Changes in HIV-2 Prevalence Between 1990 and 2007
Overall HIV-2 prevalence remained stable between 1990 (8.3%) and 1997 (7.9%) (age- and sex-adjusted PR 1.0, CI 0.9-1.2) and then declined to 4.7% in 2007 (age- and sex-adjusted PR 0.6, CI 0.5-0.8) (Table 1, Figs. 1 and 2). For both sexes, the HIV-2 prevalence was higher in the older age groups (>44 yr) than in the younger age groups (<45 years) during all three surveys. The difference in HIV prevalence between younger and older subjects increased over time, and in 2007, the HIV-2 prevalence was five times higher in older people (10.6%) than in younger people (2.0%). In men, HIV-2 prevalence peaked at 19.1% in 45 to 54 year olds in 1990 and at 17.5% in 35 to 44 year olds in 1997. In 2007, the HIV-2 prevalence peaked at 7.2% among men in the oldest age group (>54 years). In women, the HIV-2 prevalence peaked at 17.2% in 35 to 44 years in 1990 and shifted to the oldest age group (>54) at 16.3% in 1997 and remained high at 14.9% in 2007 among the oldest age group.
HIV Incidence Between 1990 and 2007
Participation in Two Subsequent Surveys
A total of 2915 people participated in the 1990 survey and the additional study in 1992, of whom 1629 (55.9%) people also participated in 1997. Reasons for not providing a second blood sample (n = 1286) were: 336 had died (26.1%), 562 had moved away (43.7%), 206 were short-term absent (16.0%), 134 refused (10.4%), 42 subjects had missing data (3.3%), 3 had insufficient sample (0.2%) and 3 subjects could not be re-identified (0.2%). Among the people who were not followed up versus people who were followed up, the percentage of women was lower (58% vs. 67%, P < 0.001); the median age was similar (35 vs. 37, P = 0.51, rank sum test); more people were HIV-1 infected (0.8% vs. 0.2%, P = 0.039); and more people were HIV-2 infected (9.5% vs. 7.1%, P = 0.025).
In 1997, 3110 persons participated in the survey, and 1360 (43.7%) of them provided a second blood sample in 2007. Reasons for not providing a second blood sample (n = 1750) were: 525 had died (30.0%), 731 had moved away (41.8%), 375 were short-term absent (21.4%), 86 refused (4.9%), 29 subjects could not be re-identified (1.7%), and 4 subjects had missing data (0.2%). Among the people who were not followed up, the percentage of women was lower (58% vs. 66%, P < 0.001); the median age was the same (33 yr, P = 0.29, rank sum test); more people were HIV-1 infected (4.1% vs. 1.0%, P < 0.001); and more people were HIV-2 infected (10.2 vs. 5.0%, P < 0.001).
In the first period (1990-1997), 534 men and 1091 women were HIV-1 negative at the start and provided a blood sample in 1997 (Table 3). Together, they contributed a total of 11,470 person-years of observation (PYO). Fifty-one subjects became newly infected with HIV-1, giving an overall incidence rate of 4.4 per 1000 PYO (CI 3.4-5.9).
In the second period (1997-2007), 465 men and 882 women were HIV-1 negative at start and provided a blood sample in 2007. They contributed a total of 12,311 PYO. Forty-nine people became newly infected with HIV-1, giving an overall incidence rate of 4.0 per 1000 PYO (CI 3.0-5.3). There were no significant differences in the incidence rates comparing men and women and comparing older and younger individuals within the two periods. The median age at HIV-1 infection was 37 (interquartile [IQ] range 32-44) years in the first period and remained very similar at 38 (IQ range 29-49) years in the second period.
In the first period, 498 men and 1,015 women were HIV-2 negative in 1990 and provided a sample again in 1997 (Table 3). They contributed a total of 10,653 PYO. Fifty-one people became newly infected with HIV-2, and the overall incidence rate was 4.8 per 1000 PYO (CI 3.7-6.4). The incidence rates among men and women and among younger and older individuals were not statistically significant (IRR men/women 0.7, CI 0.4-1.3; older/younger IRR 0.6, CI 0.3-1.1).
In the second period, 446 men and 843 women were HIV-2 negative at the start and provided a second blood sample, contributing to a total of 11,934 PYO. The overall incidence rate decreased to 1.8 per 1000 PYO (CI 1.2-2.7) (IRR 0.4, CI 0.2-0.6). The largest decrease was observed in men (IRR 0.1, CI 0.0-0.6), and women were more likely to get infected (men/women IRR 0.2, CI 0.1-0.8). Although the HIV-2 incidence rate decreased significantly overall, there was a contrast between the younger age group (a significant decrease from 5.7 to 1.0 per 1,000 PYO; P < 0.0001) and the older age group (a nonsignificant increase from 3.3 to 3.6 per 1,000 PYO; P = 0.79). This shift of incidence by age was also reflected in the increase of the median age at infection, which was 32 (IQ range 24-44) years in the first period and 52 (IQ range 41-59) years in the second.
To our knowledge, this is the largest community-based study monitoring changes in incidence and prevalence of both HIV-1 and HIV-2. We have shown a stable HIV-1 incidence and a decline in the HIV-2 incidence over an 18-year period in the adult population of a rural community in Guinea-Bissau. The HIV-1 prevalence increased and the HIV-2 prevalence decreased. Overall, women were more at risk of HIV infections, and older women showed a stable HIV-2 incidence. In 2007, HIV-1 was most prevalent in people aged 45 to 54 and HIV-2 in people older than 54 years.
The distinct patterns of rising HIV-1 and declining HIV-2 prevalence that were observed here have also been reported in Bissau in a cohort of police officers,16 pregnant women,24 and household surveys23 and in other West African countries.16,23,24,28-33 HIV-1 was probably introduced later into Guinea-Bissau than HIV-2 because HIV-1 was absent in the capital in 1987 and very low in the community from the current study in 1990, whereas HIV-2 prevalence was high (8%-10%) in both areas at that time.21,22 The local HIV-1 epidemic appears to be younger, with a prevalence that strongly increased mainly in the period 1990 to 1997. The 3.6% HIV-1 prevalence in our study was somewhat lower than that observed in the general adult population (4.6% in 2006)23 and in pregnant women (4.2% in 2004)24 in urban Bissau. Urban areas usually have a higher HIV-1 prevalence than rural areas,3 and community surveys are more likely to give true estimates in comparison with surveys performed in antenatal clinics, which may overestimate prevalence.34
HIV-1 prevalence was high compared with most countries in the subregion with stable prevalences below 2%.2 However, HIV-1 prevalence has not increased to levels observed in East and Southern Africa,2 nor did it reach the high level of the earlier HIV-2 prevalence in Guinea-Bissau. Intriguingly, in our study, HIV-1 incidence and prevalence were low in the youngest age group (15-24 yr), and the highest prevalence was found among 45 to 54 year old men and women. This is in contrast with nearly all other sub-Saharan studies, which almost invariably find the highest rates of infection among young people.35 A low prevalence in the youngest age groups was also observed in Bissau, with a prevalence among 15 to 24 year olds of 1.5% in men and 1.8% in women in 2006.23 Public health interventions by an NGO from 2002 to 2006, including free distribution of condoms and the surveys performed in the village, might have increased awareness of HIV, which could have led to diminishing risk behavior. By Manjako tradition, all adolescents in Caió are initiated into an age set every 4 years, which is completed around the age of 20. In this period, sexual relationships are strongly discouraged and may happen only within the same age set, and teenage pregnancies are rare.36 Closed sexual networks in younger individuals may therefore have contributed to the low prevalence and incidence of HIV among young people. Furthermore, most women in Caió who work as prostitutes are relatively old (>40 yr), and this might thus influence the higher prevalence in older subjects.25
Few community studies from West-Africa have measured HIV-1 incidence. The incidence of 4.0/1,000 PYO from our study is slightly lower than in Bissau (5.0/1,000 PYO)23 but high compared with a rural area just across the border in neighboring Senegal (0.8/1,000 PYO).37 Community and occupational cohort studies from other sub-Saharan countries report incidence rates between 2.5 and 48/1,000 PYO,38-42 where incidence generally peaks in younger age groups.
Possible factors for the decline of HIV-2 are the low infectivity of HIV-2, with sexual and vertical transmission rates that are much lower than in HIV-1.4,5 Having received a blood transfusion was a risk factor for HIV-2 infection in 1990 in Caió, but only 2% of participants in that study had ever had a blood transfusion.22 Therefore, it appears unlikely that the screening of blood since 1987 has had an important impact on the epidemic in Caió. Bissau and other West African countries also show declining or stable HIV-2 prevalence.16,23,24,28-33 The observed decrease in HIV-2 prevalence is compatible with the decreased HIV-2 incidence and mortality caused by old age.
In a community survey in Bissau, the incidence went down from 5.430 to 2.4/1,000 PYO23 over the same time period as our study. HIV-2 continues to infect older women, which has been observed in previous studies and might be explained by cumulative exposure or an increased susceptibility to retroviral infections in older women (reviewed in Holmgren et al43).
Limitations of Study
The time between the surveys was long (median 7.3 yr for the first period and 9.4 yr for the second), and many people were not followed up, mainly because of the highly migratory nature of the population. It is possible that newly infected individuals may have died before the survey could have detected them. However, if the median survival time of HIV-1 is similar in our population to the observed median of 10 years in Ugandan community-based cohort studies,44 this would have had a limited impact. Median survival in HIV-2 infection is not known, but it is estimated that more than 50% of infected individuals do not progress to disease.45 Individuals who were absent during the surveys may have represented a group with a higher prevalence of HIV infection,46 which would have lead to an underestimate of the incidence rates and prevalences reported here. Although this possibility cannot be excluded, an argument against this bias is the lower prevalence observed in absent individuals from the first survey who were revisited after a year.26 Differential refusal among HIV positive and negative subjects might have lead to a selection bias as well. To further explore this bias, we looked at HIV status among individuals who refused a second blood sample. They had similar or lower HIV prevalences compared with the people who did give a second sample, so this bias is probably limited (data not shown).
HIV-1 prevalence has increased with a stable incidence, whereas HIV-2 prevalence and incidence have decreased; HIV-2 is now mainly an infection of elderly women. The incidence data should be interpreted with caution because the long intervals between the surveys may have influenced the estimates. This is the only area in sub-Saharan Africa reported so far where HIV-1 prevalence is not peaking in the young adult age groups. This phenomenon is unexplained but requires further investigation. Final conclusions about the reasons for the observed patterns of HIV-1 and HIV-2 distribution cannot be drawn, and risk factor analysis could help explain these findings. Public health interventions need to continue to prevent further spreading of HIV and must address all age strata. Further immunologic and virologic studies could contribute to a better understanding of the sustained HIV-2 infection among older women. Further epidemiologic surveillance is needed to monitor the dynamics of both epidemics in the future.
The authors are grateful to the Caió population for their participation in all the studies. They are thankful for the support of the Caió field workers, the project's personnel, and the Fajara laboratory technicians and Clayton Onyango for his PCR work. They are grateful to Roel Coutinho and Matthew Cotten for commenting on the article. Contributions: The study was planned by S. Rowland-Jones. A. Jaye, and S. M. A. Zaman and executed by C. van Tienen with the help of A. Leligdowicz. M. Schim van der Loeff carried out the 1997 survey and helped with analysis and interpretation of the data. T. Vincent was responsible for coordinating the Caió project and supervising the field work and data entry for the surveys. I. Peterson helped with the statistical analyses and interpretation of the results. R. Sarge-Njie was responsible for the laboratory testing and interpretation of the laboratory results. H. Whittle was involved in the planning of the three surveys. H. Whittle and P. Aaby were involved with supervision of the surveys and the analysis and interpretation of the data. The late A. Wilkins initiated the first studies in Caió. All authors saw and approved the final version of the manuscript.
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Keywords:© 2010 Lippincott Williams & Wilkins, Inc.
HIV-1; HIV-2; Guinea-Bissau; rural population; incidence; prevalence