JAIDS Journal of Acquired Immune Deficiency Syndromes:
Epidemiology and Social Science
Two Distinct Epidemics: The Rise of HIV-1 and Decline of HIV-2 Infection Between 1990 and 2007 in Rural Guinea-Bissau
Tienen, Carla van MD*; van der Loeff, Maarten Schim MD, PhD*†; Zaman, Syed M A MBBS, MSc, PhD*‡; Vincent, Tim*; Sarge-Njie, Ramu FIBMS MSc*; Peterson, Ingrid PhD*; Leligdowicz, Aleksandra PhD*§; Jaye, Assan DVM, PhD*; Rowland-Jones, Sarah MB, ChB*§; Aaby, Peter DMSc¶; Whittle, Hilton MB, ChB, F Med Sci*
From the *Medical Research Council Laboratories, Fajara, The Gambia; †Municipal Health Service and Academic Medical Centre, Amsterdam, The Netherlands; ‡Health Protection Agency Centre for Infections, London, United Kingdom; §Weatherall Institute of Molecular Medicine, Human Immunology Unit, John Radcliffe Hospital, Oxford, United Kingdom; and ¶Projecto de Saúde de Bandim, Indepth Network, Bissau, Guinea-Bissau.
Received for publication May 8, 2009; accepted July 31, 2009.
Supported by the Medical Research Council.
There are no conflicts of interest.
A part of these results was presented at the 15th International Conference on AIDS and STIs in Africa (ICASA), 5 December 2008, Dakar, Senegal.
Reprints: Carla van Tienen, Medical Research Laboratories, PO Box 273, Atlantic Road, Fajara, The Gambia (e-mail: firstname.lastname@example.org or email@example.com).
Objectives: To assess changes in HIV incidence and prevalence in Caió, a rural area of Guinea-Bissau, between 1990 and 2007.
Design: Three cross-sectional community surveys.
Methods: In 1990, 1997, and 2007, surveys were conducted among adults. The prevalence of HIV-1 and of HIV-2 was estimated for each survey, and incidence rates were calculated for the first (1990-1997) and second period (1997-2007).
Results: The HIV-1 incidence was approximately 4.5/1000 person-years in the two periods, whereas the HIV-2 incidence decreased from 4.7 (95% confidence interval 3.6-6.2) in the first to 2.0 (95% confidence interval 1.4-3.0) per 1000 person-years in the second period (P < 0.001). HIV-1 prevalence rose from 0.5% in 1990 to 3.6% in 2007, and HIV-2 prevalence decreased from 8.3% in 1990 to 4.7% in 2007. HIV-1 prevalence was less than 2% in 15 to 24 year olds in all surveys and was highest (7.2%) in 2007 among 45 to 54 year olds. The HIV-2 prevalence was fivefold higher in older subjects (≥45 yr) compared with those less than 45 years in both sexes in 2007.
Conclusions: HIV-1 incidence is stable, and its prevalence is increasing, whereas HIV-2 incidence and prevalence are both declining. In contrast with what has been observed in other sub-Saharan countries, HIV-1 prevalence is lower in younger age groups than older age groups.
HIV-1 and HIV-2 are genetically similar1 but show a very distinct epidemiology. HIV-1 has spread globally, and more than 30 million people were estimated to be infected with HIV in 2007.2 In contrast, HIV-2 is confined to West Africa and countries with socio-economic links to Portugal.3 The relative containment of HIV-2 is probably related to lower sexual and vertical transmissibility compared with HIV-1.4,5 HIV-2 is associated with a slower rate of disease progression,6 but when people do develop AIDS, the disease manifestations and time to death are similar for both viruses.7-9 Lower levels of viremia play a key role in the reduced transmission and slower disease progression.10,11 Dual infection with HIV-1 and HIV-2 can occur, and the course of disease for HIV-dual infection usually follows that of HIV-1.12-14 One study suggested that HIV-2 infection might be protective against acquiring HIV-1,15 but other studies have been unable to confirm this.16-20
In Guinea-Bissau, HIV-2 has probably been present as early as the 1960s, and the highest prevalence by the late 1980s was 8% to 10% in the adult population, when HIV-1 was absent.21,22 Since the 1990s, most West African countries have reported a decrease in HIV-2 prevalence, whereas HIV-1 is increasing. Recent studies from the capital Bissau, a community survey of adults 23 and a cohort of police officers and pregnant women attending the public hospital,16,24 all show HIV-1 is surpassing HIV-2 as the predominant virus. No data exist on changes in the prevalence and incidence of these two viruses in rural areas of the country.
To assess the changes in the HIV-1 and HIV-2 epidemic in rural Guinea-Bissau, we conducted a cross-sectional survey in the adult community of Caió in 2006 to 2007. Two earlier surveys were performed in 1989 to 1991 and 1996 to 1998. Data from the three surveys were used here to assess the changes in prevalence and incidence of HIV-1 and HIV-2 over an 18-year period.
Study Population and Area
The study was conducted in the adult population (≥15 yr of age) of Caió, a rural area in northwestern Guinea-Bissau. The 10 zones of the village are situated among rice fields and cashew forests, which provide the main economic activity. The majority of the population is of the Manjako ethnicity, and animism is the main belief system. People travel frequently within Guinea-Bissau and to neighboring countries and to Europe (mainly Portugal and France). The reasons for traveling include visiting family members and attending school, funerals, work, and religious ceremonies.25
A demographic surveillance and community studies were started in 1988 to assess the clinical and epidemiologic impact of HIV-2 infection in a rural community. A cohort of HIV-positive cases and HIV-negative controls (matched by age, sex, and area of living) was initiated after the first survey in 1991. The current analysis comprises data from three cross-sectional community surveys among adults carried out in 1989 to 1991,22 1996 to 1998,17 and 2006 to 2007. The surveys will be referred to as 1990, 1997, and 2007 hereafter. People who were absent in the first survey were offered testing again during an additional round in 1992 (266 people tested).26 These data were not included in the prevalence estimates of 1990, but the subjects were included in incidence calculations.
Cohort members have free access to medication and medical care provided by the project's physician. Antiretroviral treatment became available in 2007, after completion of the 2007 survey.
2007 Survey Description
A survey of the adult population of Caió was performed between June 2006 and April 2007. Village meetings were held to discuss the study with the community before recruiting study participants. A local team of trained fieldworkers visited all eligible people at home. Efforts to trace subjects were no different for cohort members with a known HIV status than for other community members; subjects, irrespective of HIV status, were only included in the survey if found at home during the survey.
If informed consent was obtained, the participant was counseled, a short demographic and risk factor questionnaire administered, and a 2.5 mL venous blood sample drawn. The EDTA sample (Vacutainer, Becton Dickinson and Company, UK) was stored in a cool box before transportation to the project's laboratory in Caió. A malaria rapid test and hemoglobin measurement were performed, and treatment or referral to the project's physician was provided if necessary. Plasma samples were frozen and transported to Fajara, The Gambia, for serology testing. Syphilis results were returned to the participants at home, and people were invited to visit the project's counselor to obtain their HIV test result. This study was approved by the Gambia Government/MRC Laboratories Joint Ethics Committee and by the Ministry of Health of Guinea-Bissau.
HIV Laboratory Testing
Plasma samples were first screened for anti-HIV antibodies using the Murex ICE HIV-1.2.0 immunoassay (Murex Diagnostics, UK). Subsequently, HIV-1 or HIV-2 confirmation was obtained using the Hexagon HIV test (Human, Germany). Positive samples that showed a weak reaction or a dual reaction (HIV-1 and HIV-2) were subjected to a synthetic peptide-based assay (Pepti-Lav 1-2, Sanofi Diagnostics, France). Indeterminate results were resolved using HIV-1- and HIV-2-specific polymerase chain reaction (PCR) with nested primers targeted to the long terminal repeats.10 A similar algorithm was used in the 1997 survey.17 In the 1990 survey, the HIV diagnoses were determined by serology,22 and a subset of these samples was confirmed by PCR in a subsequent study.27
Data were double entered in an Access (Microsoft, Redmond, WA, USA) database, and the analysis was performed using Stata 9 (Stata Corporation, College Station, TX, USA). The prevalence ratio (PR) and 95% confidence intervals (CI) were calculated to assess changes in prevalence. Log binomial regression was used to adjust for sex and age of the overall PR. Binomial CIs were calculated for the prevalence. For the calculation of the incidence rates and age at infection, it was assumed that HIV infection occurred midway between the last seronegative and the first seropositive sample. Only subjects with samples in two consecutive surveys were included in the incidence analyses. To detect differences in incidence, incidence rate ratios (IRR) and 95% CI were calculated using Poisson regression. All analyses were performed separately for men and women. For calculation of overall ratios, Poisson regression was used to adjust for sex and age differences between surveys. Individuals who were positive for both HIV-1 and HIV-2 are described as HIV-dual positive and are included in all calculations unless stated otherwise.
Participation in 2007 Survey and Previous Surveys
In the 2007 survey, 2895 people participated of the 3907 adults who were registered in the census. This coverage of 74.1% was similar to previous surveys: 2770 of 3775 (73.4%) registered adults participated in 199022 and 3110 of 4127 (75.4%) registered adults participated in 1997. In all three surveys, more women participated than men because of the imbalance in the male-female ratio in the census registrations caused by men migrating out of the area.22,26 In 1997, 49% of nonparticipants were female compared with 61% of participants (P < 0.001); the median age of nonparticipants (30 yr) was lower than that of participants (33 yr) (P = 0.002). In 2007, 54% of nonparticipants were female compared with 60% of participants (P = 0.001), whereas the median age (31 yr) did not differ between the groups (P = 0.229). The main reason for nonparticipation in all surveys was short-term traveling (<6 mo). Refusal to give a blood sample was the second cause for nonparticipation, and this declined from 8.7% in 1997 to 5.0% (P < 0.001) in 2007 and was similar for both sexes.
HIV Prevalence in 2007
In 2007, 85 (2.9%) of 2895 individuals were HIV-1 positive, 115 (4.0%) were HIV-2 positive, and 20 (0.7%) were HIV-dual positive (Tables 1 and 2). Including HIV-dual infections, the overall HIV-1 prevalence was 3.6%, and the sex-specific prevalence was 3.1% in men and 4.0% in women (PR women vs. men 1.3, CI 0.9-1.9). The overall HIV-2 prevalence was 4.7% and was more than twofold higher in women than in men (6.1% vs. 2.6%, PR 2.3, CI 1.6-3.5).
Changes in HIV-1 Prevalence Between 1990 and 2007
Overall HIV-1 prevalence rose sharply from 1990 (0.5%) to 1997 (2.7%) (age- and sex-adjusted PR 5.7, CI 3.3-10.1) and rose moderately to 3.6% in 2007 (age- and sex-adjusted PR 1.3, CI 1.0-1.7) (Table 1, Figs. 1 and 2). In 1990, only 14 individuals were HIV-1 infected, and of these, 10 were HIV-dual positive. The total number of HIV-1 infected subjects (including HIV-dual positives) rose to 85 in 1997 and to 105 in 2007. HIV-1 prevalence was lowest (<2%) in the youngest age group (15-24 yr) for both sexes throughout the entire observation period. In 1997, the highest prevalence was in the age group 35 to 44 years for both men (5.6%) and women (6.1%). In 2007, the HIV-1 peak shifted to individuals aged 45 to 54, with HIV-1 prevalences of 7.1% in men and 7.2% in women. The increase in HIV-1 prevalence was significantly greater between 1990 and 1997 compared with that between 1997 and 2007 for both men (PR 5.6 vs. PR 1.4) and women (PR 5.4 vs. PR 1.3).
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.
1. Guyader M, Emerman M, Sonigo P, et al. Genome organization and transactivation of the human immunodeficiency virus type 2. Nature
3. Schim van der Loeff MF, Aaby P. Towards a better understanding of the epidemiology of HIV-2. AIDS
. 1999;13(Suppl A):S69-S84.
4. Kanki PJ, Travers KU, Mboup S. Slower heterosexual spread of HIV-2 than HIV-1. Lancet
5. O'Donovan D, Ariyoshi K, Milligan P, et al. Maternal plasma viral RNA levels determine marked differences in mother-to-child transmission rates of HIV-1 and HIV-2 in The Gambia. MRC/Gambia Government/University College London Medical School working group on mother-child transmission of HIV. AIDS
6. Marlink R, Kanki P, Thior I, et al. Reduced rate of disease development after HIV-2 infection as compared to HIV-1. Science
7. Ariyoshi K, Jaffar S, Alabi AS, et al. Plasma RNA viral load predicts the rate of CD4 T cell decline and death in HIV-2-infected patients in West Africa. AIDS
8. Whittle H, Egboga A, Todd J, et al. Clinical and laboratory predictors of survival in Gambian patients with symptomatic HIV-1 or HIV-2 infection. AIDS
9. Martinez-Steele E, Awasana AA, Corrah T, et al. Is HIV-2- induced AIDS different from HIV-1-associated AIDS? Data from a West African clinic. AIDS
10. Berry N, Ariyoshi K, Jaffar S, et al. Low peripheral blood viral HIV-2 RNA in individuals with high CD4 percentage differentiates HIV-2 from HIV-1 infection. J Hum Virol
11. Berry N, Jaffar S, Schim van der Loeff M, et al. Low level viremia and high CD4% predict normal survival in a cohort of HIV type-2-infected villagers. AIDS Res Hum Retroviruses
12. Alabi AS, Jaffar S, Ariyoshi K, et al. Plasma viral load, CD4 cell percentage, HLA and survival of HIV-1, HIV-2, and dually infected Gambian patients. AIDS
13. Kestens L, Brattegaard K, Adjorlolo G, et al. Immunological comparison of HIV-1-, HIV-2- and dually-reactive women delivering in Abidjan, Cote d'Ivoire. AIDS
14. Schim van der Loeff MF, Jaffar S, Aveika AA, et al. Mortality of HIV-1, HIV-2 and HIV-1/HIV-2 dually infected patients in a clinic-based cohort in The Gambia. AIDS
. 2002;16:1775- 1783.
15. Travers K, Mboup S, Marlink R, et al. Natural protection against HIV-1 infection provided by HIV-2. Science
16. Norrgren H, Andersson S, Biague AJ, et al. Trends and interaction of HIV-1 and HIV-2 in Guinea-Bissau, west Africa: no protection of HIV-2 against HIV-1 infection. AIDS
17. Schim van der Loeff MF, Aaby P, Aryioshi K, et al. HIV-2 does not protect against HIV-1 infection in a rural community in Guinea-Bissau. AIDS
18. Wiktor SZ, Nkengasong JN, Ekpini ER, et al. Lack of protection against HIV-1 infection among women with HIV-2 infection. AIDS
19. Aaby P, Poulsen AG, Larsen O, et al. Does HIV-2 protect against HIV-1 infection? AIDS
20. Ariyoshi K, Schim van der Loeff M, Sabally S, et al. Does HIV-2 infection provide cross-protection against HIV-1 infection? AIDS
21. Poulsen AG, Kvinesdal B, Aaby P, et al. Prevalence of and mortality from human immunodeficiency virus type 2 in Bissau, West Africa. Lancet
22. Wilkins A, Ricard D, Todd J, et al. The epidemiology of HIV infection in a rural area of Guinea-Bissau. AIDS
23. da Silva ZJ, Oliveira I, Andersen A, et al. Changes in prevalence and incidence of HIV-1, HIV-2 and dual infections in urban areas of Bissau, Guinea-Bissau: is HIV-2 disappearing? AIDS
24. Mansson F, Alves A, Silva ZJ, et al. Trends of HIV-1 and HIV-2 prevalence among pregnant women in Guinea-Bissau, West Africa: possible effect of the civil war 1998 1999. Sex Transm Infect
25. Buckner M. Village women as town prostitutes. In: Becker C, Dozon J-P, Obbo C, et al, eds. Vivre et Penser le Sida en Afrique
. Paris: Codesria, IRD, Karthala, 1999:389-404.
26. Aaby P, Ariyoshi K, Buckner M, et al. Age of wife as a major determinant of male-to-female transmission of HIV-2 infection: a community study from rural West Africa. AIDS
27. Ariyoshi K, Berry N, Wilkins A, et al. A community-based study of human immunodeficiency virus type 2 provirus load in rural village in West Africa. J Infect Dis
28. De Cock KM, Adjorlolo G, Ekpini E, et al. Epidemiology and transmission of HIV-2. Why there is no HIV-2 pandemic. JAMA
29. Djomand G, Greenberg AE, Sassan-Morokro M, et al. The epidemic of HIV/AIDS in Abidjan, Cote d'Ivoire: a review of data collected by Projet RETRO-CI from 1987 to 1993. J Acquir Immune Defic Syndr Hum Retrovirol
30. Larsen O, da Silva Z, Sandstrom A, et al. Declining HIV-2 prevalence and incidence among men in a community study from Guinea-Bissau. AIDS
31. Schim van der Loeff MF, Sarge-Njie R, Ceesay S, et al. Regional differences in HIV trends in The Gambia: results from sentinel surveillance among pregnant women. AIDS
32. Wilkins A, Oelman B, Pepin J, Trends in HIV-1 and HIV-2 infection in The Gambia. AIDS
33. Schim van der Loeff MF, Awasana AA, Sarge-Njie R, et al. Sixteen years of HIV surveillance in a West African research clinic reveals divergent epidemic trends of HIV-1 and HIV-2. Int J Epidemiol
34. Boerma JT, Ghys PD, Walker N. Estimates of HIV-1 prevalence from national population-based surveys as a new gold standard. Lancet
35. Buve A, Bishikwabo-Nsarhaza K, Mutangadura G. The spread and effect of HIV-1 infection in sub-Saharan Africa. Lancet
36. Buckner M. Manjako. In: Ember C, Ember M, eds. Encyclopedia of Sex and Gender: Men and Women in the World's Cultures
. New York: Kluwer Academic/Plenum, 2004:617-624.
37. Diop OM, Pison G, Diouf I, et al. Incidence of HIV-1 and HIV-2 infections in a rural community in southern Senegal. AIDS
38. Wawer MJ, Serwadda D, Gray RH, et al. Trends in HIV-1 prevalence may not reflect trends in incidence in mature epidemics: data from the Rakai population-based cohort, Uganda. AIDS
39. Mbulaiteye SM, Mahe C, Whitworth JA, et al. Declining HIV-1 incidence and associated prevalence over 10 years in a rural population in south-west Uganda: a cohort study. Lancet
40. Shafer LA, Biraro S, Nakiyingi-Miiro J, et al. HIV prevalence and incidence are no longer falling in southwest Uganda: evidence from a rural population cohort 1989-2005. AIDS
41. Mekonnen Y, Sanders E, Messele T, et al. Prevalence and incidence of, and risk factors for, HIV-1 infection among factory workers in Ethiopia, 1997-2001. J Health Popul Nutr
42. Kwesigabo G, Killewo J, Urassa W, et al. HIV-1 infection prevalence and incidence trends in areas of contrasting levels of infection in the Kagera region, Tanzania, 1987-2000. J Acquir Immune Defic Syndr
43. Holmgren B, Aaby P, Jensen H, et al. Increased prevalence of retrovirus infections among older women in Africa. Scand J Infect Dis
44. Morgan D, Whitworth J. The natural history of HIV-1 infection in Africa. Nat Med
45. Geskus R, Poulin N, Whittle H, et al. A Comparison of Progression of HIV-1 and HIV-2 Infection in The Gambia, Africa, Abstract 13_292. 13th International Workshop on HIV Observational Datababases, Lissabon, Portugal
46. Lagarde E, Schim van der Loeff M, Enel C, et al. Mobility and the spread of human immunodeficiency virus into rural areas of West Africa. Int J Epidemiol
HIV-1; HIV-2; Guinea-Bissau; rural population; incidence; prevalence
© 2010 Lippincott Williams & Wilkins, Inc.
What does "Remember me" mean?
By checking this box, you'll stay logged in until you logout. You'll get easier access to your articles, collections,
media, and all your other content, even if you close your browser or shut down your
To protect your most sensitive data and activities (like changing your password),
we'll ask you to re-enter your password when you access these services.
What if I'm on a computer that I share with others?
If you're using a public computer or you share this computer with others, we recommend
that you uncheck the "Remember me" box.
Highlight selected keywords in the article text.
Data is temporarily unavailable. Please try again soon.