In addition to the cohort evaluation, a formal test of knowledge and attitudes was carried out in July 2002 among all 4707 pupils who were in year 7 in the intervention and comparison schools. These were pupils in the year below the youngest group in the study cohort, and so were not cohort members. All pupils taking the test in the intervention schools had received all 3 years of the in-school intervention, which continued to be implemented after the trial period in the 10 intervention communities only. Tests were administered under examination conditions, supervised by a teacher from a different school.
Only urine specimens were collected at the baseline survey, and tested for HIV-1 antibodies using a semiquantitative particle agglutination test (GACPAT; Central Public Health Laboratory, Colindale, London, UK) . Reactive specimens were tested with Wellcozyme HIV1+2 GAC enzyme-linked immunosorbent assay (ELISA; Murex Biotech Ltd., Dartford, UK) , which provided the definitive result. Urine was also tested for Chlamydia trachomatis and Neisseria gonorrhoeae by polymerase chain reaction (PCR; Amplicor, Roche Diagnostics, Branchburg, New Jersey, USA). Samples were pooled for PCR, with a pool size of five, with samples from reactive pools then tested individually . Urine specimens from female participants were tested for pregnancy using an IPAS dipstick (Quickstick One Step HCG Pregnancy Test; IPAS/Pharmatech Inc., Denver, Colorado, USA).
At the final survey, serum and urine were collected from all participants and two self-administered vaginal swabs were collected by female subjects. Sera were tested for HIV-1 and HIV-2 using the Murex HIV Ag/Ab Combination ELISA (Murex Biotech). No specimen was reactive for HIV-2. Specimens reactive in the Murex HIV Ag/Ab ELISA were sent to the UK Central Public Health Laboratory for confirmation using a battery of antibody and antigen assays, including PCR when necessary. Full details of the HIV testing algorithm are given elsewhere . Fifteen positive baseline HIV results (based on urine testing) were reclassified as negative when serum testing at the final survey showed these participants to be HIV negative.
Sera were tested for antibodies to HSV2 using a monoclonal enzyme immunoassay (HSV2 IgG; Kalon Biological Ltd., Ash Vale, Surrey, UK) . Lifetime exposure to syphilis was examined using a Treponema pallidum particle agglutination (TPPA) test (Serodia TPPA; Fujirebio Inc., Tokyo, Japan). Urine from male subjects and vaginal swabs from female subjects were tested for C. trachomatis and N. gonorrhoeae using the same PCR methods as at baseline. Each vaginal swab was also tested for Trichomonas vaginalis using two independent sets of PCR primers [40–42]. A specimen was only defined as T. vaginalis positive if it was positive by both PCR assays. Urine specimens from female participants were tested for pregnancy using the same dipstick method as at baseline.
Based on previous survey data from the study communities , cumulative HIV sero-incidence over the 3 years of the trial was expected to be 1.6%. Assuming a between-community coefficient of variation for HIV incidence of 0.2 and 30% loss to follow-up, the sample size of 9645 would have given 75% power to detect a 50% reduction in HIV incidence in intervention communities if this had been the incidence rate within the trial.
Impact measures were based on ratios of prevalences, risks or rates in the intervention and comparison arms. For risks, the geometric mean risk for the 10 communities in each arm was computed, and the unadjusted risk ratio (RR) was calculated as the ratio of these geometric means. An approximate variance for the log(geometric mean) in each arm was obtained based on the residual mean square from a two-way analysis of variance (ANOVA) of community log-risk on stratum and study arm. A 95% confidence interval (CI) for the RR was calculated from this variance using a t-statistic with 14 degrees of freedom . Analogous methods were used for prevalences and rates.
Logistic or Poisson regression were used to adjust for individual-level covariates . The regression model included terms for risk stratum and predefined adjustment factors, but not study arm. For each community, the fitted model was used to compute the ratio of observed to expected events (O/E). The adjusted RR was obtained as the ratio of the geometric mean of these O/E estimates for the two study arms, and variances and CI were obtained from an ANOVA of log(O/E) on stratum and study arm.
For outcomes with zero cases in some communities, unadjusted and adjusted RR were obtained as the ratios of arithmetic mean risks and O/E, and approximate variances and CI were obtained from ANOVA of untransformed community risk or O/E on stratum and study arm.
Intervention impact was also analysed separately among those who were in years 4, 5 and 6 at baseline. The trend in adjusted RR with school year was assessed by regression of O/E on study arm and school year as a linear variable. A random effects model was used to allow for clustering by community. The statistical significance of the trend was obtained from the interaction between study arm and school year. A similar method was used to assess the interaction between study arm and marital status.
The analytical plan was approved by the trial's data and safety monitoring committee before the impact analysis commenced.
The trial protocol received ethical and research clearance from the Tanzanian National Medical Research Coordinating Committee and the Ethics Committee of the London School of Hygiene and Tropical Medicine. Primary school committees (which include parent representatives) gave written approval for schools to participate. Before each survey round, the study was explained to teachers and students, who were given a leaflet to take home to their parents that included notice of a meeting for parents and the right to inform the school if they did not want their child to take part. Signed informed consent was obtained from each student on the day of the survey round. At each round, cohort members could opt to receive their HIV test result after pretest and posttest counselling.
The results of the process evaluation are described elsewhere . Briefly, these showed that the intervention had been delivered to a high standard and with high coverage. For example, supervision visits to the schools showed that most teachers taught the sessions well, most class peer-educators ably performed brief dramas that were used as discussion starters, and a qualitative study confirmed that the teaching was well received by most pupils and communities . Over 80% of sessions had already been taught 2–3 months before the end of each school year during the trial . A simulated patient study found that health workers in intervention facilities were more respectful and empathic to youth than in comparison facilities . Over 57 500 condoms were sold by the youth condom promoters/distributors in the 2 years of this intervention component.
The baseline characteristics of the intervention and comparison groups were generally similar (Table 2). Slight baseline imbalances in ethnic group and lifetime number of partners were adjusted for in all analyses of trial outcomes. There were substantial differences between male and female participants, so outcomes were analysed separately by sex.
Completeness of follow-up
This is shown in Fig. 2. In summary, 7040 (73%) of the 9645 eligible cohort members were seen at the final survey. Follow-up rates were similar in intervention (72%) and comparison (74%) communities, higher among male (77%) than female (69%) participants (P < 0.001), and higher in younger participants (age at recruitment: 14 years, 74%; 15 years, 73%; 16+ years, 71%; P value for trend < 0.001).
Impact on knowledge and reported attitudes
At the final survey, there were substantial and statistically significant differences in the proportions of both male and female participants who answered all three questions ‘correctly’ for each of the three knowledge outcomes, and for the reported attitude outcome (Table 3, Fig. 3). The adjusted RR for these four outcomes ranged from 1.28 to 1.77 for male and from 1.41 to 1.58 in female participants. These results were independently confirmed by the results of a school examination administered to year 7 students in July 2002 (Table 4).
Impact on reported sexual behaviours
The proportion of young men reporting sexual debut during follow-up was 60% in the intervention and 72% in the comparison communities (adjusted RR 0.84, CI 0.71, 1.01). There was little difference among young women (adjusted RR 1.03, CI 0.91, 1.16; Table 3, Fig. 3). Similarly, the proportion of male subjects reporting more than one sexual partner in the past year was significantly lower in the intervention (19%) than in the comparison communities (28%; adjusted RR 0.69, CI 0.49, 0.95), but no significant difference was seen in female participants (adjusted RR 1.04, CI 0.58, 1.89).
The proportions who reported initiating condom use during follow-up were substantially and significantly higher in intervention communities among both male and female participants. The proportions reporting condom use at last sex were higher in intervention communities in both sexes, but this was only significant in young men, and absolute levels of condom use at last sex remained relatively low (< 30%; Table 3).
Impact on clinical symptoms and signs
At the final survey, the proportion of participants reporting genital pus or abnormal genital discharge during the past year was substantially lower in intervention communities, both among male (adjusted RR 0.58, CI 0.41, 0.83) and female (adjusted RR 0.59, CI 0.43, 0.80) participants. Among those reporting STI symptoms, however, there was no significant difference in the proportion who reported having sought care at a local health facility for their most recent STI episode during the past year, in either sex (Table 3).
Impact on HIV, sexually transmitted infections and pregnancy
The two primary outcomes of the trial, HIV incidence and HSV2 prevalence, were based on biological tests. Only 45 participants (five boys and 40 girls) seroconverted to HIV during 23 730 person-years of follow-up. After adjustment, HIV incidence in female subjects was 25% lower in the intervention communities, but this difference was not statistically significant (adjusted RR 0.75, CI 0.34, 1.66; Table 3). Overall, 12% of male and 21% of female participants were HSV2 seropositive at the final survey, but there was no difference by trial arm for either male (adjusted RR 0.92, CI 0.69, 1.22) or female (adjusted RR 1.05, CI 0.83, 1.32) participants (Table 3, Fig. 3).
Secondary biological outcomes included TPPA seroprevalence (syphilis), the prevalence of C. trachomatis and N. gonorrhoeae, and, in young women only, the prevalence of T. vaginalis and pregnancy, and the reported incidence of pregnancy during follow-up. There was no evidence of a protective effect of the intervention on any of these outcomes. In female participants, the prevalence of N. gonorrhoeae was higher in the intervention arm, and this difference was of borderline significance (Table 3). This difference was, however, only seen in those who were in year 6 at enrolment, who only had the potential to receive one year of in-school intervention (Table 5). A substantial proportion of young women were pregnant at the final survey (19%), and 46% reported having been pregnant for the first time during the 3-year follow-up period.
Trends by year of enrolment
In general, intervention/comparison differences in knowledge, reported attitudes and reported risk behaviours were greater among participants with more years of potential exposure to the in-school intervention, especially in young men (Table 5).
Impact by marital status
The impact of the intervention on pregnancy prevention knowledge was greater for those never married, among both female and male participants (P = 0.06 and P = 0.01, respectively), and there was some evidence of a greater impact on STI knowledge among never-married women (P = 0.07). The effect on HIV incidence was substantially greater in never married women (adjusted RR 0.40, CI 0.10–1.59) than ever-married women (adjusted RR 0.98, CI 0.47–2.03), although this was not statistically significant. There was no consistent difference by marital status for any of the behavioural or other biological outcomes (results not shown).
The study has confirmed that young people in this rural African population were at high risk of adolescent pregnancy and STI, with a low incidence of condom use and a high proportion of the cohort reporting sexual debut during 3 years of follow-up. There is, therefore, an urgent need for effective and affordable preventive interventions.
This trial has demonstrated the feasibility of large-scale implementation of an adolescent sexual health intervention using existing government staff and structures in sub-Saharan Africa. External evaluations of this multicomponent package of interventions showed that they were of high quality, well implemented and achieved high coverage. The average annual cost of the intervention was almost US$30 000 per trial community (approximately equivalent to an administrative ward, mean total population approximately 15 000) during the trial phase, including all start-up and capital costs, approximately equivalent to US$10 per adolescent per year within the primary target age range (12–19 years). Within a district-wide programme, first-year costs are projected to be US$22 000 per ward (US$7.30 per 12–19 year old), decreasing to US$3600 per ward (US$1.20 per 12–19 year old) in subsequent years .
Important limitations of the trial were that the interventions were deliberately constrained to be affordable and replicable on a large scale, and that the trial cohort included some young people who only received one or 2 years of the main, in-school component, rather than the full 3 years. The trial design also meant that mass media and other national or region-wide approaches could not be included. HIV incidence was much lower than predicted based on a previous survey of 15–19 year olds in the same communities . This may have been a result of the closed nature of the cohort, which excluded in-migrants, whereas those who were lost to follow-up may have been at higher risk than those followed up. Despite considerable efforts to trace cohort members who were absent during the follow-up rounds, 27% were lost to follow-up (Fig. 2). As follow-up rates were very similar in the intervention and comparison arms, it is unlikely that this would have biased the results.
The intervention led to substantial and statistically significant improvements in knowledge and reported sexual attitudes in both sexes. There was no evidence that the intervention increased sexual activity. On the contrary, young men reported delayed sexual debut and a reduction in the reported number of partners in the past year. Reported behavioural effects were stronger in male than female participants, possibly because young women were exposed to older male partners who had not benefited from the programme, or because young men understood the intervention messages better or were better able to act on them. For some outcomes, especially among male participants, the data suggested a dose–response effect with greater impact among those receiving 2 or 3 years of the in-school programme (Table 5). Previous studies have shown that youth interventions can improve knowledge and attitudes in the short-term (< 6 months) ; this study has shown a strong and sustained impact on knowledge and reported attitudes, especially in young men. Young people in the intervention communities were also less likely to report STI symptoms within the past year.
Despite these differences in knowledge, and reported attitudes and behaviours, there was no consistent impact on biological outcomes, including HIV incidence, the prevalence of other STI or pregnancy rates. There are several potential explanations for this discrepancy.
First, such interventions may only change knowledge and reported attitudes, but not actual risk taking, at least in the short term. Reported behaviour can be unreliable in young people , and may be subject to differential reporting bias in intervention and comparison arms. Therefore, observed differences in reported behaviour may have reflected a better knowledge of the promoted behaviours rather than changes in actual behaviour.
Second, it may be that the differences in reported sexual behaviour were valid, but the behavioural changes were not large enough to impact significantly on biological outcomes, at least within the follow-up period.
Third, young people may need longer exposure to such interventions. Overall, 42% of the cohort only had the potential to receive one year of the in-school intervention, and a further 32% could only have received 2 years. The tendency for greater beneficial impact on knowledge and reported attitudes among those who had the potential to receive 3 years of in-school intervention lends some support to this hypothesis.
Fourth, young men have considerably more decision-making power within sexual partnerships than young women . Our study cohort were on average several years older than the young women , and would not have benefited from the school-based intervention.
Fifth, those youth who leave school early or attend irregularly may be at disproportionately high risk, but would miss the in-school component of the intervention.
Finally, it may be that additional interventions are needed to make an impact within the short term. The interventions that were tested within this trial were all directly targeted to adolescents themselves. Cultural norms, however, such as gendered and age-related power relationships and marriage and fertility norms within the wider community, compromise the ability of adolescents to change their sexual behaviour . Community-wide interventions aimed at changing societal norms may be particularly important .
Accurate knowledge and skills are a prerequisite for young people who want to change their behaviour to reduce their risk of HIV and other sexual health problems. This trial has shown that it is possible for a large-scale intervention, implemented through local government workers and supervision structures, substantially to improve knowledge, reported attitudes, and reported behaviours. The effects on these outcomes were at least as great as those recorded in previous studies in Africa [15–17], and there was no evidence of increased risk-taking behaviour. Furthermore, these effects were present after a relatively long follow-up period (approximately 3 years) after the interventions were initiated.
It has often been assumed when interpreting the results of previous studies that improvements in self-reported sexual behaviours can be used as a proxy for reductions in true behaviour and hence reductions in HIV, other STI or pregnancy [9–12,15–17]. The lack of any consistent effect on the biological outcomes measured in our trial, despite substantial impacts on knowledge, reported attitudes and self-reported sexual behaviours, raises serious questions about the interpretation of previous studies, and argues strongly for the inclusion of biological outcomes in future programme evaluations.
This study was a collaboration between the Tanzanian National Institute for Medical Research (NIMR), the African Medical and Research Foundation (AMREF), the London School of Hygiene and Tropical Medicine (LSHTM), and the Ministries of Health and of Education and Culture of the Government of Tanzania.
The authors would like to thank the entire intervention, survey, data, laboratory, social science and administrative staff in Mwanza, and in particular Joseph Chilongani, Kenneth Chima, Robert Lugundu, Julius Mngara, Godwin Mmassy, Obed Mrita, Gerry Mshana, Zachayo Salamba, and Joyce Wamoyi. They also thank Aura Beltran, France Bernier, Tania Crucitti, Sandra Molina, Angels Natividad Sancho, Iain Tatt, and Rosanna Peeling, who either conducted or supervised additional laboratory analyses, Lilani Kumaranayake who supervised the costing study, and Sarah Henson, Eloise Turner and Onno Dekker, who provided administrative support to the study in Europe. The main authors apologize to the co-authors of this paper whose names are only listed in an appendix. This was due to the limits imposed by the journal editors.
The authors are grateful to the members of the study's Steering and Scientific Advisory Committees, which were co-chaired by the Director of Preventive Services in the Tanzanian Ministry of Health, and the Director of Basic Education in the Ministry of Education and Culture, and to the members of the Data and Safety Monitoring Committee: Peter Smith, Andrew Kitua, and Helen Weiss (before she became the trial statistician). They thank the Tanzanian Ministry of Health and Ministry of Education and Culture, National AIDS Control Programme, and Medical Research Co-ordinating Committee, and the Ethics Committee of the LSHTM, for permission to carry out and publish the results of this study. They are also grateful to the Regional Medical and Education Officers of Mwanza and the National Directors of NIMR and AMREF for their support.
This report is dedicated to the young people of Mwanza Region who participated in the study, and the teachers, health workers, and community members who implemented the interventions.
Sponsorship: The study was supported by grants from the European Commission, Development Cooperation Ireland (now Irish Aid), UK Medical Research Council, UNAIDS, and UK Department for International Development. The sponsors of the study had no role in the study design, data collection, analysis, interpretation, or writing of the report.
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Additional co-authors: Rebecca Baliraa, Daniel Wightb, Awene Gavyolec, Maende J. Makokhac, Frank Moshaa, Fern Terris-Prestholtd, John V. Parrye
aNational Institute for Medical Research, Mwanza Centre, Mwanza, Tanzania
bSocial and Public Health Sciences Unit, Medical Research Council, Glasgow, UK
cAfrican Medical and Research Foundation (AMREF), Mwanza, Tanzania
dLondon School of Hygiene and Tropical Medicine, London, UK
eSexually Transmitted and Blood Borne Virus Laboratory, Central Public Health Laboratory, Health Protection Agency, London, UK
Contributors: D.A. Ross was the project leader in Mwanza throughout, contributed to all aspects of the study, and took the lead in drafting the report. J. Changalucha co-supervised the laboratory testing, and contributed to the design and interpretation of the impact evaluation component of the study. A.I.N Obasi led the team that designed and implemented the interventions and contributed to the design of the impact evaluation. J. Todd was in charge of the data management and analysis from 1997 to 2000, and played a leading role in the design and implementation of the initial survey and baseline and interim follow-up survey rounds. M.L. Plummer led the team that conducted detailed qualitative social research that contributed to the design of the interventions and the interpretation of the findings, and played a leading role in the design and implementation of the final follow-up survey round. B. Cleophas-Mazige was directly responsible for the design and implementation of the health services component of the intervention, and led the intervention team during 2002. A. Anemona was in charge of the data management and analysis from 2000 to 2002. M. Makokha was actively involved in the implementation of the intervention from 2001 onwards, and played a major role in the design of the in-school component in 2001 and 2002. R. Balira played a major role in the data management for the trial. D. Everett co-supervised the laboratory testing of the interim and final follow-up survey rounds. H. Weiss took the lead in the analysis of the trial results. D. Wight contributed to the design of the intervention and interpretation of the trial results, and supervised the qualitative social research. F. Mosha was in charge of the field data collection teams throughout the trial. J. Parry was responsible for external quality control on the HIV testing, and for resolving the HIV status of problem sera from the final survey. F. Terris-Prestholt was responsible for the costing of the intervention. A. Gavyole was AMREF's Programme Coordinator for the Lake Zone of Tanzania throughout the trial, and advised on the design and implementation of the intervention and the interpretation and policy implications of the findings. D.C. Mabey contributed to the design of the trial and supervised the laboratory procedures. H. Grosskurth contributed to the design of the trial and the intervention, and advised on other aspects of the study. R.J. Hayes took the lead on the design of the trial and the interpretation of the results, and contributed to all other aspects of the study. All co-authors contributed to the writing of the report.
Keywords:© 2007 Lippincott Williams & Wilkins, Inc.
adolescents; HIV; pregnancy prevention; sexually transmitted infections; Tanzania