In 2006, almost 4.5 million people worldwide became newly infected with HIV-1. Sub-Saharan Africa continues to be the region that bears the brunt of the global epidemic with 24.7 million out of the 39.5 million infected individuals worldwide .
The HIV epidemic continues to grow in all southern African countries but Zimbabwe . Meanwhile in East Africa the general trend is stabilization or reduction of the HIV prevalence. In West and Central Africa the observed trends are divergent. Using different sentinel populations, studies from Burkina Faso, Cote d'Ivoire , Ghana, Senegal  and Gambia  show signs of stabilization or reduction of HIV-1 prevalence, but in Mali the HIV epidemic appears to be growing .
In Guinea-Bissau, the country with the highest HIV-2 prevalence (8–10%) among adults in West Africa, HIV-1 was nonexistent in 1987 [5–7]. Two years later the first HIV-1/HIV-2 double infection was identified in a community cohort study carried out in Bissau, the capital of the country . Since then, the spread of HIV-1 has accelerated with a reported increase in prevalence from 1.1% in 1992  to 2.6% in 1996 [9,10] while HIV-2 prevalence was decreasing during the same period. In 2000, the HIV-1 prevalence among younger adults may have exceeded the prevalence of HIV-2 for the first time; the sentinel surveillance study among pregnant women in the capital found an HIV-1 prevalence of 3.6% and a HIV-2 prevalence of 3.3% .
In order to evaluate the trends in HIV prevalence and incidence in Guinea-Bissau, an urban population from Bissau has been followed by the Bandim Health Project with epidemiological survey studies since 1987 [5,6,9,12–15]. The present serosurvey is a continuation of these studies of retroviral infections including individuals from an open cohort of adults living in 384 randomly selected houses in the study area. Using data from the previous and the present survey we intended to examine the changes in the prevalence and incidence of HIV infections between 1987 and 2006.
The study was conducted in Bissau in an area included in the demographic surveillance system (DSS) of the Bandim Health Project (BHP), which was initiated in 1978. The BHP study area comprises five suburbs in the capital, and three of these have been followed with epidemiological studies of HIV infection since 1987. These three suburbs: Bandim 1, Bandim 2 and Belem have a total adult population of about 31 896 individuals according to a census performed in 2004. The cohort comprises individuals aged 15 years and older living in 384 randomly selected houses in the three districts mentioned above, that is a 10% sample of the houses in the three districts. The housing density has increased markedly since the initial survey and the number of houses enrolled in the study has therefore increased. In the original survey in 1987 a total of 100 houses were included, of these 92 were still inhabited in 2006. In 1996, 211 houses were added of which five had fallen down and one was uninhabited 10 years later. In the present survey from 2004 to 2006, 88 new houses were selected randomly among the houses constructed in the area after 1996 to maintain a 10% sample of the houses. One house fell down during the time that the study was carried out. Hence, of the 399 houses originally selected, 384 were followed.
We performed the survey between May 2004 and January 2007 covering all individuals aged 15 years and older living in the random sample of houses in Bandim 1, Bandim 2 and Belem.
In order to estimate HIV incidence rates between 1996 and 2006, individuals with a sample in both surveys were included in the incidence analyses if the first sample was negative. We also included people who had moved out of the randomized houses but had remained within the Bandim Health Project study area.
Before the initiation of the serosurvey, the implications and aims of the study were explained and discussed in community meetings. All individuals aged at least 15 years living in the randomly selected houses were visited. Information about the study was provided by one of three experienced field workers. As in previous surveys in this population in which a majority was illiterate, field workers obtained verbal consent from the individuals who agreed to participate in the study. An interview was carried out using a structured questionnaire focusing on demographic behavioral risk factors for HIV infection.
Before taking the blood sample, the field worker/counselor provided pretest counseling. A venous blood sample of 2.0 ml was collected in a microtainer evacuated blood collection system with additives (K2EK2EDTA – Greiner bio-one, USA). The participants were invited to return to the Bandim Health Centre 2 weeks later to obtain their HIV results. All subjects involved in the study were provided free access to medical consultations, essential drugs (including Cotrimoxazole prophylaxis if needed) and posttesting HIV counseling at the local health center by a physician associated with the project.
At the beginning of the study antiretroviral treatment (ART) was not available in the country. However, during the study the situation changed in Guinea-Bissau, and individuals from the cohort are now included in the national HIV care programme with the possibility to receive ART if needed.
In the present survey, blood samples were analyzed at the National Public Health Laboratory in Guinea-Bissau. Sera were screened using Enzygnost Anti-HIV 1/2 Plus (Behring Diagnostics Gmbh, Marburg, Germany) and reactive sera were confirmed with Capillus HIV-1/HIV-2 (Cambridge Diagnostics, Galway, Ireland) as well as Immunocomb II HIV-1&2 Bispot (Orgenics, Yavne, Israel) [16,17].
Data was entered in a dbase file and key variables were double entered. The analysis was carried out using STATA version 9. Age was categorized into five groups in the analyses (15–24, 25–34, 35–44, 45–54, 55 years and older). An age limit of below and above 45 years was also used as other studies from the area have shown a high risk of being HIV-2-infected among women over 45 years of age [14,15,18].
We calculated risk ratio (RR) and 95% confidence intervals (CI) to estimate the changes in HIV prevalence. Overall comparisons between 1996 and 2006 were adjusted for age and sex. No attempt to calculate confidence intervals from zero risk rates was made. Adjustments for sex and age were performed using binomial regression. When the analyses were adjusted or stratified by age and sex, incidence rate ratios (IRR) and their 95% CI were obtained through Poisson regression models.
Due to the cross-sectional nature of data collection the exact incidence rates could not be calculated. We assumed that seroconversions occurred midway between the 1996 and 2006 surveys, giving a mid-point risk time. Assuming minimal and maximal risk time led to only small changes in the results (data not shown).
Only individuals not infected with HIV-1 or HIV-2 in the previous survey were included in the HIV-1 and HIV-2 incidence analyses respectively.
We denote HIV-1 not including dual infections as single HIV-1, whereas HIV-1 infections including dual infections are denoted HIV-1. The same applies to HIV-2. Dual infections are denoted HIV 1+2.
The study was approved by the Guinea-Bissau Government Ethics Committee and the Danish Central Scientific Ethics Committee. All participants were counseled and provided informed verbal consent before HIV testing.
Participation in the 2006 survey and in previous surveys
Of the individuals registered in the 384 inhabited houses in the last census, 731 had moved, 144 had died and 13 could no longer be identified (Table 1). Among the remaining 3232 individuals eligible for inclusion in the study, 83% participated in an interview, 3.2% refused an HIV test and interview, 14% were either absent or traveling and 0.3% had an inconclusive HIV test result. Some of the interviewed individuals refused to supply a blood sample (n = 124). With a coverage of 79% in the serosurvey, participation was 6–7% lower than in the previous studies (86% in 1987 and 85% in 1996). Participation was clearly higher among women (85.2%) than among men (71.0%). The most important reason for nonparticipation was absence due to travel (5.4%) and work or school attendance at the time of the home visit (8.4%). This pattern of participation has also been observed in the past surveys [6,9]. The proportions of dropout, participation rates and reasons for nonparticipation in the two last studies are shown in Table 1. The increase in nonparticipation was strongest among men and was due to a slight increase in the proportion of individuals who refused HIV testing and a high increase in the proportion of individuals who were absent due to school, work and travel.
Among the 2548 providing results for HIV serology, the mean age was 31.6 years (SD, 12.9; range, 15–94 years) with no difference in men and women. The largest ethnic group was Papel (43.6%) followed by Mancanha (12.2%), Manjaco (11.2%), Balanta (9.7%), Fula (6.8%), Mandinga (2.9%) and others (13.6%).
Prevalence of HIV in 2006
In 2006, out of 2548 participants a total of 106 (4.2%) were single HIV-1-seropositive (Table 2); 100 (3.9%) were single HIV-2-seropositive (Table 3) and 12 (0.5%) tested positive for both viruses. With dual reactions included, the overall HIV-1 prevalence was 4.6% (118 out of 2548) and the HIV-2 prevalence was 4.4% (112 out of 2548).
The HIV prevalence was lower in men for both viruses, the female:male age-adjusted prevalence ratios being 1.45 (95% CI, 0.99–2.12) for HIV-1 and 2.00 (95% CI, 1.33–3.02) for HIV-2.
Changes in HIV prevalence from 1996 to 2006
We observed an increase in the overall prevalence of HIV-1 from 2.3% (54/2301) in 1996 to 4.6% (118/2548) in 2006 with an age and sex adjusted 2006/1996 prevalence ratio of 1.90 (Table 2). The single HIV-1 infection prevalence increased threefold, whereas the prevalence of dual infections, HIV 1+2, declined (prevalence ratio = 0.46; 95% CI, 0.23–0.93).
HIV-1 prevalence increased more for women than men over this 10-year time period. Adjusted for age the difference was not significant (test for interaction, P = 0.54). Among young adults aged 15–24 years the prevalence was low at 1.5% for men and 1.8% for women. In the older age groups, the largest increase was among women aged 25–34 years and among men aged 35–44 years. The prevalence was around 9% in these groups in 2006.
The HIV-2 prevalence decreased from 7.4% in 1996 to 4.4% in 2006 (Table 3). HIV-2 declined significantly below 45 years for both men and women. No decline was found for people older than 45, the prevalence ratio being 0.91 for men and 0.82 for women in this age group. Measured over the whole study period from 1987 to 2006, the prevalence ratio was 0.46 for men and 0.99 for women in this age group. The prevalence is therefore still very high for older women, 17.6%.
Our study design implied that some subjects were included in both surveys in 1996 and 2006. This could possibly distort the comparison of the prevalence in the two periods. Comparing only newly included subjects in 1996 and 2006 made only small changes to the results. Hence, little bias seemed to be created by including all subjects in the analyses.
HIV incidence in 1996 to 2006
In the 1987 survey there were no cases of HIV-1 infection . In the present study, 650 (278 men, 372 women) of the participants who were HIV-1-seronegative in 1996 survey were reexamined in 2006 contributing a total of 6058 person-years of observation (PYO). Thirty had become HIV-1-seropositive (8 men, 22 women), giving an overall incidence rate of HIV-1 infection of 0.50 per 100 person-years (Table 4). The incidence rate was lower in men than in women, the female/male incidence rate ratio (IRR) being 2.08.
The HIV-1 incidence rate was highest in the 25–34-year age group, followed by the 15–24-year age group. The HIV-1 incidence declined with age in the groups from 25–34 to 55+ years. The HIV-1 incidence was significantly higher in people below 45 years of age than people older than 45 years, the IRR being 0.29.
Six hundred and twelve (268 men, 344 women) of the participants who were HIV-2-seronegative in 1996 survey were reexamined in 2006. The follow-up time was 5770 person-years. Fourteen had become HIV-2-seropositive (3 men and 11 women), giving an overall incidence of HIV-2 infection of 0.24 per 100 person-years, being lower in men than in women (Table 4). The female-male IRR was 2.87. The IRR between the age groups 45+ and 15–44 was 1.16.
HIV 1+2 incidence
Six hundred and fifty four (279 men and 375 women) of the participants, who were negative for dual infection in the 1996 survey, were reexamined in 2006, contributing a total of 6222 person-years. Four female participants had become HIV 1+2-seropositive, giving an incidence of HIV 1+2 infections of 0.06 per 100 person-years. One participant was HIV-2-positive in the last survey and became HIV dual infected, and the other three participants were HIV-negative in the 1996 survey and seroconverted to both HIV-1 and HIV-2 infection in the 10-year period.
Changes in HIV incidence between two periods: 1987–1996 and 1996–2006
There was a nonsignificant increase in the incidence of HIV-1 between the first period (1987–1996) and the second period (1996–2006). The incidence was 0.34 per 100 PYO in the first period  and 0.50 per 100 PYO in the second period, the IRR for the two periods being 1.46 (95% CI, 0.78–2.76). For people less than 44 years old, the incidence of HIV-1 increased between the two periods being 0.37 per 100 PYO and 0.61 per 100 PYO respectively, the IRR being 1.65 (95% CI, 0.85–3.20). For people older than 45 the incidence rates were 0.22 and 0.18 respectively. For men the HIV-1 incidence rate decreased from 0.45 per 100 PYO in the first period to 0.31 per 100 PYO in the second period, with an IRR of 0.68 (95% CI, 0.26–1.82). For women the HIV-1 incidence rate increased from 0.25 per 100 PYO to 0.64 per 100 PYO, the IRR being 2.51 (95% CI, 1.02–6.19). The difference between men and women was borderline significant, P = 0.05. For women younger than 45 the incidence rate increased from 0.30 per 100 PYO to 0.76 per 100 PYO, the IRR being 2.58 (95% CI, 1.03–6.47).
There was a significant decline in the HIV-2 overall incidence from 0.53 per 100 PYO in the first period to 0.24 per 100 PYO in the second period, the IRR being 0.45 (95% CI, 0.23–0.90). For men, the HIV-2 incidence declined from 0.31 per 100 PYO to 0.12 per 100 PYO, the IRR being 0.39 (95% CI, 0.09–1.61). For the women, the HIV-2 incidence had the same pattern, decreasing from 0.71 per 100 PYO to 0.34 per 100 PYO, the IRR being 0.48 (95% CI, 0.22–1.04).
Studies of pregnant women form the predominant source of data on the HIV-1 prevalence in different African countries. However, they are less reliable for generating population-level estimates [19,20] due to the sex bias and the bias associated with studying only a fertile population . Therefore, community studies with extensive follow-up can offer a more accurate overview of the dynamics of the spread of the HIV infection in different strata and age groups in a population.
The Bandim Health Project carried out the first community study of HIV-2 covering the whole population. In the initial survey in 1987  children were included but the prevalence was so low that it was subsequently decided to restrict the study to adults. Over the years, we have tried to maintain the same methodology representatively covering around 10% of the houses in the study area. The number of houses included in the study has therefore been gradually enlarged. Although the participation rate in 2006 was slightly lower (78.6%) compared with the 1987 (86.0%)  and 1996 (85.0%)  serosurveys carried out in the Bandim study area, the patterns of participation were the same. As in previous studies, men were more likely to be absent at the time of the interview at home due to school or work attendance in all age groups. With improvement in transport traveling has become more common, and absence due to traveling was an important reason for nonparticipation. We tested whether the individuals who had been most difficult to reach had a higher prevalence of HIV. If so we might have underestimated the prevalence due to the lower participation rate. However, there was no indication of this being the case (data available on request). Hence, it seems unlikely that the lower participation rate has seriously affected our observations.
Our study  has documented the continuation of the trends we first observed in 1996, namely an increase in the HIV-1 prevalence and a constant decline in the prevalence of HIV-2 in Guinea-Bissau. The prevalence of HIV-1 has increased two-fold globally in the past 10 years and this augmentation occurred in all age groups and in both sexes. The 25–34-year age group was the most affected in women whereas in men the highest prevalence was observed in the age group 10 years older (35–44).
A similar pattern of increasing prevalence rates of HIV-1 and declining prevalence rates of HIV-2 were also reported in a cohort of police officers from Guinea-Bissau in 1997  and among pregnant women attending the National Hospital in Bissau between 1987 and 2004 . This trend has also been observed in Gambia  and other West African countries .
Currently in West Africa only Côte d'Ivoire has a national adult HIV prevalence that surpasses 4% (no distinction was made between HIV-1 and HIV-2) . In Nigeria about 4.4% of the women attending antenatal clinics nationally were found to be infected with HIV . Thus, Côte d'Ivoire, Nigeria and Mali are the countries with the most serious epidemic in West Africa as far as documented in studies. In contrast to neighboring countries (Senegal and Guinea-Conakry) with a low HIV-1 prevalence (<1 and 1.5% respectively) , Guinea-Bissau has a prevalence that may reach the levels of the other most affected countries in the sub-region. We have only data from the capital, but the HIV-1 prevalence was as high as 4.8% in women giving birth at the National Hospital  and 4.6% for both sexes in our urban cohort.
The present study also documented that the overall HIV-1 incidence increased from the 1987–1996 period to the 1996–2006 period but not significantly. The HIV-1 incidence rate as expected was higher in people younger than 35 years of age.
Generally there was more HIV infection among women. For both HIV-1 and HIV-2 the prevalence and incidence were higher in women, and HIV-1 prevalence increased more in women. Interestingly the HIV-1 incidence increased for women but declined for men. Between the two periods the HIV-1 incidence more than doubled for women. Higher HIV-1 seroprevalence and incidence in women than in men have previously been reported from others parts of Africa .
While HIV-1 infection has increased rapidly over the last decade, the HIV-2 infection has an opposite trend. The decline in the prevalence of HIV-2 that we noted in 1996  has continued. The overall HIV-2 prevalence among adults had declined from 8.9% in 1987  to 7.4% in 1996  and 4.4% in 2006. Initially this decline was only for men, now the prevalence is declining in both sexes. Regarding incidence, we observed that the HIV-2 incidence rate between 1996 and 2006 was half the incidence in the preceding 10-year period. Hence, the decrease in the HIV-2 risk was genuine and not only due to mortality or migration from a previously established cohort.
Nevertheless, it should be noted that the prevalence of HIV-2 is not declining among older people. This may indicate a cohort effect, previously infected young adults coming of age due to the longer survival of HIV-2 infected individuals. Furthermore, older women continue to become infected (Table 4). Hence, HIV-2 may continue as an independent infection among the oldest for some time, especially in women. An increased susceptibility to HIV and human T cell lymphotropic virus (HTLV) infections in older women, possibly due to changes in vaginal mucosal immunity, has previously been suggested to be the cause of this pattern [15,26,27].
The reasons why the HIV-2 is disappearing are probably complex and could be related to different factors. First of all, screening of blood donors for HIV-1 and HIV-2 was introduced in Bissau in March 1987, so the spread of HIV through blood transfusion was mainly prevented from that date. In the 1996 survey, transfusions were no longer a general risk factor for HIV-2 transmission . This change may have been very important for transmission of HIV-2 as around 20% of blood donors were infected when screening was initiated in 1987. Second, HIV-2 is probably not very effective as a sexually transmitted disease [28,29]. We have previously found that women married to an HIV-2-infected man only became infected after 45 years of age .
In conclusion, the HIV epidemic in Guinea-Bissau is still evolving and further studies are needed in order to monitor the trends. Understanding the behavioral patterns of older people and providing practical prevention guidelines based on national data will help the National HIV/AIDS Control Program to control the situation. Information, counseling and voluntary HIV testing programmes should be reinforced in all age groups in order to stop the further spread of HIV-1 epidemic in the country.
We are thankful to the laboratory technicians at the National Public Health Laboratory, field assistants and office staff at the Bandim DSS site for making this study possible. The study was supported by grants from the Danish International Development Agency (DANIDA)/ENRECA and Swedish Agency for Research Cooperation with Developing Countries (SAREC).
Contributions: The study was planned by Z. J. da Silva and P. Aaby and executed by Z. J. da Silva. A. Rodrigues and I. Oliveira were involved with supervision and interpretation of data. A. Andersen was responsible for the statistical analyses. B. Holmgren had carried out the previous cohort studies. S. Andersson and F. Dias have been responsible for the laboratory testing strategies. Z. J. da Silva wrote the first draft and all authors contributed to the final version of the paper.
There are no conflicts of interest.
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