Seroprevalence and risk factors for HIV, HCV, HBV and syphilis among blood donors in Mali

Background HIV, HBV and HCV remain a global public health concern especially in Africa. Prevalence of these infections is changing and identification of risk factors associated with each infection in Mali is needed to improve medical care. Methods We conducted a cross-sectional study of all individuals donating blood (n = 8207) in 2018 to the blood bank at university hospital in Bamako, Mali, to assess prevalence and risks factors associated with HIV, HBV, HCV and syphilis infections. Results HIV-seroprevalence was 2.16% and significantly increased with age, being married and decreasing education level. In multivariate analysis, after adjustements with age, marital status and geographical setting, only education level was associated with HIV-infection (OR, 1.54 [95% CI, 1.15–2.07], p = 0.016). HBsAg prevalence was 14.78% and significantly increased with to be male gender. In multivariate analysis, adjusting for age, marital status and type of blood donation, education level (OR, 1.17 [95%CI, 1.05–1.31], p = 0.02) and male gender (OR, 1.37 [95%CI, 1.14–1.65], p = 0.005) were associated with HBV-infection. HCV-prevalence was 2.32% and significantly increased with living outside Bamako. In multivariate analysis, adjusting for gender, age and education level, living outside Bamako was associated with HCV-infection (OR, 1.83 [95% CI, 1.41–2.35], p < 0.001). Syphilis seroprevalence was very low (0.04%) with only 3 individuals infected. Contrary to a prior study, blood donation type was not, after adjustments, an independent risk factor for each infection. Conclusions Overall, HIV and HBV infection was higher in individuals with a lower level of education, HBV infection was higher in men, and HCV infection was higher in people living outside of Bamako. Compared to studies performed in 1999, 2002 and 2007 in the same population, we found that HIV and HCV prevalence have decreased in the last two decades whereas HBV prevalence has remained stable. Our finding will help guide infection prevention and treatment programs in Mali.


Background
Human Immunodeficiency virus (HIV), Hepatitis B virus (HBV) and Hepatitis C virus (HCV) infections remain a global public health concern especially in Africa [1,2]. West and central Africa region accounts for 21% of the world's new HIV-infections and 30% of global deaths from AIDS-related illness [3]. Both the rate of new HIVinfections and the burden of HIV remain high in western and central Africa. The incidence prevalence ratio in the region has changed little since 2010, it stood at 0.06 [0.04-0.09] in 2017, twice as high as the epidemic transition benchmark of 0.03 [3]. Deaths from AIDS-related illness in the region have declined by nearly a quarter since 2010, and annual new HIV-infections declined by 8%. Cameroon, Ivory Coast and Nigeria together accounted for approximately 71% of new HIV-infections in the region in 2017 [3]. The World Health Organization (WHO) estimated that globally in 2015, viral hepatitis led to 1.34 million deaths and 96% were the results of complication of chronic HBV (66%) and HCV (33%) infections [4]. In African region, prevalence of this two virus infections was respectively 6.1% (about 60 million people) and 1% (about 11 million people) [4]. In 2019, Hepatitis Scorecard 2019 for WHO Africa Region reported HBV and HCV prevalence for various countries located in West Africa: Nigeria 5.5 and 2.1%, Ivory Coast 6.1 and 1.7%, Cameroon 4.4 and 0.7% or Mali 8.5 and 3.1% respectively [5]. Otherwise, Syphilis prevalence in Africa varies according to population study; among blood donors in Nigeria prevalence was 3.1% [6] whereas in a population of men who have sex with men (MSM) living in Burkina Faso, 6.1% were tested positive for Treponema pallidum antibodies [7].
Previous studies including blood donors from Bamako reported that HIV and HBV prevalence were respectively 4.5 and 14.9% in 2002 and 2.6 and 13.9% in 2007 [8,9], HCV prevalence was 4% in 1998/1999 and 3.3% in 2007 [9,10] and Syphilis infection prevalence was 0.3% [9]. This cross-sectional study aimed to estimate recently HIV, HBV, HCV and syphilis infections from blood donors in Bamako, Mali and to identify risk factors associated with each infection because no data are available yet.

Study population
We conducted a cross-sectional study of individuals donating blood from January 1st 2018 and December 31st 2018 to the blood bank of Gabriel Toure University teaching hospital in Bamako, Mali. We aimed to estimate HIV, HBV, HCV and syphilis infection prevalence and risk factors of blood donors during this time. The current study included all blood donations during 2018 (n = 8207) and respecting blood donation criteria: age between 18 and 60 years, body weight above 55 kg and physically healthy. Excluded from donation were individuals with known chronic diseases, high blood pressure, anemia, not transfused in the last 10 years, not hospitalized in the last 3 months, and not addicted to intravenous or oral drugs.
For each blood donor, socio-demographic data including age, marital status, education level, geographical setting and type of blood donation (volunteer or parental) were collected during a predonation examination.

HIV, HBV, HCV and syphilis testing
To assure the safety of blood products transfused to patients at Gabriel Toure teaching hospital, all donations are analyzed for HIV-1/HIV-2 antibodies, HCV antibodies, hepatitis B surface antigen (AgHBs) and T. pallidum (TPHA/VDRL). Testing was performed on blood tubes taken after each donation, and consisted of the measurement of antibodies for HIV-1 and HIV-2 (Genscreen VIH1/2 version 2, BioRad, France), HCV (Murex, Abbott, France), hepatitis B surface antigen (HBsAg) (Monolisa AgHBS plus, BioRad, France) and T. pallidum (VDRL). All initial positive results were confirmed by performing of a second test using the same assay on a blood sample from a second phlebotomy. Confirmatory or supplemental testing, such as western blot for HIV, was not performed since such testing is not practice in the blood donation algorithm in Mali. Thus, data for these analyses were obtained from individual blood donors who had infection testing performed as part of routine practice to screen the blood supply at this hospital in Mali.

Statistical analysis
Continuous variables were described with median and interquartile range [IQR] and categorical variables as number and percentages. The prevalence of HIV, HBV and HCV was expressed with a 95% confidence interval (CI95%) and group's comparison was performed using Chi-2 test for categorical variables. Univariable and multivariable (including gender, age, education level (none, primary school, secondary school, higher), marital status, geographical setting and type of blood donation covariates) logistic regression analyses were performed with R (v3.6.1) [11] software to identify risk factors of each infection. Factors associated with HIV, HBV or HCV infection with a P value of < 0.20 in the univariate logistic regression analyses were included in the multiple logistic regression model. The level of significance for each analysis was set at 0.05. HIV, HBV and HCV prevalence HIV-seroprevalence was 2.16% (95% CI: 1.86-2.50) with no significant difference between men (2.15%) and women (2.22%) (p = 0.90). HIV-prevalence increased with age (p = 0.06), from 1.86% in the youngest category (18-30 years old) to 3.40% in the oldest (> 50 years old). HIV-prevalence also varied by marital status, with a significantly higher prevalence for those who were married (2.42%) compared to single (1.54%) (p = 0.013). People living in Bamako also tended to have lower HIVprevalence than those living in surrounding areas (2.00% versus 2.66%, respectively) (p = 0.08). Otherwise, higher HIV-seroprevalence was observed with decreasing education level (p = 0.0024). None of the voluntary donors were HIV-infected (p = 0.05) ( Table 1).

Syphilis prevalence
Only 3 (0.04%, [95% CI, 0.01-0.11]) blood donors tested positive for syphilis. All were men, younger than 30 years and parental donors. Two were single and lived in Bamako. One of them was co-infected with HIV.

Risk factors associated with HIV, HBV and HCV infections
Univariate and multivariate logistic regression analyses were performed to assess independent associations between socio-demographic data and HIV, HBV or HCV infections. In univariate analysis, HIV was significantly associated with being married (odds ratio [

Discussion
This cross-sectional study aimed to measure prevalence and risk factors for HIV, HBV, HCV, and syphilis infections from blood donors in Bamako, Mali.
HIV-seroprevalence was independently associated with a decreasing education level as has been observed in prior studies from several regions of the world [12]. Prior research suggests that knowledge about HIV/AIDS increases with both level and quality of education [12,13], and consequently, higher education level has been associated with less HIV/AIDS risk taking behavior [14]. For example, a study reported that for every additional year in education, there was greater use of condoms [14]. Conversely, low education level was associated with higher likelihood of engaging in transactional sex (drugs or money), as well as neighbor's education level, and thus increased HIV acquisition risk [15]. HBVprevalence was higher in men and blood donors with educational level lower than secondary school. Similar results were reported in Burkina Faso where HBV-seroprevalence was significantly higher in men than in women (10.5% vs 7.8%) [16]. This finding could be due to better access to HBV vaccination for women accessing medical care during pregnancy. But it may also related to different T-cell immunity between gender; indeed, women were reported to exhibit greater humoral and cell-mediated responses to antigenic stimulation, vaccination and infection than do men [17]. We also found that HCV was more prevalent in blood donors living outside of Bamako; this could be related to unsafe non aseptic practices putting individuals in rural areas at risk for HCV such as female excision (removal of a part or entire clitoris), circumcision or cultural scarification as previously reported in others African countries [18] but probably not linked to injection drugs users mainly present in the center of Bamako. None of these specific factors were assessed in this study and further investigation should be undertaken to completely assess HCV epidemiology and transmission knowledge in Mali. Finally as expected, syphilis prevalence was very low with Although sexual orientation was not collected in our study, a recent study performed in Burkina Faso reported that the prevalence of syphilis among MSM was also low and comparable to that of other reproductive age individuals, suggesting that public health intervention programs were effective [7]. Although HIV-prevalence was significantly higher in parental donors compared to volunteer donors (2.20 vs 0.00, p = 0.05), HBV and HCV prevalence were not different between the parental and voluntary donors (14.69 vs 18.75, p = 0.15 and 2.33 vs 1.88, p > 0.99, respectively) and in multivariate analysis, parental donor was not associated with any of these infections. A prior study performed in the National Centre for Blood Transfusion (CNTS) of Mali located in Bamako reported higher prevalence of HIV and HBV in parental blood donors suggesting that number of regular, volunteer blood donors should be increased [9]. However, they didn't perform multivariate logistic regression analysis and thus blood donation type should not be considered as an independent risk factor for each infection.
HIV, HBV and HCV prevalence were previously evaluated in a blood donor population from CNTS of Bamako in 1999, 2002 and 2007 [8][9][10] (Fig. 1) [19], as this program was not fully initiated in Mali until 2010. Thus, the benefit of widespread childhood HBV vaccination is not yet evident. As with HIV-prevalence, HCV prevalence also decreased in the last two decades, from 4% in 1999, to 3.3% in 2007 and 2.28% in 2018. This decrease can likely be attributed to the systematic screening of all blood donors for HCV since 2004 but also by the initiation of HIVinfection prevention and treatment program since 2001, whose transmission route is similar to HCV-infection.