IN THE BEGINNING OF the human immunodeficiency virus (HIV) epidemic in Africa, it was shown that HIV infection increased with increased level of education and socioeconomic position.1–9 High education and socioeconomic position were associated with increased opportunity for travel, disposable income, and ability to exchange money for sex. Infectious diseases have been linked with poverty and illiteracy. As the HIV epidemic evolves and becomes generalized, it was believed that the pattern of increased risk among educated individuals will change adopting the usual pattern of other infectious diseases.10 The negative correlation between education attainment and HIV-1 infection has been explained to be due to the role of education as a “social vaccine.”11,12 The education vaccine may work in 2 ways: exposure to acquired immune deficiency syndrome (AIDS) information and sex education in school and the role of basic education in equipping and empowering people to understand and internalize relevant information and translate knowledge into behavioral change. Education attainment also helps to change the community environment in which behavioral change becomes socially acceptable.12,13 Studies have shown that, even attending and completing primary education might have an effect in the spread of HIV-1 infection compared to not attending school at all. This is supported by findings from a number of studies that staying in school even if it did not advance literacy skills was helpful in impacting correctional behavioral outcomes.14
As was the case in most African studies, earlier studies in Tanzania showed an increased risk of HIV infection among educated individuals.2,6,7,15–17 This relationship was more significant in rural areas than in urban areas.15,16,18 Evidence is now mounting on the reversed association between education attainment and HIV-1 infection in Zambia, Ethiopia, and Uganda.5,11,19–24 Moreover, a review by Hargreaves and Glynn concluded that pattern of new HIV infections may be changing toward a greater burden among less educated groups.3 In Tanzania, hard data are lacking and recent studies have failed to show the reported reversed association.18 Local descriptions of the reversed association are important in redefining the package of current interventions and the group at risk.
We surveyed a rural population in Kilimanjaro Tanzania, in 1991; the beginning of the epidemic in this population, and again in 2005 when the epidemic was mature.25,26 Crude analyses have shown increasing HIV-1 prevalence in this rural population with less educated individuals at an increased risk.26 To investigate these dynamics further between 1991 and 2005, we compared prevalence rates across education level from the 2 surveys. To explain the observed changes in HIV prevalence over time, we described changes in risk sexual behaviors across education levels.
Materials and Methods
Study Area and Population
The data in this article comes from studies conducted in Oria, a rural village located 30 km south of Moshi town at the foot of Mount Kilimanjaro in Kilimanjaro region, Tanzania. Details of this study area have been described elsewhere.25,26 In brief, the village is located in Moshi rural district, 1 of the 6 districts in the region. Most of the villagers are peasant farmers, laborers, craftsmen, and some engage in seasonal work at the nearby rice plantations. The village has 2 primary schools and 1 secondary school that provide ordinary (4 years) secondary education.
Two cross-sectional surveys were conducted in the village in 1991 and 2005 (N = 1152 and 1528). The response rates achieved in these surveys were 76.4% (1152 of 1507) for 1991 and 73.0% (1528 of 2093) for 2005. The overall age and sex adjusted prevalence of HIV-1 infection was 3.2% and 5.9% in 1991 and 2005 survey, respectively (Mmbaga et al., unpublished data, 2007). Eligibility in all the surveys was based on having a residential address in the village and age between 15 and 44 years at the time of the study. All eligible individuals were registered by the research team and then invited to participate at all surveys. In the first survey in 1991, a temporary survey center was established in the village and those eligible were invited to participate. During the follow-up survey in 2005, the research team did house-to-house visits and conducted the interviews and sampling at the participants homes. Information on study aims and procedure was given to the participants before participation in both surveys, and those who agreed to participate provided an informed consent. A structured questionnaire was administered where sociodemographic data and behavioral risk factors for HIV-1 infection were collected. Data on education status was based on the Tanzanian system of education. In this system, individuals attend 7 years of primary education, 4 years of ordinary secondary education, and 2 years of advanced secondary education. After ordinary secondary education or advance secondary education, individuals qualify for college education. Although fees are required for other levels of education, primary education is free and compulsory for all Tanzanians. Failure to enroll an eligible child could lead into jail time for the parent or guardian. There is also a nationwide encouragement for parents to enroll their children for primary education. The interviews were then followed by a pretest counseling and venous blood collection for HIV-1 testing. Appointments were made with each participant for posttest counseling within 2 weeks from the date of sample collection. Test results were issued to respondents in person and those who were HIV-1 positive, were offered medical follow-up.
Both surveys were approved by the Ethical Committee of the Ministry of Health in Tanzania and the Norwegian Committee for Medical Research Ethics. The village government of Oria gave permission for the study. As mentioned above, participants gave their consent before participation. Free access to treatment of various medical conditions was provided by the research team during the survey period. The treatments were provided equally for participants, nonparticipants, and their families, and medical conditions treated were not a function of participation.
All blood samples in all surveys were tested for HIV-1 antibodies using a similar testing algorithm. Details of the blood testing strategies have been presented in detail elsewhere.26 In summary, HIV-1 antibodies were detected using 2 independent recombinant enzyme-linked immunosorbent assay systems. All discordant or doubtful sera were confirmed by Western blot (Organon, Epitope, Beaverton, OR). Quality control of the HIV-1 testing was done at the Centre for International Health, University of Bergen by retesting 11.2% of the sera in 1991 where excellent agreement was found with the testing performed at Kilimanjaro Christian Medical Centre.25
Data from the interviews and laboratory tests were checked for consistency, entered, and analyzed using Statistical Package for Social Scientists versions 13.0 (SPSS, Chicago, IL). Education levels were defined as <7 years primary education (no or <7 years of primary education), primary education completed (7 years of education), and secondary education or higher (>7 years of education). Only a small fraction of participants had postsecondary education [7 (0.6%) in 1991 and 15 (1.0%) in 2005]. These were, therefore, included in the last category of secondary education or higher. HIV-1 prevalence was computed using cross-sectional measures. The numerator was the number of adults with an HIV-1 seropositive status and the denominator was the total number of adult residents with a definitive HIV-1 serostatus at that particular survey. Comparison of HIV-1 prevalence by various sociodemographic characteristics between 1991 and 2005 was done where χ2 test for difference in proportion was used. For each survey, overall trends in HIV-1 prevalence across education level were computed and P values for trends in proportions are presented.
To follow the changes in the association between HIV-1 prevalence and education level between 1991 and 2005, crude odds ratios by education level were estimated. We subsequently presented adjusted odds ratios (AOR) for sex, marital status, and age as continuous variable. To be able to explain the changes in HIV-1 prevalence, we compared the sexual risk behaviors (condom use and number of sexual partners) by education level. These analyses were stratified by sex. All the reported confidence intervals (CIs) were at 95% level and the P values were 2-tailed.
The comparison of HIV-1 prevalence by sociodemographic characteristics between 1991 and 2005 surveys are depicted in Table 1. Significant increase in HIV-1 prevalence were observed among women, individuals aged 35 to 44 years, married/cohabiting, divorced/separated individuals, those with primary education (completed) or less, Chagga and other mixed tribes, farmers, and Catholics. The distribution of participants by education levels in 1991 were <7 years of primary 93 (8.1%), primary (completed) 985 (85.5%), and secondary or higher 74 (6.4%). The corresponding distribution for 2005 were 161 (10.5%), 1250 (81.8%), and 117 (7.7%), respectively (Table 1) (Mmbaga et al., unpublished data, 2007).
In the 1991 survey, the overall prevalence of HIV-1 infection by education level was <7 years of primary 1.2%, primary (completed) 3.2%, and secondary or above 5.3% (Ptrends <0.001). The corresponding prevalence's in the 2005 survey were 11.2%, 5.8%, and 5.7%, respectively (Ptrends 0.028). The sex specific patterns of HIV-1 prevalence by education level from 1991 to 2005 are illustrated in Figures 1 and 2. In 1991, HIV-1 prevalence increased with education both for women and men. In contrast to the above, a reversed pattern was observed in the 2005 survey (Figs. 1 and 2).
From the 1991 overall analyses, individuals with primary education (AOR, 2.7; 95% CI: 1.3–20.0) and secondary education or higher (AOR, 4.5; 95% CI: 1.4–24.9) were at increased risk of infection when compared with those with <7 years of primary education. These associations were reversed in 2005, where individuals with primary education (AOR, 0.5; 95% CI: 0.2–0.8) and those with secondary education or higher (AOR, 0.4; 95% CI: 0.3–0.9) had a reduced odds of infection when compared with those with <7 years primary education. The associations between education level and HIV-1 prevalence by sex in 1991 and 2005 are shown in Table 2. Although women with completed primary education had almost 3 times the likelihood of been infected with HIV infection, the corresponding likelihood of infection was 6 times among those with secondary education or higher. In the same year (1991), no men was infected in the <7 years primary education group, but HIV-1 prevalence was higher among those with higher education. In the 2005 survey, the data indicate that higher education level was associated with lower HIV-1 prevalence. Women who completed primary education and above had 30% to 50% less risk of HIV-1 infection compared with those with <7 years of primary education. The corresponding group of men had 60% to 70% reduced risk of infection (Table 2).
Associations between education level and HIV-1 risk sexual behaviors are depicted in Table 3. The likelihood of having ever used a condom increased with increased education level among women (AOR, 2.8; 95% CI: 1.1–7.3). Women with secondary education or higher also recorded a 70% decreased odds of reporting multiple sexual partners in the past year preceding the survey (AOR, 0.3; 95% CI: 0.1–0.7). This was in contrast to what was observed in 1991 where the increased likelihood of reporting ≥2 sexual partners among those with secondary education or higher in the past year was recorded (AOR, 2.1; 95% CI: 1.2–7.4). The relationship between education level and reported sexual risk behaviors was similarly reversed among educated men. When compared with noneducated men (<7 years primary education), educated men had almost 3 times higher odds (AOR, 2.7; 95% CI: 1.3–9.9) of reporting ≥2 sexual partners in the past month preceding the 1991 survey, this was reversed in 2005 where educated men had 60% lower risk of reporting ≥2 sexual partners when compared with noneducated men (Table 3).
This article reports a reversed association between HIV-1 infection and education attainment in rural Kilimanjaro, Tanzania. The overall change in the risk of HIV-1 infection from educated to noneducated individuals was observed between 1991 and 2005. The observed reversed association was highly significant among men. The risk of HIV-1 infection was reduced by 70% among men who attained secondary school or higher. This risk reduction among educated men in rural areas has recently been reported in Zambia24 and Ethiopia.23 As in the Zambian study, the modest decline in the risk of infection was also recorded among educated women. A decline in HIV-1 prevalence among educated women was also seen in this population. Despite large number of studies in Africa with information on education level and HIV-1 infection, the association between education attainment and HIV-1 infection itself has not been the focus of analysis in those studies.15,18,27 This has therefore shielded thorough assessment of the changing role of education in HIV-1 transmission in Africa. This is the first study in Tanzania to focus in its analysis and show in hard data a reversed association between education attainment and HIV-1 infection.
The patterns of behavioral change corroborated the findings of reversed association between education attainment and HIV-1 prevalence in this population. Decreased prevalence of HIV-1 infection among educated individuals was associated with increased practice of safer sexual behaviors. Educated women were 3 times more likely to report ever use of condom in 2005 than noneducated women. With the increased condom use, educated women also had 70% decreased odds of reporting ≥2 sexual partners in the past year. These findings are of paramount importance as education seems to empower women, promote self-efficacy, and increase their negotiating power during sexual acts.28,29 In rural sub-Saharan Africa, traditional normative behaviors such as dominance against women and men having concurrent partners are socially acceptable. The empowering role of education is an important tool for women who want to change their behaviors in ways that may conflict with this traditional norms and customs. A change toward safer sex among educated men was also observed. When compared with the noneducated, educated men had 60% decreased odds of reporting ≥2 sexual partners in the past month preceding the 2005 survey. This is the reverse of what was observed in 1991. Adoption of safer sex among educated men is encouraging because studies have shown that marriage occurs predominately between people of the same socioeconomic status and that a woman's risk of infection is associated with the husband's behavior and education level.1 All these findings of positive behavioral change associated with decreased HIV-1 infection among educated individuals have been reported in other studies in Africa.19,21,22,24,28–30 The association between these behaviors and HIV-1 infection in this population have been presented elsewhere.26 All these behaviors were associated with HIV-1 transmission in this population hence change in these behaviors as observed among educated individuals may have a positive impact in reducing HIV-1 transmission.
The positive response of educated individuals to preventive messages could explain the current observation on reversed association between education attainment and HIV infection. Both AIDS-specific and basic education play an equally important role in behavioral change that reduces the risk of HIV infection. Staying in school is also associated with increased likelihood of exposure to health education including knowledge on HIV/AIDS and other sexually transmitted infection prevention.10,12,31–33 When AIDS-specific health education diffuses into the community, educated individuals are more likely to process, understand, adapt quickly, and act on health promotion messages.5,12,13,31 This may lead to behavioral change faster than among illiterate people in terms of delaying first sexual encounter and marriage, reducing number of sexual partners and negotiating, accepting and increasing condom use.32,34 This could thus mean that through adoption of safer sexual behaviors, educational attainment acts both in reducing the risk and vulnerability to HIV infection.
HIV/AIDS education was not provided in Tanzanian public schools until recently. However, an in-school health education campaign called “Afya kwa vijana” (“Health for youth” in Swahili the national language used in Tanzania and most of east Africa) was introduced in the study area involving grade 6 and 7 pupils in late 1990s until 2005.33 The program goal was to reduce students' risk of HIV infection by delaying initiation of sexual activity. The programs focused on increasing HIV/AIDS transmission knowledge, skills on condom use, improve perceived susceptibility, and foster communication on HIV/AIDS. This program was implemented in the area until 2005. Individuals who attended primary school up to at least grade 6, had the opportunity to be exposed to the program and this might explain the observed positive behavioral change among the educated group. In our study no significant increase in HIV-1 prevalence was noted among young age groups (15–34 years). This could be because this younger group who went to school more recently when compared with the older group (35–44 years) may have benefited from the HIV/AIDS education campaigns hence adopting safer sexual behaviors (Mmbaga et al., unpublished data, 2007).26 Reproductive health education was recently introduced to all Tanzanian public primary and secondary education curriculums, meaning that all schools are now offering skills vital in mitigating the spread of HIV infection.
In Africa, majority of the population live in rural areas (78% in the case of Tanzania) where the level of education is known to be low compared with urban population. Although primary education is still free in Tanzania, the rates of school enrolment are still low in rural areas because of poor motivation, and follow-up to ensure adequate enrolment. In this article, we have demonstrated that even attending 7 years of primary education could have an important impact on HIV-1 risk. These findings should encourage more involvement of parents and all education stakeholders in the fight against the epidemic by promoting increased educational attainment to the younger generation with vigorous follow-up and legal action for those failing to enroll their children. These measures may not only save their lives but open more doors for economical development.
The results of this article may be affected by a number of biases. First, change in population structure over time might have affected comparability between the 2 cross-sectional studies. Moreover, we only achieved a response rate of about 75% in both studies. Although this response rate is acceptable, selection bias because of the 25% nonrespondents could have biased our findings. Second, we have assessed only the level of education in this study but the quality of the education received was not possible to assess. Finally, it is possible that education attainment may influence reported behavior rather than actual behavior. Despite this, the observed decrease in HIV-1 prevalence (a biologic marker out of participant's control) among educated individuals suggests that the reported decrease in risk behavior might reflect the actual behavior.
In conclusion, although HIV-1 infection increased in rural Kilimanjaro, the risk of infection seems to have shifted from educated to noneducated individuals. Reversed association between education attainment and HIV-1 infection was observed between 1991 and 2005. This reversed risk was corroborated by an increase in reported practice of safer sexual behaviors among educated individuals. Educated individuals might have benefited most from health education campaigns. Increased condom use among educated women suggests that education could be an important tool to empower women and increase their negotiating power. The role of the education sector in the fight against HIV/AIDS should be emphasized, as the more educated society is more responsive to health information.
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