al., 2008 were adjusted for baseline differences and certain covariates. Values from remaining studies are unadjusted. *p<0.05, **p<0.010, and ***p<0.001.

doi:10.1371/journal.pone.0089692.g002
thumbnail

Table 3. Meta-analytic outcomes assessing associations between school-based sex education interventions and HIV/AIDS knowledge, condom use, initiation of first sex, number of sex partners, and self-efficacy.

doi:10.1371/journal.pone.0089692.t003

When considering length of follow-up time, standardized mean differences in knowledge scores were largest when data were collected 3 to 11 months post-intervention compared to all other categories of follow-up time (Hedges' g = 0.87, 95% CI 0.60–1.13, p<0.001). The smallest differences were seen when knowledge was measured 3 months or less post-intervention (Hedges' g = 0.70, 95% CI: 0.43–0.97, p<0.001). Studies with the shortest follow-up time generally corresponded to studies of the shortest duration (≤3 weeks). However, duration was difficult to measure due to wide variations in length and intensity of intervention implementation. Two studies evaluated the long-term effects (≥3 years post-intervention) of year-long interventions based in schools in Tanzania [30] and Kenya [68]. The study from Tanzania found that effects on knowledge remained significant after 3 years, but limited sustained effects on behaviors were seen [30]. The study from Kenya found significant improvements in HIV-related knowledge 3 years post-intervention, although knowledge initially appeared to decline in the period from pre-intervention to 18-months [68]. Regarding type of measure used, studies measuring knowledge as a dichotomous outcome generated smaller effect sizes than studies measuring knowledge continuously; this difference was statistically significant (β = −0.42, p = 0.02).

A funnel plot of the distribution of effect sizes by their standard error (figure not shown) suggests that some bias exists across studies as the plot was asymmetrical, indicating a possible underdispersion of less precise effect sizes. Following the assumption of normally distributed effect sizes across studies, finding more studies demonstrating at least a null effect would be expected, but finding studies showing a negative effect is less likely given the nature of the outcome, knowledge. Given the wide range of scales used to assess knowledge and the different facets of sexual education being taught across interventions, the asymmetrical plot could also be interpreted as presenting more evidence of a truly heterogeneous effect of school-based sexual education on HIV-related knowledge. The I2 value also supports this hypothesis.

Self-efficacy.

Twenty-two studies measured self-efficacy. Fourteen of these studies were excluded from meta-analysis for measuring general self-efficacy or self-efficacy not related to condom use or sex refusal (n = 8) [41], [46], [51], [64], [71], [79], [80] or for not providing enough data to convert to standardized effect size measures (n = 6) [50], [62], [73], [74], [77], [78]. The remaining eight studies measured self-efficacy related to either sex refusal or condom use and were included in meta-analysis [31], [43], [68], [81][85]. All but one study included in meta-analysis measured self-efficacy on a continuous scale; the remaining study measured self-efficacy as a proportion. The one dichotomous outcome was transformed into a standardized mean difference to allow comparison across studies. The standardized mean difference (Hedges' g) comparing those who received the intervention to those who did not was 0.25 (95% CI: 0.14–0.36, p<0.001), meaning those receiving the intervention exhibited significantly more self-efficacy in regards to being able to refuse sex or use a condom during sex. The intervention with the largest mean difference in self-efficacy was implemented among university students in Nanjing, China using an adapted version of the “Focus on Kids” program originally identified as an effective intervention by the U.S. Centers for Disease Control and Prevention (CDC), which involved group activities and games facilitated by trained graduate students and faculty [43]. The intervention with the second highest mean difference in self-efficacy involved an intervention delivered to secondary students in Ukraine by trained young physicians consisting of 6 weekly 1 hour sessions focusing on HIV transmission and biology, condom use negotiation skills, preventive measures, and dangers of drug use through small group activities, role playing, games, and discussions [83]. This intervention was adapted using the WHO Training and Resource Manual on School Health and HIV Prevention. One included study involving a 3 hour HIV-prevention workshop found no increase in condom use self-efficacy [85].

Condom use.

Twenty one studies measured condom use as a primary outcome. Of these, 13 were eligible for meta-analysis [31], [37], [52], [59], [66], [68], [73], [85][88]. Eight studies were excluded for not presenting enough data to convert to a standardized effect size [39], [43], [45], [62], [77], [78], [82], [89]. Condom measures included in the analysis were condom use at last sex, 100% condom use, and consistent condom use (all dichotomous measures). When synthesized across interventions, condom use was significantly higher among intervention participants (OR = 1.34, 95% CI: 1.18–1.52, p<0.001). Individually, only three of the twelve studies found a significant difference in condom use between intervention and control groups [37], [66], [68]. All three of these studies included some form of training for healthcare workers outside of the school-setting on how to provide youth-friendly sexual and reproductive health information, including condom use [37], [66], [68]. In one study based in Kenya, providing lessons on condom use was met with strong resistance from teachers who feared that teaching students about condoms would encourage sexual activity [68]. As a result, condom use was not included in the regular lesson plans although teachers were trained on how to respond to students' questions about condoms in a factual manner [68]. Of all interventions included in this meta-analysis, there was one abstinence-plus program that reported emphasizing delay of sexual debut until marriage while still provided information on other prevention measures, such as condom use [59]. This study did not find a significant difference in consistent condom use comparing those who received the intervention to those who did not 3-months post-intervention (OR = 1.13, 95% CI: 0.30–4.20, p = 0.86).

Number of sex partners.

Of 10 studies measuring participants' number of sexual partners, four were eligible for meta-analysis [31], [37], [58], [87]. Six were excluded for not containing enough data to convert results into standardized effect sizes [36], [45], [59], [62], [78], [90]. Of the four studies included in meta-analysis, three presented results dichotomously; the remaining study presented results continuously (mean number of sex partners). The continuous outcome was converted to a standardized mean difference to allow for comparison across all studies. Outcomes synthesized for this analysis included: having greater than 1 partner in the last 12 months [37], mean reported number of partners [58], having greater than 2 sexual partners in the last 6 months [31], and reporting multiple partners during the past 3 months [87]. Across studies students receiving interventions demonstrated a 25% reduction in odds of reporting more partners compared to control or comparison groups (OR = 0.75, 95% CI: 0.67–0.84, p<0.001). However, individually, only one study with a large sample size (n = 6877) showed students receiving the intervention reported fewer sex partners [37] whereas the other studies showed a non-significant difference. Data from this study were collected 36 months following the intervention, which was the longest reported follow-up of all included studies [37].

Initiation of first sex.

Nine studies measured initiation of first sex. Three were excluded for not containing enough data to convert results into standardized effect sizes for meta-analysis [62], [78], [90]. The remaining six studies were included in meta-analysis [31], [33], [37], [60], [68], [85]. All studies measured this outcome dichotomously. Participants who received the intervention had a 34% reduction in odds of initiating sexual intercourse during follow-up compared to control or comparison groups (OR = 0.66, 95% CI = 0.54–0.83, p<0.001). Individually all but one study [60] showed significant reductions in sexual debut for those who received the intervention. The study showing the highest reduction in sexual debut involved activities that took place beyond the classroom setting, including the provision of youth friendly reproductive health services, condom distribution, and community mobilization [37]. The one abstinence-only program that measured sexual initiation [33] also showed a significant reduction in odds of sexual debut between the 6th and 7th grade school years for youth who received the intervention (OR = 0.36, 95% CI 0.21–0.62, p<0.001).

Discussion

This review found that school-based sex education is an effective intervention for generating HIV-related knowledge and decreasing sexual risk behaviors among participants, including delaying sexual debut, increasing condom use, and decreasing numbers of sexual partners. Importantly, no individual study included in meta-analysis, including abstinence-only, abstinence-plus, and comprehensive school-based sex education interventions, found detrimental effects of school-based sex education on increased risky sexual behavior. This finding is notable given that some argue programs including information on abstinence and safe sex strategies give mixed messages to students and may promote sexual activity [91].

Comprehensive school-based sex education comprised the majority of interventions included in this review despite extensive attempts to identify abstinence-only and abstinence-plus interventions. Given PEPFAR's past emphasis on abstinence-only and abstinence-plus interventions [4], it is surprising to find so few peer reviewed evaluations of this strategy that met our inclusion criteria. The uneven distribution in comprehensive versus abstinence-only or abstinence-plus interventions made it difficult to compare the effectiveness of these intervention types. Additionally, many abstinence-only or abstinence-plus interventions measured outcomes related to HIV-knowledge but did not include outcomes related to sexual risk behavior, such as condom use or number of sexual partners, thus rendering comparisons to comprehensive sex education unfeasible. These findings are similar to those of parallel systematic reviews and meta-analyses comparing the effectiveness of comprehensive sex education and abstinence-only interventions, which found that although comprehensive sex education interventions were effective at reducing high-risk sexual behavior, no conclusion could be drawn from interventions emphasizing abstinence due to the small number of eligible studies and inconsistent findings [10].

Interventions producing the most significant changes in behavior seemed to have several characteristics in common. First, several effective interventions included community-based components that extended beyond school-based sex education by involving resources and activities outside of the school environment, such as training healthcare staff to offer youth-friendly services, distributing condoms, and involving parents, teachers, and community members in intervention development. Additionally, studies that adapted curricula from interventions already deemed efficacious also tended to produce significant changes on HIV-related behaviors. These findings are similar to another review which concluded that replicating effective sex education programs continued to produce significant behavior changes even when programs were implemented in different settings [92].

It is encouraging that many of the reviewed studies used controlled designs and randomized intervention assignments, especially as earlier reviews have emphasized the need to improve study designs when evaluating school-based sex education interventions [92], [93]. Despite this improvement, many studies exhibited methodological flaws that have been discussed at length elsewhere [94], which inhibited our ability to include these studies in meta-analysis. Out of 64 included studies, 50 measured at least one of the five outcomes included in this meta-analysis, and of these 33 provided enough data to include in the quantitative synthesis. This finding highlights the need to further improve the methodological rigor of studies.

Limitations

This review must be seen in light of several limitations. Firstly, all outcomes reported in this review were based on self-report, which creates potential for social desirability bias and memory error. Secondly, we combined outcomes in meta-analysis that are not identical, such as combining effect sizes generated from different scales measuring HIV-related knowledge, which could lead to inaccuracies in synthesized effects. We also combined both continuous and dichotomous outcomes in several meta-analyses, which could introduce error [95], although comparability has been shown between continuous and dichotomous outcomes used in meta-analysis when certain assumptions are met [96]. Additionally, it is possible our search strategy excluded potentially eligible articles. We used multiple search strategies in an effort to minimize this risk. This review could also be affected by publication bias, which was assessed by constructing funnel plots when feasible, although several studies showing null effects for various outcomes were included.

Conclusions

School-based sex education is a critical tool for HIV prevention among youth, and research suggests school-based HIV prevention programs are cost-effective when implemented in the context of combination prevention [97]. Intervention evaluations need to go beyond addressing the question of whether school-based sex education increases knowledge and focus instead on understanding implementation factors that led to the most success in shaping and changing subsequent HIV-related risk behaviors. As recently stated by the United Nations Special Rapporteur on the Right to Education, access to education about sex and reproductive health is a human right [98]; therefore greater efforts should be made to identify and scale-up effective interventions. However, school-based education alone cannot be relied on to prevent HIV infections among young people since not all young people attend school and since school funds and resources are often already strained. Instead, school-based sex education should be part of more holistic HIV prevention intervention aiming to engage young people in learning about and shaping their sexual and reproductive future.

Supporting Information

Checklist S1.

PRISMA Checklist for systematic reviews.

doi:10.1371/journal.pone.0089692.s001

(DOC)

Acknowledgments

The authors thank Samantha Herrera, Jewel Gausman, Alexandria Smith, Hieu Pham, Jeremy Lapedis, Erica Layer, Tina Dickenson, Eugenia Pyntikova, Lorraine Beraho, Meera Seshadri, and Aisha Yansaneh, for their coding work on this review. The authors also thank Sarah Robbins and Jenny Tighe for their help with formatting and manuscript review.

Author Contributions

Conceived and designed the experiments: MS KO CK VF. Analyzed the data: KA VF. Wrote the paper: VF KA CK KO MS.

References

  1. 1. UNAIDS (2012) UNAIDS Report on the Global AIDS Epidemic. Geneva, Switzerland.
  2. 2. Mmari K, Blum RW (2009) Risk and protective factors that affect adolescent reproductive health in developing countries: A structured literature review. Global Public Health 4: 350–366. doi: 10.1080/17441690701664418
  3. 3. Gallant M, Maticka-Tyndale E (2004) School-based HIV prevention programmes for African youth. Soc Sci Med 58: 1337–1351. doi: 10.1016/s0277-9536(03)00331-9
  4. 4. Santelli JS, Speizer IS, Edelstein ZR (2013) Abstinence promotion under PEPFAR: The shifting focus of HIV prevention for youth. Glob Public Health 8: 1–12. doi: 10.1080/17441692.2012.759609
  5. 5. Ott MA, Santelli JS (2007) Abstinence and abstinence-only education. Curr Opin Obstet Gynecol 19: 446–452. doi: 10.1097/gco.0b013e3282efdc0b
  6. 6. Wagman J, Baumgartner JN, Waszak Geary C, Nakyanjo N, Ddaaki WG, et al. (2009) Experiences of Sexual Coercion Among Adolescent Women: Qualitative Findings From Rakai District, Uganda. Journal of Interpersonal Violence 24: 2073–2095. doi: 10.1177/0886260508327707
  7. 7. Kirby D, Coyle K (1997) School-based programs to reduce sexual risk-taking behavior. Children and Youth Services Review 19: 415–436. doi: 10.1016/s0190-7409(97)00025-x
  8. 8. Paul-Ebhohimhen VA, Poobalan A, van Teijlingen ER (2008) A systematic review of school-based sexual health interventions to prevent STI/HIV in sub-Saharan Africa. BMC Public Health 8: 4. doi: 10.1186/1471-2458-8-4
  9. 9. Speizer IS, Magnani RJ, Colvin CE (2003) The effectiveness of adolescent reproductive health interventions in developing countries: a review of the evidence. J Adolesc Health 33: 324–348. doi: 10.1016/s1054-139x(02)00535-9
  10. 10. Chin HB, Sipe TA, Elder R, Mercer SL, Chattopadhyay SK, et al. (2012) The Effectiveness of Group-Based Comprehensive Risk-Reduction and Abstinence Education Interventions to Prevent or Reduce the Risk of Adolescent Pregnancy, Human Immunodeficiency Virus, and Sexually Transmitted Infections: Two Systematic Reviews for the Guide to Community Preventive Services. American Journal of Preventive Medicine 42: 272–294. doi: 10.1016/j.amepre.2011.11.006
  11. 11. Denison JA, O'Reilly KR, Schmid GP, Kennedy CE, Sweat MD (2008) HIV voluntary counseling and testing and behavioral risk reduction in developing countries: a meta-analysis, 1990–2005. AIDS Behav 12: 363–373. doi: 10.1007/s10461-007-9349-x
  12. 12. Fonner VA, Denison J, Kennedy CE, O'Reilly K, Sweat M (2012) Voluntary counseling and testing (VCT) for changing HIV-related risk behavior in developing countries. Cochrane Database Syst Rev 9: CD001224. doi: 10.1002/14651858.cd001224.pub4
  13. 13. Kennedy CE, Fonner VA, Sweat MD, Okero FA, Baggaley R, et al. (2012) Provider-Initiated HIV Testing and Counseling in Low- and Middle-Income Countries: A Systematic Review. AIDS Behav doi: 10.1007/s10461-012-0241-y
  14. 14. Sweat MD, Denison J, Kennedy C, Tedrow V, O'Reilly K (2012) Effects of condom social marketing on condom use in developing countries: a systematic review and meta-analysis, 1990–2010. Bull World Health Organ 90: 613–622A. doi: 10.2471/blt.11.094268
  15. 15. Kennedy CE, Medley AM, Sweat MD, O'Reilly KR (2010) Behavioural interventions for HIV positive prevention in developing countries: a systematic review and meta-analysis. Bull World Health Organ 88: 615–623. doi: 10.2471/blt.09.068213
  16. 16. Medley A, Kennedy C, O'Reilly K, Sweat M (2009) Effectiveness of peer education interventions for HIV prevention in developing countries: a systematic review and meta-analysis. AIDS Educ Prev 21: 181–206. doi: 10.1521/aeap.2009.21.3.181
  17. 17. Sweat M, O'Reilly K, Kennedy C, Medley A (2007) Psychosocial support for HIV-infected populations in developing countries: a key yet understudied component of positive prevention. AIDS 21: 1070–1071. doi: 10.1097/qad.0b013e3280f774da
  18. 18. Bertrand JT, O'Reilly K, Denison J, Anhang R, Sweat M (2006) Systematic review of the effectiveness of mass communication programs to change HIV/AIDS-related behaviors in developing countries. Health Educ Res 21: 567–597. doi: 10.1093/her/cyl036
  19. 19. Kennedy C, O'Reilly K, Medley A, Sweat M (2007) The impact of HIV treatment on risk behaviour in developing countries: a systematic review. AIDS Care 19: 707–720. doi: 10.1080/09540120701203261
  20. 20. Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6: e1000097. doi: 10.1371/journal.pmed.1000097
  21. 21. WorldBank In: Regions Ca, editor.
  22. 22. (1994) The Handbook of research synthesis. In: Cooper HM, Hedges LV, editors. New York :: Russell Sage Foundation.
  23. 23. Hasselblad V, Hedges LV (1995) Meta-analysis of screening and diagnostic tests. Psychological Bulletin 117: 167–178. doi: 10.1037/0033-2909.117.1.167
  24. 24. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to Meta-Analysis. John Wiley & Sons, Ltd.
  25. 25. Borenstein M, Hedges L, Higgins J, Rothstein;(2005) Comprehensive Meta Analysis (CMA). Version 2.2, Biostat, Englewood NJ
  26. 26. Hedges LV, Vevea JL (1998) Fixed-and random-effects models in meta-analysis. Psychological methods 3: 486. doi: 10.1037/1082-989x.3.4.486
  27. 27. Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327: 557–560. doi: 10.1136/bmj.327.7414.557
  28. 28. Agha S (2002) An evaluation of the effectiveness of a peer sexual health intervention among secondary-school students in Zambia. AIDS Educ Prev 14: 269–281. doi: 10.1521/aeap.14.5.269.23875
  29. 29. Agha S, Van Rossem R (2004) Impact of a school-based peer sexual health intervention on normative beliefs, risk perceptions, and sexual behavior of Zambian adolescents. J Adolesc Health 34: 441–452. doi: 10.1016/j.jadohealth.2003.07.016
  30. 30. Doyle AM, Ross DA, Maganja K, Baisley K, Masesa C, et al. (2010) Long-Term Biological and Behavioural Impact of an Adolescent Sexual Health Intervention in Tanzania: Follow-up Survey of the Community-Based MEMA kwa Vijana Trial. PLoS Med 7: e1000287. doi: 10.1371/journal.pmed.1000287
  31. 31. Fitzgerald AM, Stanton BF, Terreri N, Shipena H, Li X, et al. (1999) Use of Western-based HIV risk-reduction interventions targeting adolescents in an African setting. J Adolesc Health 25: 52–61. doi: 10.1016/s1054-139x(98)00120-7
  32. 32. Huang H, Ye X, Cai Y, Shen L, Xu G, et al. (2008) Study on peer-led school-based HIV/AIDS prevention among youths in a medium-sized city in China. Int J STD AIDS 19: 342–346. doi: 10.1258/ijsa.2007.007208
  33. 33. Klepp KI, Ndeki SS, Leshabari MT, Hannan PJ, Lyimo BA (1997) AIDS education in Tanzania: promoting risk reduction among primary school children. Am J Public Health 87: 1931–1936. doi: 10.2105/ajph.87.12.1931
  34. 34. Klepp KI, Ndeki SS, Seha AM, Hannan P, Lyimo BA, et al. (1994) AIDS education for primary school children in Tanzania: an evaluation study. AIDS 8: 1157–1162. doi: 10.1097/00002030-199408000-00019
  35. 35. Lou CH, Zhao Q, Gao ES (2005) Effects of high middle school students' learning sex and reproductive health knowledge by Internet. Fudan University Journal of Medical Sciences 32: 289–294.
  36. 36. Lou CH, Zhao Q, Gao ES, Shah IH (2006) Can the Internet be used effectively to provide sex education to young people in China? J Adolesc Health 39: 720–728. doi: 10.1016/j.jadohealth.2006.04.003
  37. 37. Ross DA, Changalucha J, Obasi AI, Todd J, Plummer ML, et al. (2007) Biological and behavioural impact of an adolescent sexual health intervention in Tanzania: a community-randomized trial. AIDS 21: 1943–1955. doi: 10.1097/qad.0b013e3282ed3cf5
  38. 38. Stanton BF, Li X, Kahihuata J, Fitzgerald AM, Neumbo S, et al. (1998) Increased protected sex and abstinence among Namibian youth following a HIV risk-reduction intervention: a randomized, longitudinal study. AIDS 12: 2473–2480. doi: 10.1097/00002030-199818000-00017
  39. 39. Ye XX, Huang H, Li SH, Xu G, Cai Y, et al. (2009) HIV/AIDS education effects on behaviour among senior high school students in a medium-sized city in China. Int J STD AIDS 20: 549–552. doi: 10.1258/ijsa.2008.008471
  40. 40. Enah C, Sommers M, Moneyham L, Ann Long C, Childs G (2010) Piloting an HIV Prevention Intervention for Cameroonian Girls. J Assoc Nurses AIDS Care doi: 10.1016/j.jana.2010.02.011
  41. 41. Fiscian VS, Obeng EK, Goldstein K, Shea JA, Turner BJ (2009) Adapting a multifaceted U.S. HIV prevention education program for girls in Ghana. AIDS Educ Prev 21: 67–79. doi: 10.1521/aeap.2009.21.1.67
  42. 42. Singh S (2003) Study of the effect of information, motivation and behavioural skills (IMB) intervention in changing AIDS risk behaviour in female university students. AIDS Care 15: 71–76. doi: 10.1080/095401202100039770
  43. 43. Li X, Stanton B, Wang B, Mao R, Zhang H, et al. (2008) Cultural adaptation of the Focus on Kids program for college students in China. AIDS Educ Prev 20: 1–14. doi: 10.1521/aeap.2008.20.1.1
  44. 44. Low WY (2004) Impact of sexual health course on Malaysian university students. Med J Malaysia 59: 443–449.
  45. 45. Miller AN, Mutungi M, Facchini E, Barasa B, Ondieki W, et al. (2008) An outcome assessment of an ABC-based HIV peer education intervention among Kenyan university students. J Health Commun 13: 345–356. doi: 10.1080/10810730802063470
  46. 46. Singh S, Bankole A, Woog V (2005) Evaluating the need for sex education in developing countries: Sexual behaviour, knowledge of preventing sexually transmitted infections/HIV and unplanned pregnancy. Sex Education 5: 307–331. doi: 10.1080/14681810500278089
  47. 47. Zheng YH, Yi LX, Yang X (2002) [Short-term effect evaluation of health education on the prevention of AIDS among university students in Changsha]. Hunan Yi Ke Da Xue Xue Bao 27: 515–518.
  48. 48. Gao Y, Lu ZZ, Shi R, Sun XY, Cai Y (2001) AIDS and sex education for young people in China. Reprod Fertil Dev 13: 729–737. doi: 10.1071/rd01082
  49. 49. Munodawafa D, Marty PJ, Gwede C (1995) Effectiveness of health instruction provided by student nurses in rural secondary schools of Zimbabwe: a feasibility study. Int J Nurs Stud 32: 27–38. doi: 10.1016/0020-7489(94)00029-j
  50. 50. Norr KF, Norr JL, Kaponda CPN, Kachingwe SI, Mbweza EMD (2007) Short-term effects of a peer group intervention for HIV prevention among trainee teachers in Malawi. African Journal of AIDS Research 6: 239–249. doi: 10.2989/16085900709490420
  51. 51. Pick S, Givaudan M, Sirkin J, Ortega I (2007) Communication as a protective factor: evaluation of a life skills HIV/AIDS prevention program for Mexican elementary-school students. AIDS Educ Prev 19: 408–421. doi: 10.1521/aeap.2007.19.5.408
  52. 52. Diaz M, Mello MB, Sousa MH, Cabral F, Castro e Silva R, et al. (2005) Outcomes of three different models for sex education and citizenship programs concerning knowledge, attitudes, and behavior of Brazilian adolescents. Cad Saude Publica 21: 589–597. doi: 10.1590/s0102-311x2005000200026
  53. 53. James S, Reddy P, Ruiter RA, McCauley A, van den Borne B (2006) The Impact of an HIV and AIDS Life Skills Program on Secondary School Students in KwaZulu-Natal, South Africa. AIDS Educ Prev 18: 281–294. doi: 10.1521/aeap.2006.18.4.281
  54. 54. Kuhn L, Steinberg M, Mathews C (1994) Participation of the school community in AIDS education: an evaluation of a high school programme in South Africa. AIDS Care 6: 161–171. doi: 10.1080/09540129408258627
  55. 55. Visser M (1996) Evaluation of the First AIDS Kit, the AIDS and lifestyle education programme for teenagers. S Afr J Psychol 26: 103–113.
  56. 56. Aplasca MR, Siegel D, Mandel JS, Santana-Arciaga RT, Paul J, et al. (1995) Results of a model AIDS prevention program for high school students in the Philippines. AIDS 9 Suppl 1: S7–13.
  57. 57. Saksena S, Saldanha S (2003) Impact of a course on human sexuality and adolescence. Indian J Pediatr 70: 203–206. doi: 10.1007/bf02725582
  58. 58. Shuey DA, Babishangire BB, Omiat S, Bagarukayo H (1999) Increased sexual abstinence among in-school adolescents as a result of school health education in Soroti district, Uganda. Health Educ Res 14: 411–419. doi: 10.1093/her/14.3.411
  59. 59. Thato R, Jenkins RA, Dusitsin N (2008) Effects of the culturally-sensitive comprehensive sex education programme among Thai secondary school students. J Adv Nurs 62: 457–469. doi: 10.1111/j.1365-2648.2008.04609.x
  60. 60. Wang LY, Davis M, Robin L, Collins J, Coyle K, et al. (2000) Economic evaluation of Safer Choices: a school-based human immunodeficiency virus, other sexually transmitted diseases, and pregnancy prevention program. Arch Pediatr Adolesc Med 154: 1017–1024. doi: 10.1001/archpedi.154.10.1017
  61. 61. Dalrymple L, du Toit MK (1993) The evaluation of a drama approach to AIDS education. Educational Psychology 13: 147–154. doi: 10.1080/0144341930130205
  62. 62. Harvey B, Stuart J, Swan T (2000) Evaluation of a drama-in-education programme to increase AIDS awareness in South African high schools: a randomized community intervention trial. Int J STD AIDS 11: 105–111. doi: 10.1258/0956462001915453
  63. 63. Milleliri JM, Krentel A, Rey JL (2003) [Sensitisation about condom use in Gabon (1999): evaluation of the impact of a comic book]. Sante 13: 253–264.
  64. 64. Halpern CT, Mitchell EM, Farhat T, Bardsley P (2008) Effectiveness of web-based education on Kenyan and Brazilian adolescents' knowledge about HIV/AIDS, abortion law, and emergency contraception: findings from TeenWeb. Soc Sci Med 67: 628–637. doi: 10.1016/j.socscimed.2008.05.001
  65. 65. Kinsman J, Nakiyingi J, Kamali A, Carpenter L, Quigley M, et al. (2001) Evaluation of a comprehensive school-based AIDS education programme in rural Masaka, Uganda. Health Educ Res 16: 85–100. doi: 10.1093/her/16.1.85
  66. 66. Okonofua FE, Coplan P, Collins S, Oronsaye F, Ogunsakin D, et al. (2003) Impact of an intervention to improve treatment-seeking behavior and prevent sexually transmitted diseases among Nigerian youths. Int J Infect Dis 7: 61–73. doi: 10.1016/s1201-9712(03)90044-0
  67. 67. Perez F, Dabis F (2003) HIV prevention in Latin America: reaching youth in Colombia. AIDS Care 15: 77–87. doi: 10.1080/0954012021000039789
  68. 68. Maticka-Tyndale E, Wildish J, Gichuru M (2010) Thirty-month quasi-experimental evaluation follow-up of a national primary school HIV intervention in Kenya. Sex Education 10: 113–130. doi: 10.1080/14681811003666481
  69. 69. Martiniuk AL, O'Connor KS, King WD (2003) A cluster randomized trial of a sex education programme in Belize, Central America. Int J Epidemiol 32: 131–136. doi: 10.1093/ije/dyg014
  70. 70. Torabi MR, Crowe JW, Rhine S, Daniels DE, Jeng I (2000) Evaluation of HIV/AIDS education in Russia using a video approach. J Sch Health 70: 229–233. doi: 10.1111/j.1746-1561.2000.tb07422.x
  71. 71. Caceres CF, Rosasco AM, Mandel JS, Hearst N (1994) Evaluating a school-based intervention for STD/AIDS prevention in Peru. J Adolesc Health 15: 582–591. doi: 10.1016/1054-139x(94)90143-q
  72. 72. Iurcovich M, Lourie KJ, Brown LK (1998) The AIDS prevention training program for high school students in Buenos Aires, Argentina. Journal of HIV/AIDS Prevention & Education for Adolescents & Children 2: 91–105. doi: 10.1300/j129v02n03_07
  73. 73. Cartagena RG, Veugelers PJ, Kipp W, Magigav K, Laing LM (2006) Effectiveness of an HIV prevention program for secondary school students in Mongolia. J Adolesc Health 39: 925 e929–916. doi: 10.1016/j.jadohealth.2006.07.017
  74. 74. Cheng Y, Lou CH, Mueller LM, Zhao SL, Yang JH, et al. (2008) Effectiveness of a school-based AIDS education program among rural students in HIV high epidemic area of China. J Adolesc Health 42: 184–191. doi: 10.1016/j.jadohealth.2007.07.016
  75. 75. Shen LX, Hong H, Cai Y, Jin XM, Shi R (2008) Effectiveness of peer education in HIV/STD prevention at different types of senior high schools in Shanghai, People's Republic of China. Int J STD AIDS 19: 761–767. doi: 10.1258/ijsa.2008.008053
  76. 76. Thakor HG, Kumar P (2000) Impact assessment of school-based sex education program amongst adolescents. Indian J Pediatr 67: 551–558. doi: 10.1007/bf02758475
  77. 77. Karnell AP, Cupp PK, Zimmerman RS, Feist-Price S, Bennie T (2006) Efficacy of an American alcohol and HIV prevention curriculum adapted for use in South Africa: results of a pilot study in five township schools. AIDS Educ Prev 18: 295–310. doi: 10.1521/aeap.2006.18.4.295
  78. 78. Magnani R, Macintyre K, Karim AM, Brown L, Hutchinson P, et al. (2005) The impact of life skills education on adolescent sexual risk behaviors in KwaZulu-Natal, South Africa. J Adolesc Health 36: 289–304. doi: 10.1016/j.jadohealth.2004.02.025
  79. 79. Chhabra R, Springer C, Rapkin B, Merchant Y (2008) Differences among male/female adolescents participating in a School-based Teenage Education Program (STEP) focusing on HIV prevention in India. Ethn Dis 18: S2–123–127.
  80. 80. Srisuphun W, Senaratana W, Fongkaew W, Potjanamart C, Soparat P (2002) School-based program for HIV/AIDS prevention for adolescent school children. Thai Journal of Nursing Research 6: 11–23.
  81. 81. Givaudan M, Leenen I, Van de Vijver FJ, Poortinga YH, Pick S (2008) Longitudinal study of a school based HIV/AIDS early prevention program for Mexican adolescents. Psychol Health Med 13: 98–110. doi: 10.1080/13548500701295256
  82. 82. Kinsler J, Sneed CD, Morisky DE, Ang A (2004) Evaluation of a school-based intervention for HIV/AIDS prevention among Belizean adolescents. Health Educ Res 19: 730–738. doi: 10.1093/her/cyg091
  83. 83. Kyrychenko P, Kohler C, Sathiakumar N (2006) Evaluation of a school-based HIV/AIDS educational intervention in Ukraine. J Adolesc Health 39: 900–907. doi: 10.1016/j.jadohealth.2006.06.006
  84. 84. Li S, Huang H, Cai Y, Ye X, Shen X, et al. (2010) Evaluation of a school-based HIV/AIDS peer-led prevention programme: the first intervention trial for children of migrant workers in China. Int J STD AIDS 21: 82–86. doi: 10.1258/ijsa.2009.008514
  85. 85. Martinez-Donate AP, Hovell MF, Zellner J, Sipan CL, Blumberg EJ, et al. (2004) Evaluation of two school-based HIV prevention interventions in the border city of Tijuana, Mexico. J Sex Res 41: 267–278. doi: 10.1080/00224490409552234
  86. 86. Fawole IO, Asuzu MC, Oduntan SO, Brieger WR (1999) A school-based AIDS education programme for secondary school students in Nigeria: a review of effectiveness. Health Educ Res 14: 675–683. doi: 10.1093/her/14.5.675
  87. 87. Visser MJ (2007) HIV/AIDS prevention through peer education and support in secondary schools in South Africa. SAHARA J 4: 678–694. doi: 10.1080/17290376.2007.9724891
  88. 88. Walker D, Gutierrez JP, Torres P, Bertozzi SM (2006) HIV prevention in Mexican schools: prospective randomised evaluation of intervention. BMJ 332: 1189–1194. doi: 10.1136/bmj.38796.457407.80
  89. 89. Smith EA, Palen LA, Caldwell LL, Flisher AJ, Graham JW, et al. (2008) Substance use and sexual risk prevention in Cape Town, South Africa: an evaluation of the HealthWise program. Prev Sci 9: 311–321. doi: 10.1007/s11121-008-0103-z
  90. 90. Daboer JC, Ogbonna C, Jamda MA (2008) Impact of health education on sexual risk behaviour of secondary school students in Jos, Nigeria. Niger J Med 17: 324–329. doi: 10.4314/njm.v17i3.37403
  91. 91. Stanger-Hall KF, Hall DW (2011) Abstinence-only education and teen pregnancy rates: why we need comprehensive sex education in the U.S. PLoS One 6: e24658. doi: 10.1371/journal.pone.0024658
  92. 92. Kirby DB, Laris BA, Rolleri LA (2007) Sex and HIV education programs: their impact on sexual behaviors of young people throughout the world. J Adolesc Health 40: 206–217. doi: 10.1016/j.jadohealth.2006.11.143
  93. 93. Kirby D (1992) School-based programs to reduce sexual risk-taking behaviors. J Sch Health 62: 280–287. doi: 10.1111/j.1746-1561.1992.tb01244.x
  94. 94. Magnussen L, Ehiri JE, Ejere HO, Jolly PE (2004) Interventions to prevent HIV/AIDS among adolescents in less developed countries: are they effective? Int J Adolesc Med Health 16: 303–323. doi: 10.1515/ijamh.2004.16.4.303
  95. 95. Gotzsche PC, Hrobjartsson A, Maric K, Tendal B (2007) Data extraction errors in meta-analyses that use standardized mean differences. JAMA 298: 430–437. doi: 10.1001/jama.298.4.430
  96. 96. Cuijpers P, Smit F, Hollon SD, Andersson G (2010) Continuous and dichotomous outcomes in studies of psychotherapy for adult depression: a meta-analytic comparison. J Affect Disord 126: 349–357. doi: 10.1016/j.jad.2010.01.001
  97. 97. Hogan DR, Baltussen R, Hayashi C, Lauer JA, Salomon JA (2005) Cost effectiveness analysis of strategies to combat HIV/AIDS in developing countries. BMJ 331: 1431–1437. doi: 10.1136/bmj.38643.368692.68
  98. 98. UN Human Rights Council (2010) Report of the Special Rapporteur on the right to education, Addendum : Communications sent to and replies received from Governments,. 17 May 2010, A/HRC/14/25/Add.1, available at: http://www.unhcr.org/refworld/docid/4c29​b2342.html.
  99. 99. Antunes MC, Stall RD, Paiva V, Peres CA, Paul J, et al. (1997) Evaluating an AIDS sexual risk reduction program for young adults in public night schools in Sao Paulo, Brazil. AIDS 11 Suppl 1: S121–127.
  100. 100. Cai Y, Hong H, Shi R, Ye X, Xu G, et al. (2008) Long-term follow-up study on peer-led school-based HIV/AIDS prevention among youths in Shanghai. Int J STD AIDS 19: 848–850. doi: 10.1258/ijsa.2008.008129
  101. 101. Gallegos EC, Villarruel AM, Loveland-Cherry C, Ronis DL, Yan Zhou M (2008) [Intervention to reduce adolescents sexual risk behaviors: a randomized controlled trial]. Salud Publica Mex 50: 59–66. doi: 10.1590/s0036-36342008000100012
  102. 102. Rusakaniko S, Mbizvo MT, Kasule J, Gupta V, Kinoti SN, et al. (1997) Trends in reproductive health knowledge following a health education intervention among adolescents in Zimbabwe. Cent Afr J Med 43: 1–6. doi: 10.1016/s0277-9536(96)00204-3
  103. 103. Visser MJ (2005) Life skills training as HIV/AIDS preventive strategy in secondary schools: evaluation of a large-scale implementation process. SAHARA J 2: 203–216. doi: 10.1080/17290376.2005.9724843