High sexual risk taking and diverging trends of HIV-1 and HIV-2 in the military of Guinea Bissau

Background: HIV and other sexually transmitted infections are a growing problem in the military personnel of Africa, and information about this problem in Guinea-Bissau is lacking. The aims of this study were to determine the prevalence and trends of the HIV epidemics in the military forces of Guinea Bissau and to explore possible risk factors for HIV infection. Methodology: Repeated cross-sectional surveys of HIV-1 and HIV-2 were conducted between 1992 and 2005, and knowledge, sexual behaviour and risk factors for HIV-1 and HIV-2 in military personnel in Guinea-Bissau were assessed. Results: The seroprevalence of HIV-1, HIV-2 and HIV-1+HIV-2 dual reactivity was 1.1%, 8.4% and 0.1% in 1992-95, and in 2005 7.7%, 5.1% and 1.9%, respectively. Both the increase of HIV-1 and the decline of HIV-2 between 1992-95 and 2005 were significant when adjusted for age (p < 0.001 for both changes). Only a minority did not know how HIV transmits, but sexual risk taking was high. Several significant risk factors were found in univariate analyses for HIV-1 and HIV-2, but the only risk factor that remained significant after multivariate regression analysis was previous contact with a prostitute among HIV-1-positive subjects (single and dually reactive) (p < 0.01). Conclusion: The increasing trend of HIV-1 and the high risky sexual behavior illustrate the need for improvement in HIV/AIDS prevention efforts among military personnel in Guinea Bissau.


Introduction
Military personnel in Africa are at high risk of contracting and transmitting sexually infections (STIs), including HIV/AIDS.The impact of HIV on the military in the African continent has assumed alarming dimensions.It is estimated that sexually transmitted disease rates among armed forces are generally two to five times higher than in the civilian populations [1], and prevalence rates of HIV between 5.8% and 26.7% have been reported from different African militaries [2].AIDS is now the leading cause of death in military and police forces in some African countries, accounting for more than half of in-service mortality [3].
Guinea-Bissau has the highest prevalence of HIV-2 in the world, but over the last years declining prevalence rates have been observed, both among pregnant women and in two population-based studies from urban and rural Guinea-Bissau [4][5][6].Concurrently, the prevalence of HIV-1 has increased significantly in the same study groups.
The objectives of this study were to determine the prevalence and trends of the HIV epidemics in the military forces of Guinea Bissau during the period 1992-2005.We also wanted to explore possible risk factors for HIV infection.

Materials and methods
The study was conducted in seven main military bases in the seven main cities of Guinea Bissau (Bafatá, Bissau, Canchungo, Cumeré, Gabu, Mansoa, and Quebo).Four cross-sectional studies were performed at yearly intervals during the period 1992-1995 and a total of 1,592 subjects (0.9% women) were included.In every survey, all military officers and recruits from each one of the bases were invited to participate.In 2005, a new serosurvey was organized in five of these cities and in three additional cities (Nhala, Bambadinca and Buba).Similarly, all military personnel were invited to the study, and 725 subjects (1.5% women) were included.
At inclusion, after informed consent was given, a physical examination was done, a questionnaire was performed, information about STI and HIV/AIDS was given, and a blood sample was drawn for serologic testing of HIV and syphilis.The questionnaire included data on age, gender, education, HIV/AIDS knowledge and sexual behavior, such as condom use, involvement in commercial sex, and number of sexual partners outside of marriage in the last month.Information on the individual's history of blood transfusion, circumcision, genital ulcer, and urethral discharge was also gathered.Unfortunately the questions regarding knowledge of HIV/AIDS and previous contact with a commercial sex worker was not included in the questionnaire until 1994 (most of the 1994 survey and then onwards), and by mistake the question of circumcision was not included in the questionnaire of 2005 so only parts of the total number of persons were analyzed regarding these questions.Free condoms were distributed and medical treatment was given for current diseases.Positive results of syphilis serology were individually linked and adequate treatment given.In case of individual requirement, HIV results were given and individual counseling was offered.No antiretroviral treatment was available in the country when the study was done.

Statistical analysis
Odds ratios (OR) with 95% confidence interval (CI), p-values of Chi-square, Fisher's exact test and one-way analysis of variance (ANOVA) were calculated with Epi Info (Centers for Disease Control, U.S.A. and WHO, Switzerland).Multivariate logistic regression analyses were performed using STATA (Stata Corp. Texas, U.S.A.).In the regression analyses age was treated as a continuous variable.
Potential factors that could influence the probability of acquiring HIV are presented in Table 1.In univariate analysis a significantly higher proportion of HIV-2-positive subjects had only 0-4 years of education in 1992-95 as compared to HIVnegative individuals (p < 0.001).Blood transfusion or circumcision were not shown to be associated with HIV prevalence, but unfortunately the question of circumcision was not included in the questionnaire of 2005 so only a limited number of persons was  a Odds ratio for paired comparison between HIV-1-positive and HIV-negative subjects b Odds ratio for paired comparison between HIV-2-positive and HIV-negative subjects c Treponema pallidum hemagglutination assay * p < 0.05 of Chi-square test compared to HIV-negative subjects (Fisher's exact test when needed) ** p < 0.01 of Chi-square test compared to HIV-negative subjects (Fisher's exact test when needed) *** p < 0.0001 of Chi-square test compared to HIV-negative subjects (Fisher's exact test when needed) analyzed.The proportion of subjects with one or more partners in the last month previous to taking the survey (outside of marriage if married) was generally very high in all groups, and significantly more HIV-1-positive subjects reported previous contact with a commercial sex worker (CSW) compared to HIVnegative controls (p < 0.001).Surprisingly, no use of condoms was more frequent among HIV-negative soldiers compared to HIV-1-positive subjects.Knowledge about HIV/AIDS was generally satisfactory, and a trend of improvement was seen between 1992-1995 and 2005.Only a minority did not know how HIV/AIDS was transmitted, but there was a trend of a higher proportion among HIVpositive (33.3% of HIV-1-positive and 12.5% of HIV-2-positive) as compared to HIV-negative subjects (10.0%) in 1992-1995.
A history of urethral discharge was frequent in all groups including HIV-negative individuals (range 24.3-35.7%),but the difference compared to HIVnegative individuals was only significant in HIV-2positive individuals.Likewise, a history of genital ulcer disease as well as TPHA-reactivity was significantly higher among HIV-2-positive subjects compared to HIV-negative controls.
Thus several significant risk factors were found in univariate analyses among HIV-positive subjects, but performing a multivariate logistic regression analysis adjusting for all significant risk factors found (age, education, ≥ 1 number of partners in the last month, previous contact with a CSW, a history of genital ulcer or urethral discharge and TPHAreactivity), the only risk factor that remained significant was previous contact with a CSW among HIV-1-positive subjects (single and dually reactive analysed together) compared to HIV-negative subjects (adjusted OR = 2.1, 95% CI 1.2-3.6;p < 0.01).

Discussion
This study has revealed an alarming increase of HIV-1 from 1.2% in 1992-1995 to 9.6% in 2005 (including HIV-1+HIV-2-positive subjects) among the military in Guinea Bissau.Simultaneously the prevalence of HIV-2 declined from 8.5% to 7.0%.These results coincide with the changes of HIV prevalence observed in a cohort study of police officers in Guinea-Bissau between 1990 and 2007 [8].Similar changes of prevalence rates of HIV-1 and HIV-2 were also found among pregnant women in the capital Bissau and in two recently published population-based studies from urban and rural Guinea-Bissau, although the prevalence rates were generally higher in our study [4][5][6].This is in agreement with previous studies which have found higher prevalence rates of HIV among uniformed personnel compared to the general population or pregnant women [9].A limitation of our study was that we only measured the prevalence at two time points (1992-1995 and 2005) with a fairly long interval between.Thus we cannot say if the trend of HIV-1 is still rising or not.However, both in the study of police officers and among pregnant women in Guinea-Bissau a stabilization of HIV-1 has been observed in recent years [4,8].In the neighbouring countries of Senegal and The Gambia, HIV-1 and HIV-2 prevalence rates have continued on a comparatively low level in pregnant women (around or below 1 %) [10,11].However, similar trends of increasing HIV-1 prevalence and a decreasing HIV-2 prevalence was reported among clinical patients in The Gambia as well as in a cohort of female commercial sex workers in Senegal [12,13].
Guinea-Bissau experienced a civil war in 1998-1999, causing major population displacements and general decline in public services such as health institutions during that time [14,15].This could be one explanation for the dramatic increase of HIV-1 among military personnel over the study period.The relationship between HIV and conflict is complex.As opposed to earlier beliefs that conflicts in general should aggravate HIV transmission, several publications have described how conflicts may actually limit the spread of HIV during the period of conflict [16].However, there is substantial evidence of mobility as an important factor increasing the risk of HIV transmission [17], and in the conflict in Guinea-Bissau approximately 250,000 inhabitants of the capital Bissau repeatedly left for the interior of the country during several outbreaks of conflict.The reason we didn't find a similar increase of HIV-2 after the war was probably because of the much lower transmission risk of HIV-2 as compared to HIV-1 [18)] Other reasons for the increase of HIV-1 could be changes in sexual risk behaviour or cultural factors, but data on these parameters are scarce in Guinea-Bissau.
HIV-2 was found to be more prevalent among the older age groups, and in the 2005 survey very few HIV-2-positive subjects younger than 35 years of age were found (no subjects younger than 25 years of age).Conversely, HIV-1 was more or less evenly distributed across the age groups.One explanation could be a cohort effect due to the slower disease progression in HIV-2 compared to HIV-1.Another reason could be attributed to the spread of HIV-2 during the war of independence in the 1960s and early 1970s in Guinea-Bissau, when HIV-2 already existed in Guinea-Bissau [18].It has been suggested that transmission of HIV-2 then might have been driven by multiple mechanisms, such as inoculation campaigns, non-sterile surgical procedures or injections, blood transfusions and sexual transmission [19].None of the neighbouring countries had a similar period of prolonged armed conflict during the sixties and the seventies.Thus, the declining prevalence of HIV-2 that we have observed in this study could be the return of the HIV-2 prevalence to a steady state level similar to levels in The Gambia and Senegal.In a recent mathematical simulation model regarding a rural population in Guinea-Bissau, it was suggested that 30% of the decline in HIV-2 prevalence is due to competition from HIV-1 including the excess mortality of core groups transmitting both HIV-1 and HIV-2.Seventy percent of the decline should be due to a behavioural change from a conflict setting to a peacetime situation after the end of the war of independence in 1963-1974 [20].
Even though the majority of the participants knew about HIV/AIDS transmission methods and a trend of better knowledge was noted over the study period, sexual risk taking was high.This could also be an explanation for the increasing prevalence of HIV-1.Almost half the participants reported one or more sexual partners outside of their marriage in the last month while approximately one third had previous contact with a CSW.Furthermore, for both these risk factors the trend was unfortunately increasing between 1992-1995 and 2005.Most participants did not use condoms and another minority only sometimes used condoms.The collection of this kind of data is always connected with a certain amount of unreliability.Since both underreporting and exaggerations are possible, the effect of bias is hard to anticipate.Regarding history of genital ulcer or urethral discharge, it is more likely that events will be forgotten as time passes, and therefore underreporting is plausible.Even so, more than three times more HIV-2 infected subjects and almost two times more HIV-1-positive persons reported a history of genital ulcer as compared to HIV-negative subjects.This association (only significant in HIV-2-positive subjects) might be a sign of high sexual risk behaviour, but it is also well known that disrupted mechanical barriers by a genital ulcer increase the risk of acquiring HIV [21].However, in a multivariate regression analysis the only risk factor that remained significant was previous contact with a CSW, which demonstrates the importance of reaching CSWs in the preventive efforts in controlling the epidemic of HIV-1.
In most other countries in Africa, the prevalence of HIV is higher among military personnel than in the general population [2].However, there are some examples where prevention campaigns among the armed forces have led to improved knowledge of HIV/AIDS as well as a decline in STI-incidence [22,23].Our observations indicate that military leadership must recognize the urgent need to increase HIV/AIDS prevention efforts through the promotion of programs focusing on HIV/AIDS and STI prevention and treatment among the armed forces.Counseling, voluntary and confidential HIV testing of military personnel, socio-economic assistance to families and survivors of ill soldiers and start of antiretroviral therapy among military personnel are also recommended.
No association could be found between circumcision and HIV.However, since the majority of males in Guinea-Bissau are traditionally circumcised during adolescence, few subjects were not circumcised (totally 19.1%) and therefore the statistical power for this comparison was weak.In addition, the question regarding circumcision was included only in the 1992-1995 survey, and at that time (1992-1995) HIV-1 was very rare so the probability to detect a great difference in HIV-1prevalence was quite small.It has never been shown that circumcision might be a protective factor against HIV-2.
In conclusion, the prevalence of HIV-1 increased significantly while the prevalence of HIV-2 decreased significantly between 1992-1995 and 2005 among military personnel in Guinea-Bissau.Sexual risk taking was high and previous contact with a prostitute was an independent risk factor for HIV-1.These observations call for attention and point to an urgent need to increase HIV/AIDS prevention efforts among the armed forces in Guinea-Bissau.

Figure 2 .
Figure 2. Seroprevalence (%) of HIV according to age distribution in military personnel in Guinea-Bissau 1992-2005.Mean age was 31.3 and 38.2 years in 1992-95 and 2005, respectively.Total number of subjects in the different age groups in the period 1992-1995 was 385, 688, 389 and 117, and in 2005 63, 232, 219 and 210.

Table 1 .
Risk factors for HIV in military personnel in Guinea-Bissau 1992-2005.HIV-1/HIV-2 dually reactive subjects are included in both the HIV-1-positive and the HIV-2-positive group (two subjects in 1992-95 and 14 subjects in 2005).
a Odds ratio for paired comparison between HIV-1-positive and HIV-negative subjects b Odds ratio for paired comparison between HIV-2-positive and HIV-

Table 1 (
Continued).Risk factors for HIV in military personnel in Guinea-Bissau 1992-2005.HIV-1/HIV-2 dually reactive subjects are included in both the HIV-1-positive and the HIV-2-positive group (two subjects in 1992-95 and 14 subjects in 2005).