Herpes Simplex Virus Type 2 (HSV-2) and HTLV-1 & 2 among Female Sex Workers in Ouagadougou, Burkina Faso ()
1. Introduction
Herpes Simplex Virus type-2 (HSV-2) infection is one of the most common worldwide sexually transmitted [1] [2]. In fact, it is implicated in sexually transmitted infections worldwide and is strongly associated with HIV infection [1] [2] [3]. Global and regional estimates of the contribution of HSV-2 infection to HIV incidence reported about 420,000 of 1.4 million sexually acquired incident HIV infections in individuals aged between 15 and 49 years in 2016 were attributable to HSV-2 infection [1]. Authors found that the contribution of HSV-2 to HIV was likely to be greatest in areas where HSV-2 is highly prevalent, particularly in Africa (37.1% as a population attributable fraction (PAF), women (PAF = 34.8%) [1]. Africa is a region with the highest prevalence of HSV-2 [1] [2] [4] [5]. In Malawi, HSV-2 prevalence rose with age in all periods and was higher among women than men, reaching 70% by the age of 40 [4]. Pooled HSV-2 seroprevalence in Sub-Saharan Africa was found to be 37.3% in general populations and high among high risk populations such as female sex workers (62.5%) [2].
Female sex workers are most at risk for sexually transmitted infections. Besides HSV-2, the Human T-lymphotropic virus (HTLV) is one infection with a high risk of sexual transmission. HTLV-1 causes T-cell leukaemia and myelopathy [6] [7]. The other subtypes of HTLV such as HTLV-2 have been identified. The number of HTLV-1-infected people was first estimated between 10 - 20 million people [8], and more recently between 5 - 10 million, even the authors state that this number is likely to be underestimated [9]. From a systematic review conducted in 25 African countries, the HTLV-1 seroprevalence varied from 0 to 17% and that of HTLV-2 from 0 to 4% [8]. In Burkina Faso, about 4% of men who have sex with men (MSM) carried anti-HTLV 1 & 2 antibodies [10].
Little is known about the HSV-2, HTLV-1 and HTLV-2 infections among female sex workers in West Africa in general, and particularly in Burkina Faso. The aim of this study was to estimate HSV-2 and HTLV-1/2 seroprevalence in this subgroup by using archived sera samples in order to inform HIV prevention programs.
2. Materials and Methods
2.1. Study Design and Setting
We screened archived sera from a biological and behavioral cross-sectional study among Female sex workers conducted from February to May 2013 in Ouagadougou, capital of Burkina Faso in West Africa.
2.2. Study Material and Participants
Sera samples were collected from recruited FSWs following these eligible criteria: 1) being at least 18 years old, 2) assigned female sex at birth, 3) having at least 50% of annual income from sex work in the past 12 months, 4) having stayed in the city at least for the past three months, 5) having a valid study coupon and 6) being able to provide informed consent for participation in study activities. Respondent driven sampling (RDS), a peer-driven sampling method designed to reach hidden populations such as FSWs [11] [12], was selected for FSWs recruitment in order to collect rigorous, and representative data. RDS starts out with recruitment “seeds” that are used to create chains of individuals and can be adjusted for in regression models. Five seeds were selected on purpose and recruited based on diverse socio-demographic selection criteria, including popularity, sociability, age, location, type of sex work and nationality, with the assumption that each individual represented a different social network within the female sex worker population as a whole in each site. After giving informed consent, seeds were invited to complete a behavioural questionnaire and blood sampling for HIV and syphilis testing. These seeds were each provided with three coded coupons which were valid for four weeks, to recruit peer FSWs from their social network. This process continued until the target sample size was reached. In order to avoid individuals participating multiple times, a single study office was used in addition to the use of a unique identification code. Full details of the study methodology have been previously described elsewhere [13].
2.3. Sample Size
The sample size was previously calculated to recruit 345 FSWs for the primary HIV seroprevalence study. Sample size calculations were based on the assumption that populations who always use condoms, have a 75% lower HIV prevalence than populations who do not, and the effectiveness of condoms is roughly 80%, with 73% as a conservative estimate [14]. HIV prevalence was estimated at 15% with a 19% among those who did not consistently use condoms [15] [16]. A design effect of 1.5 associated with respondent driven sampling, a significance level of 0.05 and a power of 80% were employed.
2.4. Data Collection
After informed consent, each participant completed private behavioral interviewer-administered questionnaires conducted in French or the local language. Topics included demographic and socio-economic characteristics, sexual partnership and behavior, knowledge, attitudes and practices towards sexual transmitted infections and HIV, condom use during the last 12 months. Pre-and post-test HIV and syphilis counseling, was conducted for all participants after completion of the behavioral questionnaire. Venous blood specimens were collected from each consenting participant for HIV testing, and frozen at −20˚C.
2.5. Laboratory Methods
Venous blood specimens were collected and HIV and syphilis tests were performed directly in the study site. After these tests, anonymized sera were stored at the IRSS biomedical research laboratory with participant additional consents for further infections testing. All frozen samples were returned to laboratory temperature before testing. Serum samples were tested using Enzyme-Linked Immuno-Sorbent Assay (ELISA) methods for the measurement of IgG antibodies to HSV type 2 (Diagnostic BioProbes Srl, Italy), and Anti-HTLV1 & 2 Antibodies were tested by ELISA HTLV I & II Ab-DiaPro ULTRA version (Diagnostic BioProbes, Srl. Italy). All tests were performed according to manufacturer’s instructions.
2.6. Data Processing
Data were entered using EpiData 3.1 (The EpiData Association, Odense, Denmark) (and exported into Stata 14 (StataCorp, College Station, TX) for analysis.
Descriptive statistics were used to describe participants’ characteristics, HSV-2 and HTLV 1 & 2 seroprevalences. All proportions were adjusted to account for the RDS method. This adjustment takes into consideration the probability of each participant to be included in the study. We present population estimates and 95% confidence intervals (CI) adjusted for RDS design using the RDS Analysis Tools (RDSAT) version 6.0.1 (RDS, Inc., Ithaca, NY).
2.7. Ethical Issues and Protection of the Participants
The study received ethical approval from the Ethics Committee for Health Research (CERS) of Burkina Faso. In addition to the consent for participation to the HIV behavioral survey, individual consent was obtained for serum samples storage for further research related to sexual transmitted diseases.
3. Results
3.1. Socio-Demographic Characteristics of Study Participants
A total of 348 et 333 FSWs were included for HSV-2 testing and in this analysis. The mean age of the study participants was 24.9 ± 6.4 years. Table 1 shows the socio-demographic and socio-professional characteristics of the female sex workers (FSWs). About 23.8% had no formal education, and one third of them had a primary level education (38.1%). More than 63% of the FSWs in the sample were single. The vast majority of the FSWs (about 70%) had at least one
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Table 1. Characteristics of study participants.
biological child. Half of the FSWs (50.4%) declared to have no other income generating activity (except for sex work).
3.2. HSV-2 Seropravelence
More than three-quarters of FSWs were positive for HSV-2 antibodies (75.7%, 95% CI: 70.8 - 79.9). HSV-2 seroprevalence ranged from 69.3% among FSWs under 24 years old to 88.5% among those who were at least 30 years old. Furthermore, HSV-2 seroprevalence was high among FSW with no formal education (87.7%) and decreased significantly among those with at least primary education (76.0%) and those with secondary education and above (64.9%). In bivariate analysis, factors associated with HSV-2 were aged, education, the number of children, ever be pregnant. In multivariate analysis, only none of formal education was independently associated with the HSV-2 among FSWs (Table 2).
3.3. HTLV-1 & 2 Seroprevalence
Table 3 shows that 11.2% (95% CI: 08.3 - 15.1) of FSWs in Ouagadougou were positive for HTLV-½. By age groups, 11.8% were positive among those under 25 years of age; 15.2% among those 25 to 29 years old, and 5.8% among those over 30 years of age. Although there were variations according to some socio-demographic and socio-professional characteristics, the differences observed were not statistically significant in multivariate analysis, except for FSWs who have experienced condom torn in the last 12 months (aOR = 0.39, p = 0.018).
4. Discussion
The purpose of this study was to estimate the HSV-2 and HTLV-1/2 seroprevalence among FSWs. It shows a high seroprevalence of HTLV-1/2 (11.2%), but especially of HSV-2 antibodies (76%) among FSWs, thus confirming their vulnerability to this infection. Indeed, HSV-2 infection is one of the most common sexually transmitted infections and the leading cause of genital ulceration worldwide [1] [17] [18]. Its prevalence is not uniform, with some populations being more affected than others depending on risk factors [5] [19].
The global prevalence of HSV-2 infection has been estimated at 11.3% in the
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Table 2. HSV-2 seroprevalence and associated factors among female sex workers.
general population aged between 15 and 49 years compared to 31.2% in the sub-Saharan African population [5]. The high prevalence of HSV-2 found in our study population is not, however, uncommon. In Uganda, the prevalence of HSV-2 in the female population was estimated at 69.3% in Rakai district [20], and 63.8% in Kampala [21]. Among FSWs, studies conducted in Kenya [22] and Tanzania [23] reported that 79% and 69% respectively were infected with HSV-2. Furthermore, as in our study, the positive association between HSV-2 infection and the age is established by several authors [22] [24] [25]. The increase in the prevalence of HSV-2 with age could be explained by the chronic nature of the infection, which is generally contracted at the beginning of sexual activity in young individuals, can be latent for a long time and reappear periodically, but also due to the accumulation of risk during sex work [26]. Of the factors
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Table 3. HTLV - 1 & 2 seroprevalence and associated factors among female sex workers.
tested after adjustment, only the modalities of the formal education variable were associated with HSV-2 infection. Indeed, by keeping the other variables of the model constant, FSWs with a primary level and a secondary level and above have a risk reduction of 69% and 78% respectively of being infected with HSV-2. This reduction is statistically significant at the 5% level.
HTLV-1 & 2 are endemic in Africa, and particularly affect certain populations at risk. In our study, 11.2% of FSWs were positive for HTLV-1 or 2, which is 10 to 15 times higher than what was reported among pregnant women and blood donors in Nouna (1.4%) and Ouagadougou (0.5%) [27]. In Nigeria, Forbi and Odetundé in a study published in 2007 estimated the prevalence of anti HTLV-1 & 2 antibodies in FSWs to be 22.9% while it was 16.7% among pregnant women [28]. The extent of HTLV infection among FSWs is of particular concern because the vast majority (90%) of those infected with these viruses remains asymptomatic and unaware of their infection status [29] [30]. This could sustain the transmission of the infection from one person to another, especially in a context where screening for this infection is almost non-existent. Due to the lack of a vaccine against HTLV-1 & 2 and the difficulties in managing late complications, including highly lethal leukemic cancer, prevention of transmission remains the best solution [29] [31] [32] [33]. Among sexually active populations such as FSWs, emphasis should be placed on prevention of sexually transmitted infections, including consistent condom use [34]. However, awareness of these non-HIV retroviruses in at-risk communities will need to be increased for more precautionary measures as condoms provide only partial protection. Curiously, for HTLV1 & 2, among the factors used for adjustment, only the variable “condom torn in the last 12 months” was associated with seroprevalence (p = 0.018) compared to those whose condom used in the last 12 months was not torn. Since condoms are used to protect from sexually transmitted infections, this result may be related to participant self-reporting, which we are not able to verify.
The main limitation of our study is that the data are based on serum samples collected several years earlier. However, the use of archived samples was an interesting alternative to provide information on HSV-2 and HTLV 1 & 2 seroprevalence in the population of FSWs. Furthermore, our study provides the first data on HTLV 1 & 2 and HSV-2 seroprevalence in FSWs in Burkina Faso. These data fill a gap and will contribute to the mapping of HSV-2 and HTLV 1 & 2 epidemiology among high-risk populations in Africa.
5. Conclusion
Herpes Simplex Virus-type 2 and Human T-lymphotropic virus 1 & 2 infections are very common among female sex workers, which confirms the need for effective preventive interventions. In absence of a vaccine against these two viruses, prevention of sexual transmission through sexual education and early screening, followed by treatment, mainly for HSV-2, should be considered for female sex workers.
Acknowledgements
The authors would like to acknowledge the entire Female Sex Workers community in Ouagadougou for their participation in the present study, the facilitators and the data collectors, the Permanent Secretary of the National Council against AIDS and STIs (SP/CNLS-IST) of Burkina Faso, AIDSETI-network of Burkina and especially the Zoodo Health center of Ouagadougou, ant the Research To Prevention (R2P) team.