1 Institut National de la Santé et de la Recherche Médicale, U88-IFR69, Saint-Maurice, France.
2 Medical Research Council Laboratories, Fajara, The Gambia.
3 Institut National dEtude Démographique, Paris, France.
4 Programme de recherche sur le SIDA de lInstitut de Recherche et Développement, Montpellier, France.
5 Laboratoire Population-Environnement-Developpment UME 151 IRD-Université de Provence, Marseille, France.
6 Laboratoire de virologie-bactériologie de lhôpital Le Dantec, Dakar, Sénégal.
7 Comité National de Lutte contre le SIDA, Dakar, Sénégal.
8 Projecto de Saúde de Bandim, Bissan, Guinea-Bissau and Danish Epidemiology Science Centre, Statens Serum Institut, Copenhagen, Denmark.
9 Members of the MECORA group (Etude Multisite des Comportements et MST en zone Rurale dAfrique) are listed at the end of the paper.
Emmanuel Lagarde, INSERM U88, 14 rue du Val dOsne, Hôpital National de Saint Maurice, 94410 SAINT MAURICE, France. E-mail: emmanuel.lagarde{at}st-maurice.inserm.fr
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Abstract |
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Method A comparative cross-sectional study using a standardized questionnaire and biological tests was conducted among samples in two rural communities of Senegal (Niakhar and Bandafassi, 866 and 952 adults, respectively) and a rural community of Guinea-Bissau (Caio, 1416 adults). We compared the distribution of population characteristics and analysed risk factors for HIV infection in Caio at the individual level.
Results The level of HIV infection was very low in Niakhar (0.3%) and Bandafassi (0.0%), but 10.5% of the adults in Caio were infected, mostly with HIV type 2 (HIV-2). Mobility was very prevalent in all sites. Short-term mobility was found to be a risk factor for HIV infection among men in Caio (adjusted odds ratio (aOR) = 2.06; 95% CI: 1.063.99). Women from Caio who reported casual sex in a city during the past 12 months were much more likely to be infected with HIV (aOR = 5.61 95% CI: 1.5620.15). Short-term mobility was associated with risk behaviours at all sites.
Conclusions Mobility appears to be a key factor for HIV spread in rural areas of West Africa, because population movement enables the virus to disseminate and also because of the particularly risky behaviours of those who are mobile. More prevention efforts should be directed at migrants from rural areas who travel to cities with substantial levels of HIV infection.
Accepted 31 January 2003
Sub-Saharan Africa is the region of the world hardest hit by HIV infection: 70% of all those with human immunodeficiency virus (HIV)/AIDS worldwide live there.1 The pandemic is not distributed homogeneously, however. In countries such as Zambia, Zimbabwe or Namibia, more than 25% of adults are infected, while in countries such as Senegal or Gambia, the prevalence does not exceed 2%.2 The heterogeneity of the spread of HIV is also found within countries, and infection rates are usually higher in urban than rural areas. Moreover, HIV infections in rural areas most often come from urban sources, and migration has often been found to be one of their principal risk factors in studies of rural populations.36 Mobility and migration enable the virus to shift from urban centres to the countryside, and populations living in interfaces such as trading centres7,8 or main roads9,10 are infected at higher rates than those living in isolated villages. Round trips between villages and cities are not per se a vector for HIV: the key issue is the behaviours of migrants and travellers. Previous studies in Africa found that migrants have more risk behaviours than non-migrants.5,11,12 Two non-exclusive explanations seem likely. Firstly, travelling exposes migrants to new behaviours. Previous observations showed that risk behaviours are more frequent in towns than in nearby rural areas.13,14 Secondly, migration disrupts traditional social constraints on and control of sexual behaviour. Married people often travel without their spouse and thereby increase their risk of extramarital sex. It can sometimes be very difficult for migrants to find a sex partner among local inhabitants of the area into which they have moved. This can lead them to have sex with commercial sex workers, who have much higher rates of HIV infection than the general adult population.
Finally, it is possible that changes in sexual behaviours, for example following marriage disruption, may lead to changes in mobility behaviours and could partly explain the association observed between sexual behaviours and mobility. This has not yet been documented, however.
A recent study in Uganda15 found that migrants reported higher levels of sexual risk-taking behaviours but also higher rates of condom acceptance than among non-migrants. Travellers are more likely to report condom use according to a study in Tanzania13 and to our study in southern Senegal.11 This opens the way for specific prevention among mobile populations.
To identify the key determinants of HIV infection in rural West Africa, we conducted standardized comparative surveys in three rural settings with highly mobile populations and levels of HIV infection that we expected to be heterogeneous. Two of these areas are located in regions where nearby cities have very low HIV infection levels and the third is located in a region where the nearby cities have relatively high HIV levels.16
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Methods |
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Niakhar
The survey was conducted in July 1997 in the region of Fatick, in central Senegal. The population of the area has been under demographic follow-up since 1983. As of 1 January 1997, 29 104 individuals lived in the study area.17 Most of the population farms and belongs to the Sereer ethnic group: 74% are Muslim, 20% Catholic, and 3% Protestant. Although very few report they are animists (1%), all follow traditional rites to some degree.
Bandafassi
The survey was conducted in March 1998 in the region of Tambacounda in southeast Senegal, near the borders with Guinea and Mali. The population of this area has been under demographic surveillance for the past 25 years. In 1998, the population in the study area was 9576. The population consists mostly of farmers belonging to one of three ethnic groups. The Peul (57% of the population) are Muslims, while the Bedik (28%) and Malinke (16%) include Muslims, animists, and Christians.
Caio
The survey area is located in the region of Cacheu in northwest Guinea-Bissau, near the Senegalese border. Between March 1997 and January 1998, all consenting adults gave blood samples for HIV testing. The interviews were conducted in May and June 1998. The population of this area has been under demographic surveillance since 1989. The population in the study area in 1996 was 10 500. The population here too is mainly farmers, more than 95% of whom belong to the Manjako ethnic group. The distribution of religions is: 79% of the population report themselves to be animists, 20% Catholic, and 1% Muslim.
Study sample
The demographic databases for Bandafassi and Niakhar were used to build a random sample of adults aged 1559 years. A sample size of 1000 adults was sought. Because we estimated the proportion of people away from the area as 20% in Niakhar and 34% in Bandafassi from the demographic follow-up data, we set the initial sample sizes at 1200 and 1510, respectively. Eligible subjects from Niakhar and Bandafassi were asked to answer the study questionnaire and to give blood samples for HIV testing. In Caio, the biological data came from a sero-survey conducted between March 1997 and January 1998. All 5528 residents who were 15 years according to the demographic database were eligible for the study: 3104 participated. The sample was drawn from the population eligible for the earlier study (whether or not they had participated). The sample included 1920 adults. Because the serological data showed a high prevalence of HIV-2 and its prevalence, unlike that of HIV type 1 (HIV-1), is elevated in older age groups, the Caio survey also included those >59 years.18
Interview
Interviewers were recruited from the local population of each area. They went through a 4-day training period made up of coursework and individual interview simulation. They were taught to translate the questionnaire extemporaneously from written French or Portuguese to the local spoken language (they do not write or read it, since schooling is in French in Senegal and in Portuguese in Guinea-Bissau). Much of the training period was devoted to standardizing the translation. After informed consent was obtained, the interviews took place in private settings to protect confidentiality.
Content of the questionnaire
We derived a questionnaire from the Knowledge Attitudes Behaviour and Practices (KABP) questionnaire of the World Health Organizations Global Program on AIDS19 and from our experience during previous sexual behaviour surveys in another area of Senegal.11 This questionnaire was designed to study risk factors for HIV infection as well as perceptions of AIDS and its prevention, while taking the local socio-cultural context into account. The questionnaire was first tested during a 1995 pilot study.20
The following personal information was recorded: age, sex, marital status, religion, education, ethnic group, and occupation. The level of exposure to radio and television was also recorded. Long-term mobility was measured by the question: have you been away from your village for at least one month during the past 12 months? Short-term mobility was measured by the question: have you been away from your village for at least one day and one night in the past 4 weeks? Information about departure and arrival dates, destination, and reason for migration was recorded for up to two long-term voyages in the past 12 months and up to four short-term trips in the past 4 weeks.
Respondents were asked to provide information on up to four regular sexual partners and four casual partners in the past 12 months. A regular partner was defined as a sexual partner with whom the participant had sex regularly for at least one year, including spouses (even if married less than one year). A casual partner was defined as a partner who was not regular. The respondent was asked to provide for each, when possible, age, ethnic group and marital status, site (away or in the village), condom use, exchange of gift and of money for sex, and period and duration of the partnership. The Caio study area was divided into a peripheral and a central zone; almost all shops and facilities were in the latter, which was also the closest part of the study area to the only road to the nearest urban centre. Men were asked how many commercial sex workers they had sex with in the past 12 months. They were also asked whether they noticed any sexual discharge, sore or ulceration in the past 12 months, whether they were circumcised and, if so, at what age. Hospitalization and injection histories were recorded. A final part of the questionnaire was devoted to knowledge and perception of HIV and other sexually transmitted diseases (STD).
Biological tests
Between 1 and 2 ml of blood were collected from each consenting participant. Samples at all sites were screened for HIV with the commercial enzyme-linked immunosorbent assay (ELISA) ICE BASE PACK (Murex Diagnostics, Dartford, UK). Positive samples in Senegal were confirmed with a commercial immunoblot (BIO-RAD, NOVAPATH) for HIV-1 and with a homemade immunoblot for HIV-2 (whole virus lysate of HIV-2: MS-U937). Samples were classified as HIV-1 according to the manufacturers criteria and as HIV-2 when anti-env, -pol, or -gag antibodies were recognized. Positive samples in Caio were confirmed with commercial tests from Murex Diagnostics (Wellcozyme I for HIV-1 and ICEHIV-2 for HIV-2). Samples that were positive for both ELISA were tested by Pepti-Lav (Diagnostics Pasteur, Marnes-la Coquette, France) to confirm dual infections.
Ethics
Ethical approval for the study in Senegal was obtained from the national AIDS control programme and the national ethics committee, in Guinea-Bissau from the Ministry of Public Healths Co-ordination unit of Health Research and in Gambia, from the Joint Ethics Committee of the Gambian government and the Medical Research Council laboratories.
Analysis
All analyses were performed separately for each sex. Statistical significance was always set at 0.05. The analysis was conducted in three steps: (1) an ecological analysis compared the distribution of variables in populations with low and with high levels of HIV infection; (2) analyses on the individual level were performed for the population with a high HIV prevalence; (3) and finally the sexual risk taking behaviours of mobile and non-mobile participants were compared.
Ecological analysis
We determined whether the two populations in Senegal, where the level of infection was low, differed for any of the variables from the population in Guinea-Bissau, which had a relatively high level of infection. Only variables that differed significantly between either Niakhar or Bandafassi and Caio for at least one sex are presented in Table 1. A
2 test was used to compare proportions and a Wilcoxon-Mann-Whitney rank test to compare medians.
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Mobility and sexual behaviours
Because the multivariate analysis found that short-term mobility was associated with HIV infection, we completed the analysis by comparing the sexual behaviour reported by those who did and did not travel. A model was built for each behavioural variable for each gender and included the following potential confounding variables, when significant: age, matrimonial status, educational level, access to radio and television, religion, and ethnic group.
All statistical computations were performed with SPSS 9.0 for Windows (SPSS Inc. 1997, Chicago, IL).
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Results |
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Bandafassi
The initial sample included 1510 adults 1559 years (755 men and 755 women): 391 (26%) were away from their village, deceased or mentally disabled and could not be interviewed. Another 167 (15% of those present) refused to participate. The final sample included 440 men and 512 women. The mean age of the respondents was 33 years for men and 34 for women; for the non-participants, 30 and 32 years, respectively. Again, the differences were statistically significant for men (P = 0.001) and women (P = 0.03). None of the 393 men and 462 women tested was infected with HIV.
Caio
An initial sample of 1920 adults aged 15 years (954 men and 966 women) was drawn from those who participated in the serological survey between March 1997 and January 1998 (but were not necessarily tested for HIV infection): 486 (25%) were away from their village, deceased, or mentally disabled and could not be interviewed. Another 18 (1%) refused to answer the questionnaire. The final sample thus consisted of 671 men and 745 women. The mean age of the respondents was 38 years for men and 42 for women, and for non-respondents, 30 and 34 years, respectively. Again, these differences were statistically significant for men and women (P < 103).
Of those who were tested and who participated in the questionnaire (616 men and 675 women aged 15 years), 10.5% were infected with HIV (1.5% with HIV-1, 7.5% with HIV-2, 1.4% with both, and 0.2% with an undetermined type). More women were infected than men, and the difference is even higher when HIV-1 is excluded (6% of the men and 9% of the women).
Ecological analysis
Table 1 summarizes the variables that differed between Caio, the site with relatively high HIV levels and either or both of the sites with low HIV levels. To ensure comparability, the sample from Caio was restricted to those aged 1559 for this analysis.
The sample was sorted by age at interview. Age at marriage was estimated by the age at which half of the sample was or had ever been married; it was higher in Caio for men (29 years in Caio, 26 in Niakhar and in Bandafassi) and women (19, 16, and 17 years, respectively).
Median age at first sexual activity was significantly lower among men from Caio (17) than those from Niakhar (19) or Bandafassi (18). Conversely, this age was significantly higher among women from Caio (18) than those from the other sites (16 in Niakhar and 14 in Bandafassi). These results, together with those for age at marriage, suggest that women but not men have their first sexual relations and marry at nearly the same age. Moreover, the gap for men between age at first sexual activity and age at marriage is substantial and even wider for the men from Caio (12 years) than from Niakhar (7 years) or Bandafassi (8 years).
Both men and women from Caio were more than twice as likely to report alcohol consumption in the past week than those from the other sites (80% of the men and 84% of the women versus less than 32% of respondents from the other two sites). They also reported condom use in the past 4 weeks at a higher rate than respondents from the other sites. More men from Caio had any schooling than those from Niakhar and Bandafassi, while the women from Caio were more likely to have any schooling than those from Niakhar.
Married men, but not women, from Caio reported non-spousal regular partners more often (for men: 23% versus 4% in Niakhar and 8% in Bandafassi). Respondents from Caio, men or women, were not more likely than those from Senegal to report casual partners, casual partners in a city or partners with an exchange for money.
Sexual contacts with exchange of money and commercial sex are clearly two different concepts: one-third of the male respondents reported sex with an exchange of money in Bandafassi, but only 2% reported contacts with sex workers. The highest proportion of men reporting contacts with sex workers was in Caio (8%). Nobody in Niakhar reported contact with sex workers.
Men from Caio were less likely to report being circumcised: male circumcision was almost universal in Niakhar and Bandafassi while 72% of the men from Caio reported they were circumcised. This reflects both a lower rate of male circumcision in Caio and a later age at circumcision. It is nonetheless likely that a substantial proportion of the men from Caio will never be circumcised: 9% of those >29 years are not. Female circumcision is almost non-existent in Niakhar and Caio, but universal in Bandafassi.
Both long- and short-term mobility were very common in all three sites. Long-term mobility was most frequent in Niakhar, where it was reported by 39% of the men and 26% of the women. In Bandafassi it was reported by 19% and 7%, respectively, and in Caio by 21% and 22%. Short-term mobility was most frequent in Bandafassi, reported by 56% of the men and 35% of the women. In Niakhar it was reported by 33% and 29%, respectively, and in Caio by 35% and 24%.
Individual-level analysis
Because of the low HIV prevalence at the sites in Senegal, the risk factor analysis was restricted to Caio. The HIV prevalence varied greatly by age group, and the age distribution is the result of the combination of two different and well-known age distributions: a peak at young ages for HIV-1 and prevalence that increases with age for HIV-2. These groups were pooled for the risk factor analysis however, to ensure sufficient statistical power. Because mobility could be associated with seeking health care, we excluded from the multivariate analyses all respondents who reported at least one short-term trip for a medical reason. The multivariate analysis thus considered 520 sexually active men and 626 sexually active women from Caio. Table 2 presents the results of the univariate analysis of risk factors for HIV infection and Table 3
the multivariate analysis.
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Only 16 men reported that a wife was not currently living in Caio, and 140 women a husband residing elsewhere. The HIV prevalence among these 16 men was 18.8%, twice the level of the general adult population (but not significant, probably because of the absence of statistical power: P = 0.17, Fishers exact test). The rates of HIV infection were similar for the women whose husbands did live in Caio and for those whose did not (10.7% [N = 140] versus 11.1% [N = 505]).
Respondents in Caio were asked to state where they went for up to four short-term trips. This enabled us to compare HIV infection levels according to destination for the participants. Men who reported at least one short-term trip to Bissau were more likely than the men who reported short-term trips elsewhere to be infected with HIV (15.7% versus 6.5%, P = 0.005). When a short-term trip to Bissau was included in the multivariate risk factor analysis, it was a better predictor of HIV infection than overall short-term mobility (aOR = 3.44; data not shown). No specific destination was significantly associated with an increased probability of HIV infection among women.
Mobility and sexual behaviours
Because the risk factor analysis strongly suggested the importance of short-term mobility and (for women) associated risk behaviours, we investigated this issue further at all three sites by comparing behavioural variables between those who reported short-term mobility and those who did not. Table 4 shows the associations of risk behaviours and condom use with short-term mobility, adjusted for potential confounding social and demographic characteristics. Short-term mobility was associated with a higher frequency of risk behaviours for men in Bandafassi (casual partner in the last 12 months: aOR = 1.9) and Caio (more than one partner in the last 12 months: aOR = 2.8) and for women in Niakhar and Caio (casual partner in the past 12 months: aOR = 8.3 and 5.7, respectively). Among men from Bandafassi and women from Niakhar, short-term mobility was also associated with an increase in reported condom use (aOR = 3.3 and 5.3, respectively). This trend was also observed in Caio, where it was not, however, statistically significant.
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Discussion |
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We sought to identify social, demographic, and behavioural factors that might be associated with HIV infection at the population and the individual level so that we could explain its heterogeneity at our three sites. No factors, however, were found to be a risk factor in Caio or to distinguish Caio from the two Senegalese populations with low levels of infection. The associations observed between HIV infection and mobility do not, however, imply that mobility is the only source of HIV within the Caio area. Support for a broader range of sources comes from the findings among women: both residence in the central area and a casual partner in a city during the past year were independently associated with an increased risk of HIV infection. This result suggests that mobility alone cannot explain the HIV prevalence observed in Caio.23
Surveillance of HIV prevalence in Ziguinchor, Senegal, during the late 1980s found that prostitutes from Guinea-Bissau were more likely to be infected with HIV-2 than those from elsewhere.24 Further observation indicated that many of the prostitutes working in Bissau and Ziguinchor came from Caio. This led the Medical Research Council to conduct a study in 19891991 to investigate the epidemiology of HIV in the area in 19891991.16,23 No woman in our survey reported working as a prostitute while outside the village. On the other hand, the question was not specifically asked: rather, we asked the reasons for short- and long-term absences. In an in-depth qualitative study in Caio, no women reported commercial sex work either (Enel C, personnal communication), but the sample was small (25 women). The strong association between casual sex in a city and HIV infection may reflect commercial sex work by some women.
Despite the predictive role of short-term mobility in the 4 weeks before the survey, identified in multivariate risk factor analyses, this mobility should not be misinterpreted as a genuine exposure variable: the interview was conducted shortly or immediately after the serological survey. The variable is used as an index of mobility habits. Another concern is the reliability of self-reported data on behaviours related to AIDS and sexuality. A reliability survey we carried out in another rural area of Senegal showed that the same interview procedure (questionnaires filled out by local interviewers) provided very reliable data on sexual behaviour in married couples.25
Participants were consistently older than those who were not interviewed, at all three sites. The principal reason for non-participation was that the pre-selected sample members were not at home on any of the repeated occasions that the interviewer tried to contact them. Non-participation is therefore associated with mobility and could lead to selection bias. We do not see, however, how this selection bias could differ significantly from one site to another. We therefore think that even if it is likely that mobility was underestimated in our study, the comparison of population characteristics between sites remains valid. Because those who are most mobile are also probably at the greatest risk of HIV infection, it is likely that both the overall HIV prevalence and the magnitude of the association between the risk of HIV infection and mobility have been underestimated in our study. The very large age difference between participants and non-participants in Caio is explained by the fact that permanent migration is very common in this area. Many adults >30 years were reported by their family to be part of the population, although they had been living elsewhere for a long time.
The study areas had a relatively low level of HIV infection compared with southern and eastern Africa. The prevalence level in Caio, however, is similar to that in the capital city, Bissau.26 It is also consistent with the findings of an earlier (19891991) study in the same area,16 with an increase from 0.1% of adults infected with HIV-1 in 1990 to 1.5% now. This augmentation confirms the trend found in the nearby region of Ziguinchor, Senegal, where the prevalence of HIV-1 has risen while that of HIV-2 remains stable.27,28
Mobility appeared to be a key factor in the spread of HIV spread in rural areas of West Africa, not only because population movements enable the virus to disseminate but also because of the particularly risky behaviour of those who are mobile. More prevention efforts should be directed at migrants from rural areas who travel to cities with substantial levels of HIV infection.
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MECORA group members |
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KEY MESSAGE
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Acknowledgments |
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References |
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