Original research article
HIV infection and risk factors among the armed forces personnel stationed in Kinshasa, Democratic Republic of Congo
International Journal of STD & AIDS 2015, Vol. 26(3) 187–195 ! The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0956462414533672 std.sagepub.com
AW Rimoin1, NA Hoff1, CF Djoko2, NK Kisalu3, M Kashamuka4, U Tamoufe2, M LeBreton2, PK Kayembe4, JJ Muyembe5, CR Kitchen6, K Saylors2, J Fair2, R Doshi1, E Papworth7, E Mpoudi-Ngole8, MP Grillo9, F Tshala10, M Peeters11 and ND Wolfe2,12
Abstract Despite recent declines in HIV incidence, sub-Saharan Africa remains the most heavily affected region in the global HIV/AIDS epidemic. Estimates of HIV prevalence in African military personnel are scarce and inconsistent. We conducted a serosurvey between June and September 2007 among 4043 Armed Forces personnel of the Democratic Republic of Congo (FARDC) stationed in Kinshasa, Democratic Republic of Congo (DRC) to determine the prevalence of HIV and syphilis infections and describe associated risk behaviours. Participants provided blood for HIV and syphilis testing and responded to a demographic and risk factor questionnaire. The prevalence of HIV was 3.8% and the prevalence of syphilis was 11.9%. Women were more likely than men to be HIV positive, (7.5% vs. 3.6% respectively, aOR: 1.66, 95% C.I: 1.21–2.28, p < 0.05). Factors significantly associated with HIV infection included gender and self-reported genital ulcers in the 12 months before date of enrollment. The prevalence of HIV in the military appears to be higher than the general population in DRC (3.8% vs. 1.3%, respectively), with women at increased risk of infection.
Keywords Africa, syphilis (Treponema pallidum), HIV (Human immunodeficiency virus), AIDS, prevalence, sexual behaviour, epidemiology Date received: 22 January 2014; accepted: 30 March 2014
Introduction Despite recent declines in HIV incidence, sub-Saharan Africa remains the most heavily affected region in the global HIV/AIDS epidemic. It is estimated that 1 Department of Epidemiology, Los Angeles Fielding School of Public Health, University of California, Los Angeles, CA, USA 2 Global Viral Forecasting (now known as Metabiota) San Francisco, California, USA, and Yaounde´, Cameroon 3 Vaccine Research Center, NIAID/NIH, Bethesda, MD, USA 4 Kinshasa School of Public Health, University of Kinshasa, Democratic Republic of Congo 5 National Institute for Biomedical Research, Kinshasa, Democratic Republic of the Congo 6 Department of Biostatistics, Fielding School of Public Health, University of California, Los Angeles, Los Angeles, CA, USA
sub-Saharan Africa currently accounts for nearly 70% of the world’s HIV infections with a prevalence of more than 22.5 million.1 7
Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, USA 8 Virology Laboratory, CREMER/IMPM/IRD, Yaounde´, Cameroon 9 Department of Defense HIV/AIDS Prevention Program (DHAPP), Naval Health Research Center, San Diego, CA, USA 10 Military Health Services, Ministry of Defense, Kinshasa, Democratic Republic of the Congo 11 Laboratoire Retrovirus, UMR 145, Institute for Research and Development (IRD) and University of Montpellier 1, Montpellier, France 12 Program in Human Biology, Stanford University, Stanford, CA, USA Corresponding author: Anne W Rimoin, Department of Epidemiology, UCLA School of Public Health, CHS 41-245, Los Angeles, CA 90005, USA. Email: [email protected]
188 In addition to high-risk sexual behaviours, the disproportionate burden of HIV experienced by this region has been attributed to a number of economic, social, and political factors including poverty, civil unrest, and increased mobility.2,3 Moreover, certain occupations involving frequent migration such as migrant labour, mining, truck driving, and military involvement are associated with an increased risk of contracting HIV and other sexually transmitted infections (STIs).4 Migratory lifestyles characterised by long periods of familial separation provide an opportunity to engage in casual sex with multiple partners and commercial sex workers.2 Recent studies have shown that the HIV prevalence of adults aged 15–49 in the Democratic Republic of Congo (DRC) is lower than the overall sub-Saharan African estimate (1.3% vs. 5.2%).5 However, HIV prevalence among DRC’s most-at risk-populations (MARPs) are significantly higher, which includes sex workers (14.7% in Kinshasa and 23.3% in Lubumbashi) and conflict-afflicted populations (3.1% to 6.7%).1,6–8 Reports documenting the high rates of non-partner sexual violence in mathematical modeling scenarios show the potential for an increase in annual HIV incidence by 7%, impacting up to 10,000 women and girls in the DRC under extreme conditions.9 Past publications have suggested (non-empirically) that the HIV prevalence in the Congolese military could be as high as 60%.10–14 Additionally, reports based on predictions may have overestimated the prevalence of HIV in the Congolese military.10–12,14 These estimates were generated in 1999, while the DRC was actively engaged in a multi-country civil war. In addition, the confidentiality of information regarding the size and structure of the FADRC may contribute to inaccurate estimates of disease prevalence within the military. Estimates of HIV prevalence in African military personnel are limited and inconsistent. Some research has suggested that HIV rates are higher in military populations, while other studies indicate that rates are, instead, comparable to the general population.15,16 The sexual behaviours of soldiers have significant implications for the spread of HIV and other STIs, who appear to be at an increased risk of infection.17,18 Military personnel tend to be young men, spending considerable amounts of time away from home, and have access to a large number of sexual partners, including commercial sex workers and internally displaced women.15,19–21 In a 2008 study of military personnel in Ethiopia, participants self-reported their military background, work-associated travel, sexual history and risk behaviours. Higher military rank, higher numbers of sex partners, and month-long travel in the past year were factors associated with an elevated risk of HIV
International Journal of STD & AIDS 26(3) infection and other STIs compared to those in the general population.2 In a recent survey of Nigerian naval personnel, about 20% of men had sexual contact with a commercial sex worker in the past six months and 40% had not used a condom.22 Studies have also suggested that military personnel are often paid more consistently than other government employees, leading to increased financial stability and the ability to purchase sex, placing them at higher risk of HIV infection.22–24 Preliminary HIV genetic analysis using specimens collected from DRC military personnel suggest high HIV heterogeneity, yet a fairly low prevalence of infection.25 Although these results are similar to previous studies in the general population,26–28 scant data are available on the risk factors and prevalence of STIs, including HIV and reasons behind the high genetic diversity of the disease, in the Armed Forces personnel of the Democratic Republic of Congo (FARDC). Further analysis was conducted to estimate the HIV prevalence in the FARDC and evaluate risk factors associated with HIV and other STIs.
Methods Population selection From June to September 2007, a single-stage 30-cluster sample survey was conducted among active FARDC personnel stationed in Kinshasa. The military population is currently estimated to be 155,000 persons, 2.7% (4185) of which are women, who participate in both administrative roles and in field operations.29 A complete list of companies based in Kinshasa obtained from the Ministry of National Defense was used to randomly select individual companies to serve as study sites. In each selected unit (company), every active duty man and woman (officers and enlisted) was offered enrollment in the study, and informed consent was required for participation. The study protocol was approved by Human Subjects Protection Organisations at both the Kinshasa School of Public Health and United States Army Medical Research and Material Command.
Questionnaire, specimen collection and testing All participants were provided with HIV testing and counseling, and a detailed explanation of the purpose, confidentiality and procedures of the study. Trained interviewers administered a 60-min questionnaire that included socio-demographic characteristics, duration and location of military service, sexual behaviours and self-reported STI symptoms within the past 12 months. Participants were asked to return for their HIV and syphilis test results one week later.
Rimoin et al. Blood samples were processed and separated into buffy coat and plasma on the same day and kept at 20 C at the DRC National AIDS Program Laboratory in Kinshasa. Buffy coat samples conserved at 80 C were used for HIV genetic testing.26 Plasma was tested for HIV antibody following the DRC national testing algorithm; a rapid test (Determine HIV-1/2 from Abbott, IL, USA) followed by an ELISA test (Enzygnost HIV1/2 integral from Dade Behring, Dresden, Germany). Specimens were classified as HIV positive if reactive on both tests. Discordant or indeterminate samples were retested by two ELISA tests, Enzygnost HIV 1/2 and Vironostika (bioMerieux SA, Marcy, l’Etoile, France), and classified as positive if reactive for both of the ELISA tests. Individuals testing positive for HIV and returning for results were referred to the military health centre. Samples were tested for syphilis using the Determine Syphilis rapid test,30 and results were available to participants within 48 h. Individuals testing positive for syphilis infection were treated on site with a single shot of benzathine penicillin G, and referred to a health centre for follow-up.
Statistical analysis and variable selection Data analysis for this paper was conducted using SAS software, version 9.2.31 Participants with missing HIV status or basic data from the questionnaire were excluded from the analysis. Frequency distributions of socio-demographic and behavioural characteristics were calculated for men and women separately. Due to the low number of women participants, data on HIV prevalence for socio-demographic and risk factor subgroups could not be stratified by gender. For variable categorisation, categories found in the 2007 Demographic and Health Survey (DHS) analysis were used when possible – including age group, number of sexual partners and birth region; mobility was defined as number of posts outside Kinshasa during the preceding five years, and questions which were believed to be ambiguous in the original wording of the question were not included for further analysis. Associations between selected variables and HIV infection were first explored with complete case analysis using logistic regression. Best subset selection was used for model selection, after testing a number of other model selection methods, and the multiple imputation method was used to account for missing data (all assumptions were met, and individuals missing data were not significantly different from those not missing data). The final model was analysed using 20 imputations. The final model selected includes variables adjusted for age, gender, time in the garrison, mobility, numbers of sex partners, genital ulcer and active syphilis infection.
189
Results Socio-demographic characteristics A total of 4043 military personnel (2.6% of total estimated military population) were enrolled between June and September 2007; of these, 97% (3919 total, 3735 men, 163 women, and 21 with missing gender data) had questionnaire and laboratory data available for analysis. Participant ages ranged from 18 to 75 years; those in the 30–34 age group comprised 25% of the sample (Table 1). Men tended to have higher rank, to have spent less time in Kinshasa and have a greater number of sexual partners (Tables 1 and 2) compared with women. There were no differences by gender when self-reporting genital ulcer symptoms (9.2% in males, vs. 9.8% in females).
Prevalence of HIV and syphilis Overall HIV prevalence was 3.8%; 48 persons tested positive for HIV infection. HIV prevalence was higher among women (8.0%) compared to men (3.6%) in the study population (aOR: 1.66, 95% C.I. 1.21, 2.28) (Table 3). A total of 463 (11.9%) persons tested positive for syphilis; however, there was no significant difference in prevalence between men and women (11.9 vs. 11.7%, respectively) (Table 2).
Risk factors for HIV infection Univariate odds ratios (ORs) are presented for each variable (Tables 3 and 4). Variables included in the multivariate model were age, gender, military rank, time in Kinshasa garrison, mobility, number of sexual partners, self-reporting of genital ulcer and syphilis infection. When looking at age, participants aged 45–49 had the highest percentage of those testing positive for HIV compared to other age groups (Table 3). Additionally, those stationed for less than one year in the Kinshasa garrison were at highest risk of testing positive for HIV compared to those assigned for longer time periods (Table 3). However, these soldiers were not necessarily new recruits; based on the available data for those in this category (n ¼ 88, data not presented), all had been in the military for at least five years. While the HIV prevalence increased with the number of sexual partners reported in the past 12 months (no partners: 3.4% vs. 5þ partners: 4.2%), there were no significant differences in the adjusted odds ratios (aOR ¼ 1.18, 95% C.I. 0.77, 1.79) for HIV infection (Table 4). After adjusting for other variables, there was a significant association between those reporting a genital ulcer in the past 12 months and HIV infection.
190
International Journal of STD & AIDS 26(3)
Table 1. Socio-demographic characteristics of survey participants (n ¼ 3919). Variable Age Under 20 20–24 25–29 30–34 35–39 40–44 45–49 50þ Missing Grade Senior Officer Junior Officer Noncommissioned Officer (NCO) Enlisted Missing Years of military service
HIV infection and risk factors among the armed forces personnel stationed in Kinshasa, Democratic Republic of Congo
International Journal of STD & AIDS 2015, Vol. 26(3) 187–195 ! The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0956462414533672 std.sagepub.com
AW Rimoin1, NA Hoff1, CF Djoko2, NK Kisalu3, M Kashamuka4, U Tamoufe2, M LeBreton2, PK Kayembe4, JJ Muyembe5, CR Kitchen6, K Saylors2, J Fair2, R Doshi1, E Papworth7, E Mpoudi-Ngole8, MP Grillo9, F Tshala10, M Peeters11 and ND Wolfe2,12
Abstract Despite recent declines in HIV incidence, sub-Saharan Africa remains the most heavily affected region in the global HIV/AIDS epidemic. Estimates of HIV prevalence in African military personnel are scarce and inconsistent. We conducted a serosurvey between June and September 2007 among 4043 Armed Forces personnel of the Democratic Republic of Congo (FARDC) stationed in Kinshasa, Democratic Republic of Congo (DRC) to determine the prevalence of HIV and syphilis infections and describe associated risk behaviours. Participants provided blood for HIV and syphilis testing and responded to a demographic and risk factor questionnaire. The prevalence of HIV was 3.8% and the prevalence of syphilis was 11.9%. Women were more likely than men to be HIV positive, (7.5% vs. 3.6% respectively, aOR: 1.66, 95% C.I: 1.21–2.28, p < 0.05). Factors significantly associated with HIV infection included gender and self-reported genital ulcers in the 12 months before date of enrollment. The prevalence of HIV in the military appears to be higher than the general population in DRC (3.8% vs. 1.3%, respectively), with women at increased risk of infection.
Keywords Africa, syphilis (Treponema pallidum), HIV (Human immunodeficiency virus), AIDS, prevalence, sexual behaviour, epidemiology Date received: 22 January 2014; accepted: 30 March 2014
Introduction Despite recent declines in HIV incidence, sub-Saharan Africa remains the most heavily affected region in the global HIV/AIDS epidemic. It is estimated that 1 Department of Epidemiology, Los Angeles Fielding School of Public Health, University of California, Los Angeles, CA, USA 2 Global Viral Forecasting (now known as Metabiota) San Francisco, California, USA, and Yaounde´, Cameroon 3 Vaccine Research Center, NIAID/NIH, Bethesda, MD, USA 4 Kinshasa School of Public Health, University of Kinshasa, Democratic Republic of Congo 5 National Institute for Biomedical Research, Kinshasa, Democratic Republic of the Congo 6 Department of Biostatistics, Fielding School of Public Health, University of California, Los Angeles, Los Angeles, CA, USA
sub-Saharan Africa currently accounts for nearly 70% of the world’s HIV infections with a prevalence of more than 22.5 million.1 7
Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, USA 8 Virology Laboratory, CREMER/IMPM/IRD, Yaounde´, Cameroon 9 Department of Defense HIV/AIDS Prevention Program (DHAPP), Naval Health Research Center, San Diego, CA, USA 10 Military Health Services, Ministry of Defense, Kinshasa, Democratic Republic of the Congo 11 Laboratoire Retrovirus, UMR 145, Institute for Research and Development (IRD) and University of Montpellier 1, Montpellier, France 12 Program in Human Biology, Stanford University, Stanford, CA, USA Corresponding author: Anne W Rimoin, Department of Epidemiology, UCLA School of Public Health, CHS 41-245, Los Angeles, CA 90005, USA. Email: [email protected]
188 In addition to high-risk sexual behaviours, the disproportionate burden of HIV experienced by this region has been attributed to a number of economic, social, and political factors including poverty, civil unrest, and increased mobility.2,3 Moreover, certain occupations involving frequent migration such as migrant labour, mining, truck driving, and military involvement are associated with an increased risk of contracting HIV and other sexually transmitted infections (STIs).4 Migratory lifestyles characterised by long periods of familial separation provide an opportunity to engage in casual sex with multiple partners and commercial sex workers.2 Recent studies have shown that the HIV prevalence of adults aged 15–49 in the Democratic Republic of Congo (DRC) is lower than the overall sub-Saharan African estimate (1.3% vs. 5.2%).5 However, HIV prevalence among DRC’s most-at risk-populations (MARPs) are significantly higher, which includes sex workers (14.7% in Kinshasa and 23.3% in Lubumbashi) and conflict-afflicted populations (3.1% to 6.7%).1,6–8 Reports documenting the high rates of non-partner sexual violence in mathematical modeling scenarios show the potential for an increase in annual HIV incidence by 7%, impacting up to 10,000 women and girls in the DRC under extreme conditions.9 Past publications have suggested (non-empirically) that the HIV prevalence in the Congolese military could be as high as 60%.10–14 Additionally, reports based on predictions may have overestimated the prevalence of HIV in the Congolese military.10–12,14 These estimates were generated in 1999, while the DRC was actively engaged in a multi-country civil war. In addition, the confidentiality of information regarding the size and structure of the FADRC may contribute to inaccurate estimates of disease prevalence within the military. Estimates of HIV prevalence in African military personnel are limited and inconsistent. Some research has suggested that HIV rates are higher in military populations, while other studies indicate that rates are, instead, comparable to the general population.15,16 The sexual behaviours of soldiers have significant implications for the spread of HIV and other STIs, who appear to be at an increased risk of infection.17,18 Military personnel tend to be young men, spending considerable amounts of time away from home, and have access to a large number of sexual partners, including commercial sex workers and internally displaced women.15,19–21 In a 2008 study of military personnel in Ethiopia, participants self-reported their military background, work-associated travel, sexual history and risk behaviours. Higher military rank, higher numbers of sex partners, and month-long travel in the past year were factors associated with an elevated risk of HIV
International Journal of STD & AIDS 26(3) infection and other STIs compared to those in the general population.2 In a recent survey of Nigerian naval personnel, about 20% of men had sexual contact with a commercial sex worker in the past six months and 40% had not used a condom.22 Studies have also suggested that military personnel are often paid more consistently than other government employees, leading to increased financial stability and the ability to purchase sex, placing them at higher risk of HIV infection.22–24 Preliminary HIV genetic analysis using specimens collected from DRC military personnel suggest high HIV heterogeneity, yet a fairly low prevalence of infection.25 Although these results are similar to previous studies in the general population,26–28 scant data are available on the risk factors and prevalence of STIs, including HIV and reasons behind the high genetic diversity of the disease, in the Armed Forces personnel of the Democratic Republic of Congo (FARDC). Further analysis was conducted to estimate the HIV prevalence in the FARDC and evaluate risk factors associated with HIV and other STIs.
Methods Population selection From June to September 2007, a single-stage 30-cluster sample survey was conducted among active FARDC personnel stationed in Kinshasa. The military population is currently estimated to be 155,000 persons, 2.7% (4185) of which are women, who participate in both administrative roles and in field operations.29 A complete list of companies based in Kinshasa obtained from the Ministry of National Defense was used to randomly select individual companies to serve as study sites. In each selected unit (company), every active duty man and woman (officers and enlisted) was offered enrollment in the study, and informed consent was required for participation. The study protocol was approved by Human Subjects Protection Organisations at both the Kinshasa School of Public Health and United States Army Medical Research and Material Command.
Questionnaire, specimen collection and testing All participants were provided with HIV testing and counseling, and a detailed explanation of the purpose, confidentiality and procedures of the study. Trained interviewers administered a 60-min questionnaire that included socio-demographic characteristics, duration and location of military service, sexual behaviours and self-reported STI symptoms within the past 12 months. Participants were asked to return for their HIV and syphilis test results one week later.
Rimoin et al. Blood samples were processed and separated into buffy coat and plasma on the same day and kept at 20 C at the DRC National AIDS Program Laboratory in Kinshasa. Buffy coat samples conserved at 80 C were used for HIV genetic testing.26 Plasma was tested for HIV antibody following the DRC national testing algorithm; a rapid test (Determine HIV-1/2 from Abbott, IL, USA) followed by an ELISA test (Enzygnost HIV1/2 integral from Dade Behring, Dresden, Germany). Specimens were classified as HIV positive if reactive on both tests. Discordant or indeterminate samples were retested by two ELISA tests, Enzygnost HIV 1/2 and Vironostika (bioMerieux SA, Marcy, l’Etoile, France), and classified as positive if reactive for both of the ELISA tests. Individuals testing positive for HIV and returning for results were referred to the military health centre. Samples were tested for syphilis using the Determine Syphilis rapid test,30 and results were available to participants within 48 h. Individuals testing positive for syphilis infection were treated on site with a single shot of benzathine penicillin G, and referred to a health centre for follow-up.
Statistical analysis and variable selection Data analysis for this paper was conducted using SAS software, version 9.2.31 Participants with missing HIV status or basic data from the questionnaire were excluded from the analysis. Frequency distributions of socio-demographic and behavioural characteristics were calculated for men and women separately. Due to the low number of women participants, data on HIV prevalence for socio-demographic and risk factor subgroups could not be stratified by gender. For variable categorisation, categories found in the 2007 Demographic and Health Survey (DHS) analysis were used when possible – including age group, number of sexual partners and birth region; mobility was defined as number of posts outside Kinshasa during the preceding five years, and questions which were believed to be ambiguous in the original wording of the question were not included for further analysis. Associations between selected variables and HIV infection were first explored with complete case analysis using logistic regression. Best subset selection was used for model selection, after testing a number of other model selection methods, and the multiple imputation method was used to account for missing data (all assumptions were met, and individuals missing data were not significantly different from those not missing data). The final model was analysed using 20 imputations. The final model selected includes variables adjusted for age, gender, time in the garrison, mobility, numbers of sex partners, genital ulcer and active syphilis infection.
189
Results Socio-demographic characteristics A total of 4043 military personnel (2.6% of total estimated military population) were enrolled between June and September 2007; of these, 97% (3919 total, 3735 men, 163 women, and 21 with missing gender data) had questionnaire and laboratory data available for analysis. Participant ages ranged from 18 to 75 years; those in the 30–34 age group comprised 25% of the sample (Table 1). Men tended to have higher rank, to have spent less time in Kinshasa and have a greater number of sexual partners (Tables 1 and 2) compared with women. There were no differences by gender when self-reporting genital ulcer symptoms (9.2% in males, vs. 9.8% in females).
Prevalence of HIV and syphilis Overall HIV prevalence was 3.8%; 48 persons tested positive for HIV infection. HIV prevalence was higher among women (8.0%) compared to men (3.6%) in the study population (aOR: 1.66, 95% C.I. 1.21, 2.28) (Table 3). A total of 463 (11.9%) persons tested positive for syphilis; however, there was no significant difference in prevalence between men and women (11.9 vs. 11.7%, respectively) (Table 2).
Risk factors for HIV infection Univariate odds ratios (ORs) are presented for each variable (Tables 3 and 4). Variables included in the multivariate model were age, gender, military rank, time in Kinshasa garrison, mobility, number of sexual partners, self-reporting of genital ulcer and syphilis infection. When looking at age, participants aged 45–49 had the highest percentage of those testing positive for HIV compared to other age groups (Table 3). Additionally, those stationed for less than one year in the Kinshasa garrison were at highest risk of testing positive for HIV compared to those assigned for longer time periods (Table 3). However, these soldiers were not necessarily new recruits; based on the available data for those in this category (n ¼ 88, data not presented), all had been in the military for at least five years. While the HIV prevalence increased with the number of sexual partners reported in the past 12 months (no partners: 3.4% vs. 5þ partners: 4.2%), there were no significant differences in the adjusted odds ratios (aOR ¼ 1.18, 95% C.I. 0.77, 1.79) for HIV infection (Table 4). After adjusting for other variables, there was a significant association between those reporting a genital ulcer in the past 12 months and HIV infection.
190
International Journal of STD & AIDS 26(3)
Table 1. Socio-demographic characteristics of survey participants (n ¼ 3919). Variable Age Under 20 20–24 25–29 30–34 35–39 40–44 45–49 50þ Missing Grade Senior Officer Junior Officer Noncommissioned Officer (NCO) Enlisted Missing Years of military service
