The Open Virology Journal




ISSN: 1874-3579 ― Volume 13, 2019
RESEARCH ARTICLE

Hepatitis B, C and Delta Viruses’ Infections and Correlate Factors Among Female Sex Workers in Burkina Faso, West-Africa



Henri G. Ouedraogo1, 2, 3, *, Seni Kouanda1, 3, Sara Goodman4, Hermann Biènou. Lanou1, Odette Ky-Zerbo5, Benoît C. Samadoulougou5, Charlemagne Dabire1, Modibo Camara1, Yves Traore2, Stefan Baral4, Nicolas Barro2
1 Department of Institut de Recherche en Sciences de la Santé (IRSS), Ouagadougou, Burkina Faso, West Africa
2 Department of University Ouaga1 Prof. Joseph Ki-Zerbo, Ouagadougou, Burkina Faso, West Africa
3 Department of Institut Africain de Santé Publique, Ouagadougou, Burkina Faso, West Africa
4 Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
5 Programme d’Appui au Monde Assiciatif et Communautaire (PAMAC), Ouagadougou, Burkina Faso, West-Africa

Abstract

Background:

Female Sex Workers (FSW) have increased vulnerability to viral hepatitis B, C and D transmission. Our study aimed to assess the seroprevalence of hepatitis B, C and D viruses and their associated factors among FSW in Ouagadougou, Burkina Faso.

Methods:

This is a cross-sectional study among FSW at least 18 years old in Ouagadougou, Burkina Faso. Data were collected from February 2013 to May 2013 using Respondent-Driven Sampling (RDS). Hepatitis B, C, and D tests were performed on FSW storage serums using fourth generation ELISA kits. Survey-weighted bivariate and multivariate logistic regression analyses were performed using Stata version 14 to identify factors associated with viral hepatitis infections.

Results:

Population-weighted prevalence of viral hepatitis infections in FSW was respectively 18.2% (95%CI: 14.4-22.9) for Hepatitis B Virus (HBV), 10.6% (95%CI: 07.5-14.8) for Hepatitis C Virus (HCV) and 1.5% (95Cl: 0.2-10.3) for Hepatitis D Virus (HDV). Factors independently associated with HCV include positive HIV status, inconsistent condom use during the last 12 months, condom reuse with clients, sex with clients in the street, bars or public gardens. No sociodemographic or behavioral factors were independently associated with HBV infection.

Conclusion:

The prevalence of HBV and HCV was high among FSW and the prevalence of HDV was relatively low in this group in Burkina Faso. These findings suggest urgent and comprehensive prevention of these viruses through education for safer sex and behaviors, and immunization against HBV for FSW.

Keywords: HBV, HCV, HDV, Female sex workers, Burkina faso, Respondent-driven sampling.


Article Information


Identifiers and Pagination:

Year: 2019
Volume: 13
First Page: 9
Last Page: 17
Publisher Id: TOVJ-13-9
DOI: 10.2174/1874357901913010009

Article History:

Received Date: 4/11/2018
Revision Received Date: 21/12/2018
Acceptance Date: 20/1/2019
Electronic publication date: 28/03/2019
Collection year: 2019

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© 2019 Ouedraogo et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Department Biomedical and Public Health Department, Institut de Recherche en Sciences de la Santé (IRSS), 03BP7192, Ouagadougou, Burkina Faso, West-Africa.; E-mail: gouedraogo@irss.bf





1. BACKGROUND

Viral hepatitis is a major global health problem despite the existence of preventive measures. According to WHO, more than 257 million people are infected by Hepatitis B Virus (HBV) worldwide. HBV mortality counts in 2015 totaled approximately 887,000 due to liver cancer and cirrhosis [1WHO. Global hepatitis report, 2017. Geneva: World Health Organization. Report No: ISBN 978-92-4-156545-5 2017; 83.]. Hepatitis D Virus (HDV) is unique because it requires HBV to survive in the human body [2Alvarado-Mora MV, Locarnini S, Rizzetto M, Pinho JR. An update on HDV: virology, pathogenesis and treatment. Antivir Ther (Lond) 2013; 18(3 Pt B): 541-8.
[http://dx.doi.org/10.3851/IMP2598] [PMID: 23792471]
]. It is estimated that globally, more than 5% of the people infected by the HBV are also infected by the HDV [3Rizzetto M, Hepatitis D. Virus: Introduction and Epidemiology. Cold Spring Harb Perspect Med 2015; 5(7): a021576.https:// www.ncbi.nlm.nih.gov/ pmc /articles/ PMC4484953/
[http://dx.doi.org/10.1101/cshperspect.a021576] [PMID: 26134842]
]. Hepatitis C Virus (HCV), affects 71 million people and causes 399,000 deaths every year from hepatocellular carcinoma and cirrhosis [1WHO. Global hepatitis report, 2017. Geneva: World Health Organization. Report No: ISBN 978-92-4-156545-5 2017; 83.]. HBV, HCV, and HDV viruses are endemic in Sub-Saharan Africa [1WHO. Global hepatitis report, 2017. Geneva: World Health Organization. Report No: ISBN 978-92-4-156545-5 2017; 83., 4Spearman CW, Afihene M, Ally R, et al. Hepatitis B in sub-Saharan Africa: Strategies to achieve the 2030 elimination targets. Lancet Gastroenterol Hepatol 2017; 2(12): 900-9.
[http://dx.doi.org/10.1016/S2468-1253(17)30295-9] [PMID: 291327 59]
]. In a systematic review, the authors estimated the seroprevalence of HBV virus in Sub-Saharan Africa to be 8.83% (95%CI:8.82 -8.83) compared to 3.61% (95%CI: 3.61-3.61) globally [5Schweitzer A, Horn J, Mikolajczyk RT, Krause G, Ott JJ. Estimations of worldwide prevalence of chronic hepatitis B virus infection: A systematic review of data published between 1965 and 2013. Lancet 2015; 386(10003): 1546-55.http:// linkinghub.elsevier.com/ retrieve/ pii/ S014067361561412X
[http://dx.doi.org/10.1016/S0140-6736(15)61412-X] [PMID: 262314 59]
]. Hepatitis D virus prevalence in the West African population was estimated to be 7.33% (95% CI 3·55-12·20) [6Stockdale AJ, Chaponda M, Beloukas A, et al. Prevalence of hepatitis D virus infection in sub-Saharan Africa: A systematic review and meta-analysis. Lancet Glob Health 2017; 5(10): e992-e1003.https:// www.ncbi.nlm.nih.gov/ pmc/ articles/ PMC5599428/
[http://dx.doi.org/10.1016/S2214-109X(17)30298-X] [PMID: 289117 65]
]. In another systematic review on HCV epidemiology in 33 Sub-Saharan African countries, the overall seroprevalence of the infection was estimated to be 2.98% (95% CI 2.86-3.10), and speci-fically to be 4.34% (95%CI:3.99-4.70%) in West Africa [7Rao VB, Johari N, du Cros P, Messina J, Ford N, Cooke GS. Hepatitis C seroprevalence and HIV co-infection in sub-Saharan Africa: A systematic review and meta-analysis. Lancet Infect Dis 2015; 15(7): 819-24.
[http://dx.doi.org/10.1016/S1473-3099(15)00006-7] [PMID: 259570 78]
].

HBV and HDV are transmitted among adults through blood and sexual intercourse. Although HCV transmission is mainly transmitted through blood, the literature reports indicate increasing sexual transmission, notably through traumatic sexual intercourse [8Rooney G, Gilson RJ. Sexual transmission of hepatitis C virus infection. Sex Transm Infect 1998; 74(6): 399-404.
[http://dx.doi.org/10.1136/sti.74.6.399] [PMID: 10195047]
-10Terrault NA, Dodge JL, Murphy EL, et al. Sexual transmission of hepatitis C virus among monogamous heterosexual couples: The HCV partners study. Hepatology 2013; 57(3): 881-9.
[http://dx.doi.org/10.1002/hep.26164] [PMID: 23175457]
]. FSW are a known group of high-risk for sexually transmitted infections [11Pitpitan EV, Kalichman SC, Eaton LA, Strathdee SA, Patterson TL. HIV/STI risk among venue-based female sex workers across the globe: A look back and the way forward. Curr HIV/AIDS Rep 2013; 10(1): 65-78.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3567216/
[http://dx.doi.org/10.1007/s11904-012-0142-8] [PMID: 23160840]
], including HBV, HCV, and HDV [12Puga MAM, Bandeira LM, Weis SMDS, et al. High-risk behaviors for hepatitis B and C infections among female sex workers. Rev Soc Bras Med Trop 2018; 51(2): 198-202.http:// www.scielo.br/ scielo.php?script = sci _ abstract & pid = S0037-86822018000200198 & lng=en & nrm=iso & tlng = en
[http://dx.doi.org/10.1590/0037-8682-0231-2017] [PMID: 29768553]
]. Failure to use condoms, having multiple sexual partners, sexual violence, and co-infections with other sexually transmitted infections increase the risk of acquisition and transmission of hepatitis B, D, and C viruses [12Puga MAM, Bandeira LM, Weis SMDS, et al. High-risk behaviors for hepatitis B and C infections among female sex workers. Rev Soc Bras Med Trop 2018; 51(2): 198-202.http:// www.scielo.br/ scielo.php?script = sci _ abstract & pid = S0037-86822018000200198 & lng=en & nrm=iso & tlng = en
[http://dx.doi.org/10.1590/0037-8682-0231-2017] [PMID: 29768553]
-15Niama FR, Loukabou Bongolo NC, Mayengue PI, et al. A study on HIV, syphilis, and hepatitis B and C virus infections among female sex workers in the Republic of Congo. Arch Public Health 2017; 75: 21. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5421326/
[http://dx.doi.org/10.1186/s13690-017-0189-5] [PMID: 28503303]
]. Research on HBV and HCV, especially related to risky sexual behavior including sex work remains poorly studied in West Africa. In order to better understand the epidemiology of HBV, HCV, and HDV among FSW, the prevalence and associated risk factors related to HBV, HCV, and HDV infections were evaluated in this group in Ouagadougou.

2. METHODS

2.1. Study Design and Participants

We conducted a cross-sectional study among FSW. Participants were recruited through Respondent Driven Sampling (RDS) [16Heckathorn DD. Respondent-Driven sampling: A new approach to the study of hidden populations. Soc Probl 1997; 44: 174-99. http://www.jstor.org/stable/3096941
[http://dx.doi.org/10.2307/3096941]
, 17McCreesh N, Copas A, Seeley J, et al. Respondent driven sampling: Determinants of recruitment and a method to improve point estimation. In: Eisele T, Ed. PLoS ONE [Internet] 20138 [cited 2016 Aug 4];: e78402. http://dx.plos.org/10.1371/journal.pone.0078402]. Inclusion criteria were: (1) age not less than 18 years, (2) assigned female sex at birth, (3) having at less 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 and (7) providing additional consent for serum storage and use in other studies.

2.2. Study Setting

This study was carried out in Ouagadougou, the capital of Burkina Faso in West Africa. Ouagadougou is the largest city in Burkina Faso, located in the center of the country with a population estimated at more than 2.8 million inhabitants. From the respondent-driven sampling, the number of FSW in this city was estimated at 4988 (95% CI: 2856-7120) in 2013 [18Holland CE, Kouanda S, Lougué M, et al. Using population-Size estimation and Cross-sectional survey methods to evaluate HIV service coverage among key populations in burkina faso and togo. Public Health Rep 2016; 131(6): 773-82.
[http://dx.doi.org/10.1177/0033354916677237] [PMID: 28123223]
].

2.3. Participant Recruitment

Study participants were recruited via Respondent-Driven Sampling (RDS), a peer-driven sampling method designed to reach hidden populations [19Heckathorn DD. Respondent-Driven sampling II: Deriving valid population estimates from Chain-Referral samples of hidden populations. Soc Probl 2002; 49: 11-34. https:// academic.oup.com/ socpro/ article-lookup/ doi/ 10.1525/ sp.2002.49.1.11
[http://dx.doi.org/10.1525/sp.2002.49.1.11]
, 20Heckathorn Douglas D. Respondent-Driven sampling: A new approach to the study of hidden populations. Univ Calif Press Behalf Soc Study Soc Probl 1997; 44: 174-99.]. RDS begins with recruitment “seeds” that are used to create chains of individuals and can be adjusted for in regression models. Five seeds were selected purposively 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 FSW population as a whole in each Ouagadougou. After giving informed consent the recruitment seeds completed a demographic and 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 FSW from their social network. This process continued until the target sample size was reached.

To avoid multiple inclusions, a single survey office was used. At the study site, there was a manager (screener), two data collectors, an HIV test counselor, a lab technician and all of them were trained. Full detail of the study methodology has been previously described [21Wirtz AL, Schwartz S, Ketende S, et al. Sexual violence, condom negotiation, and condom use in the context of sex work: Results from two west african countries. JAIDS J Acquir Immune Defic Syndr [Internet] 201568 [cited 2016 Jun 23];: S171-9. Available from: http://content.wkhealth.com/linkback/openurl?sid=WKPTLP:landingpage&an=00126334-201503011-00014].

2.4. Sample Size Calculation

Sample size calculations were based on the assumption that populations that always use condoms have a 75% lower prevalence than populations who do not, and the effectiveness of condoms is roughly 80%, with 73% a conservative estimate [22Weller S, Davis K. Condom effectiveness in reducing heterosexual HIV transmission. Cochrane Database Syst Rev 2002; (1): CD003255.
[PMID: 11869658]
]. Overall, HIV prevalence was estimated at 15% with a 19% prevalence among those who did not consistently use condoms [23Nagot N, Ouangré A, Ouedraogo A, et al. Spectrum of commercial sex activity in Burkina Faso: Classification model and risk of exposure to HIV. J Acquir Immune Defic Syndr 2002; 29(5): 517-21.
[http://dx.doi.org/10.1097/00042560-200204150-00013] [PMID: 119 81369]
, 24Lankoandé S, Meda N, Sangaré L, et al. Prevalence and risk of HIV infection among female sex workers in Burkina Faso. Int J STD AIDS 1998; 9(3): 146-50.
[http://dx.doi.org/10.1258/0956462981921909] [PMID: 9530899]
], A design effect of 1.5 associated with RDS, and a significance level of 0.05 and a power of 80% were employed. The necessary sample size to achieve the significance level and power was 345 FSW.

2.5. Data Collection and HIV and Syphilis Testing

Data were collected from February to May 2013 in Ouagadougou. 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 partnerships and behavior, knowledge, attitudes and practices towards sexual transmitted infections and HIV, condom use during the last 12 months. Venous blood specimens were collected from each consenting participant for testing. Pre-and post-test HIV and syphilis counseling, was conducted for all participants after completion of the behavioral questionnaire. Male condoms, condom compatible lubricants, HIV and STIs prevention and educational material, and information regarding existing health and behavioral ser-vices were provided to all study participants.

2.6. Laboratory Methods

HIV and syphilis tests were performed in the study office using the rapid screening procedure for both tests (HIV and syphilis). After these testing in situ, anonymized serums were storage with participant additional consent for further infections testing like HBV, HDV, and HCV. Storage serum samples were tested by Enzyme Linked Immunoassay (ELISA) methods for determination of Hepatitis B surface antigen “ELISA HBsAg ULTRA-Dia.Pro 4th generation (Diagnostic BioProbes Srl, Italy)”. HBsAg reactive samples were subsequently tested for the antibodies anti-hepatitis D virus using competitive ELISA HDV Ab - Dia.Pro (Diagnostic BioProbes Srl, Italy). For antibody anti-hepatitis C virus, the Fourth generation ELISA “HCV Ab-Dia.Pro (Diagnostics BioProbes Srl, Italy) was used. All tests were performed according to the manufacturer’s procedures and equivocal samples were retested and the result of the second test was accepted.

2.7. Data Processing and Analysis

Data were entered using double data entry into EpiData 3.1 (EpiData Association, Odense, Denmark), and analyzed with Stata 14 (StataCorp, College Station, TX). Descriptive statistics were used to describe FSW characteristics, sexual behaviors, condom use, HBV, HDV and HCV prevalence. We adjusted all proportions to account for the RDS method [25Tiffany JS. Respondent-driven sampling in participatory research contexts: Participant-driven recruitment. J Urban Health 2006; 83(6)(Suppl.): i113-24. http:// link.springer.com/ 10.1007/ s11524 - 006 - 9107-9
[http://dx.doi.org/10.1007/s11524-006-9107-9] [PMID: 16933100]
]. This adjustment takes into consideration the probability of each participant to be included in the study. This probability was measured through weighting based on the size of each participant’s network. This probability was measured through weighting based on the size of each participant’s network. Network size was determined using the survey question: “How many different people do you know personally who are female sex workers or sell sex? i.e., you know them and they know you, and you could contact them if you needed to?” The mean network size was 69 FSW (95%CI: 54-84). We presented 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). Weighted bivariate and multivariate logistic regression analyses were performed using Stata to identify factors associated with HBV and HCV infections at the p<0.05 level of significance along with a 95% Confidence Interval (CI). The outcome variable was HBV or HCV status (positive or negative) as determined by blood tests. Bivariate analysis was not done for hepatitis D due to a limited number of positive cases. Predictor variables included sociodemographic variables such as age, education level, marital status, employment, and migration to Burkina Faso. Other selected predictor variables included: years of sex work experience, number of clients, and condom use, venues for sex work (sex with clients in street or public gardens), drug abuse, and alcohol abuse. Sociodemographic and selected behavioral variables associated with hepatitis virus B or C infection at the significance level of p<0.2 [26Sperandei S. Understanding logistic regression analysis. Biochem Med (Zagreb) 2014; 24(1): 12-8. https:// www.ncbi.nlm.nih.gov/ pmc/ articles/ PMC3936971/
[http://dx.doi.org/10.11613/BM.2014.003] [PMID: 24627710]
-28Comparison of Stopping Rules in Forward Stepwise Discriminant Analysis: Journal of the American Statistical Association. 74(368) [cited 2018 Aug 23]; Available from: https:// www.tandfonline.com/ doi/ abs/ 10.1080/ 01621459.1979.10481030]. in weighted bivariate analyses were included in a backward elimination model selection procedure. Variables independently associated with infection were retained in the weighted multivariate model to produce the final results.

2.8. Ethical Issues and Protection of the Participants

The study received ethical approval from the Ethics Committee for Health Research (CERS) of Burkina Faso and The Johns Hopkins Bloomberg School of Public Health Institutional Review Board. Research ethics training and sensitivity training were provided to all staff the study. Confidentiality was maintained by using a unique study identifier rather than real names on questionnaires. Participant unique and anonymized codes were used to link study questionnaires with blood sample tubes. All participants who tested positive for HIV during HIV behavior and seroprevalence survey were referred to a healthcare center for appropriate care. Those who tested positive for syphilis received syphilis treatment in situ. In addition to the consent for participation to the HIV behavioral survey, individual consent was required for serum samples storage for further research related to sexually transmitted diseases.

3. RESULTS

3.1. Socio-Demographic Characteristics of FSW

The mean age of the FSW was 24.9 ± 6.4 years. Table 1 shows the socio-demographic and socio-professional characteristics of the FSW. The education level of study participants was low; about 23.8% had no education, and one-third of them had a primary level of education (38.0%). More than 63% (219/348) of the FSW in the sample were single. The vast majority (about 70%) had at least one biological child. Half of the FSW (50.4%) declared to have no other income generating activity (except for sex work).

Table 1
Characteristics of female sex workers.


3.2. HBV, HCV and HDV Prevalence Among FSW

In total, 348 FSW were tested for viral hepatitis. Sixty-one (61) were HBV positive, with RDS adjusted prevalence of 18.2% (95%CI: 14.4-22.9). Hepatitis D prevalence among HBV antigen positive FSW was 1.64% (1/61). HCV antibody virus tests were conducted on 325 available serums and 32 were reactive (9.8%). The adjusted prevalence of the HCV in the FSW was estimated to 10.6% (95%CI: 07.5-14.8). Table 2 shows the prevalence of HBV and HCV antigen positivity and the results of the bivariate and multivariate analyses.

3.3. Factors Associated with FSW’ HBV and HCV Infection

In bivariate analysis, factors associated with HBV antigen positivity were previous pregnancy, the consistent condom use, the lower weekly wage and being HIV positive. None of these factors was independently associated with the HBV infection among FSW in multivariate analysis. The details are shown in (Table 2).

For HCV, only the being HIV positive (aOR = 5.59, p = 0.005), the consistent condom use (aOR = 0.32, p = 0.019), sex with clients in street, public gardens or bars (aOR = 3.27, p = 0.027), and the reuse of condom (aOR = 6.91, p = 0.007) were independently associated with HCV antigen positivity in FSW.

Table 2
HBV, HCV Seroprevalence and selected socio-demographic and sex work-related characteristics associated.


4. DISCUSSION

To our knowledge, this study was the first to use the RDS method among FSW for HBV, HCV, and HDV seroprevalence and one of the few studies to report seroprevalence data of these viruses among FSW in West-Africa. The results show a high prevalence of HBV (18.2%) and hepatitis C (10.6%), and low seroprevalence of hepatitis D (1.5%) among FSW in Ouagadougou. HBV and HCV prevalence reported in our study are higher than those described in the general population in the country [29Etude ANRS. 12270 : prévalence du VHC/VHB en population générale au Burkina-Faso | Vih.org [Internet] [cited 2018 May 23]; Available from: http:// vih.org/ 20160423/ etude -anrs-12270-prevalence-du-vhcvhb-en-population-generale-au-burkina-faso/138077]. In fact, the national prevalence of HBV in Burkina Faso was estimated at 8.8% [29Etude ANRS. 12270 : prévalence du VHC/VHB en population générale au Burkina-Faso | Vih.org [Internet] [cited 2018 May 23]; Available from: http:// vih.org/ 20160423/ etude -anrs-12270-prevalence-du-vhcvhb-en-population-generale-au-burkina-faso/138077]. In a recent systematic review in the country, a slightly higher prevalence of HBV was reported among specific groups: pregnant women (11.1%), blood donors (11.7%) and people living with HIV (12.6%) [30Hahn JA. Sex, drugs, and hepatitis C virus. J Infect Dis 2007; 195(11): 1556-9. https://academic.oup.com/jid/article/195/11/1556/943264
[http://dx.doi.org/10.1086/516792] [PMID: 17471423]
]. Our results are comparable to those of Forbi et al. who reported 17.1% of HBV prevalence in FSW in Nigeria [31Forbi JC, Onyemauwa N, Gyar SD, Oyeleye AO, Entonu P, Agwale SM. High prevalence of hepatitis B virus among female sex workers in Nigeria. Rev Inst Med Trop São Paulo 2008; 50(4): 219-21.
[http://dx.doi.org/10.1590/S0036-46652008000400006] [PMID: 1881 3761]
], while Musa et al. found (13.6% in general population in this country [32Musa BM, Bussell S, Borodo MM, Samaila AA, Femi OL. Prevalence of hepatitis B virus infection in Nigeria, 2000-2013: A systematic review and meta-analysis. Niger J Clin Pract 2015; 18(2): 163-72.
[http://dx.doi.org/10.4103/1119-3077.151035] [PMID: 25665986]
].

Similar results were reported by De Matos et al. who found an HBV prevalence of 17.1%, which was 1.5 times higher than the prevalence in general population estimated at 11.6% in Brazil [14de Matos MA, França DD da S, Carneiro M. Viral hepatitis in female sex workers using the Respondent-Driven Sampling. Rev Saúde Pública [Internet] 201751 [cited 2018 Apr 28]; Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5477708/]. Due to risk factors, FSW are more vulnerable to HBV infection. Universal vaccination against HBV among infants was initiated in Burkina Faso only in 2006 [33Ouedraogo HG, Kouanda S, Tiendrebeogo S, et al. Immune and Hepatitis B virus (HBV) infection status among children receiving hepatitis B immunization in Ouagadougou, Burkina Faso. J Pediatr Infect Dis 2013; 8: 167-73. https:// content.iospress.com/ articles/ journal-of-pediatric-infectious-diseases/ jpi00399]. As indicated by our study, most of FSW were not immunized against HBV (only 4% declared to be in contact at least once with the vaccine), and are at increased vulnerability to transmit HBV among the unvaccinated adult population through multiple sex partners.

Certain factors such as advanced age and seniority in sex work, previous history of STIs, previous history of a blood transfusion, and drug use were associated with HBV prevalence in some studies [14de Matos MA, França DD da S, Carneiro M. Viral hepatitis in female sex workers using the Respondent-Driven Sampling. Rev Saúde Pública [Internet] 201751 [cited 2018 Apr 28]; Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5477708/]. Our study did not identify an independent association of socio-demographic or behavioral factors with HBV infection in FSW. A study in Congo reported age as a factor associated with HBV in FSW [15Niama FR, Loukabou Bongolo NC, Mayengue PI, et al. A study on HIV, syphilis, and hepatitis B and C virus infections among female sex workers in the Republic of Congo. Arch Public Health 2017; 75: 21. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5421326/
[http://dx.doi.org/10.1186/s13690-017-0189-5] [PMID: 28503303]
]. Another study in Tanzania concluded that sexual acquisition of HBV in adults is less common [34Jacobs B, Mayaud P, Changalucha J, et al. Sexual transmission of hepatitis B in Mwanza, Tanzania. Sex Transm Dis 1997; 24(3): 121-6.
[http://dx.doi.org/10.1097/00007435-199703000-00001] [PMID: 9132 977]
]. Vertical transmission of HBV from mother to child or childhood HBV infection is the most common in Africa suggesting lower infection rates from sexual activity [35Lesi O. Hepatitis B in Africa: The challenges in controlling the scourge [Internet]. The Conversation [cited 2018 May 2]; Available from: http://theconversation.com/hepatitis-b-in-africa-the-challenges-in-controlling-the-scourge-43818, 36Nelson NP, Easterbrook PJ, McMahon BJ. Epidemiology of hepatitis B virus infection and impact of vaccination on disease. Clin Liver Dis 2016; 20(4): 607-28. Available from: https:// www.ncbi.nlm.nih.gov/ pmc/articles/PMC5582972/
[http://dx.doi.org/10.1016/j.cld.2016.06.006] [PMID: 27742003]
]. Risky sexual behaviors among FSW may lead to HBV infection or they may have been infected during childhood. The cross sectional nature of this study did not allow us to determine if HBV among the study population was acquired during childhood or during sex work. Future longitudinal cohort studies are needed to elucidate the vulnerability factors of FSW in Burkina Faso.

In our study, only one FSW among those who were HBV positive was tested positive for HDV antibodies (1.64%), and reported to the total sampling of the study, its prevalence is 0.3%. HDV is endemic in Africa and its prevalence varies from one country to another [6Stockdale AJ, Chaponda M, Beloukas A, et al. Prevalence of hepatitis D virus infection in sub-Saharan Africa: A systematic review and meta-analysis. Lancet Glob Health 2017; 5(10): e992-e1003.https:// www.ncbi.nlm.nih.gov/ pmc/ articles/ PMC5599428/
[http://dx.doi.org/10.1016/S2214-109X(17)30298-X] [PMID: 289117 65]
]. Our study shows a lower HDV prevalence in FSW compared to that of the West African population (7.33%) [6Stockdale AJ, Chaponda M, Beloukas A, et al. Prevalence of hepatitis D virus infection in sub-Saharan Africa: A systematic review and meta-analysis. Lancet Glob Health 2017; 5(10): e992-e1003.https:// www.ncbi.nlm.nih.gov/ pmc/ articles/ PMC5599428/
[http://dx.doi.org/10.1016/S2214-109X(17)30298-X] [PMID: 289117 65]
]. The prevalence of HDV in our study is however, higher than the one reported in the female population of HBsAg carriers in Burkina Faso (0.77%) [37Tuaillon E, Kania D, Gordien E, Van de Perre P, Dujols P. Epidemiological data for hepatitis D in Africa. Lancet Glob Health 2018; 6(1): e33. https:// www.thelancet.com/ journals/ langlo/ article/ PIIS2214-109X(17)30463-1/ abstract
[http://dx.doi.org/10.1016/S2214-109X(17)30463-1] [PMID: 292416 11]
]. HBV and HDV coinfection is a concern because it could accelerate the HBV evolution, and potentially lead to liver cirrhosis or cancer if proper treatment is not offered [2Alvarado-Mora MV, Locarnini S, Rizzetto M, Pinho JR. An update on HDV: virology, pathogenesis and treatment. Antivir Ther (Lond) 2013; 18(3 Pt B): 541-8.
[http://dx.doi.org/10.3851/IMP2598] [PMID: 23792471]
].

The prevalence of HCV among the study population was high, despite the low number of injection drug users. Those who reported a history of injection drug use did not test positive for HCV. Compared to developed countries where injection drug use is a contributing factor to HCV transmission, injection drug use is not common in Burkina Faso [38Aceijas C, Rhodes T. Global estimates of prevalence of HCV infection among injecting drug users. Int J Drug Policy 2007; 18(5): 352-8. http://linkinghub.elsevier.com/retrieve/pii/S0955395907000916
[http://dx.doi.org/10.1016/j.drugpo.2007.04.004] [PMID: 17854722]
, 39Madhava V, Burgess C, Drucker E. Epidemiology of chronic hepatitis C virus infection in sub-Saharan Africa. Lancet Infect Dis 2002; 2(5): 293-302. https://www.thelancet.com/journals/laninf/article/PIIS1473-3099(02)00264-5/abstract
[http://dx.doi.org/10.1016/S1473-3099(02)00264-5] [PMID: 120629 95]
]. HCV antibody prevalence was 10.6% among FSW which was three times higher compared to 3.5% among a population of reproductive age at the national level, and to 3.1% among women [29Etude ANRS. 12270 : prévalence du VHC/VHB en population générale au Burkina-Faso | Vih.org [Internet] [cited 2018 May 23]; Available from: http:// vih.org/ 20160423/ etude -anrs-12270-prevalence-du-vhcvhb-en-population-generale-au-burkina-faso/138077]. This implies that FSW are more vulnerable to contracting HCV sexually as opposed to through injection drug use [30Hahn JA. Sex, drugs, and hepatitis C virus. J Infect Dis 2007; 195(11): 1556-9. https://academic.oup.com/jid/article/195/11/1556/943264
[http://dx.doi.org/10.1086/516792] [PMID: 17471423]
].

Socio-demographic characteristics did not indicate significant differences of HCV prevalence among FSW. Sexual behavior factors relating to HIV infection including condom use, condom scarcity, and location of sexual activity were associated with HCV infection and are opportunities for public health intervention and sexual health education. Some authors suggested that risky sexual behaviors including multiple sex partners and intense sexual practices can lead to accumulated risk for HCV transmission [40Chan DPC, Sun H-Y, Wong HTH, Lee SS, Hung CC. Sexually acquired hepatitis C virus infection: A review. Int J Infect Dis 2016; 49: 47-58. http:// www.sciencedirect.com/ science/ article/ pii/ S1201971216310736
[http://dx.doi.org/10.1016/j.ijid.2016.05.030] [PMID: 27270138]
]. This sexual transmission can be facilitated in FSW by repeated exposure of vaginal mucosa to the virus particularly when they are injured [41Danta M, Rodger AJ. Transmission of HCV in HIV-positive populations. Curr Opin HIV AIDS 2011; 6(6): 451-8. https://insights.ovid.com/crossref?an=01222929-201111000-00003
[http://dx.doi.org/10.1097/COH.0b013e32834b4974] [PMID: 220018 90]
]. Also, the risk of contracting HCV among those infected with HIV people has previously been studied [42Barth RE, Huijgen Q, Taljaard J, Hoepelman AI. Hepatitis B/C and HIV in sub-Saharan Africa: an association between highly prevalent infectious diseases. A systematic review and meta-analysis. Int J Infect Dis 2010; 14(12): e1024-31.http:// www.sciencedirect.com/ science/ article/ pii/ S1201971210024562
[http://dx.doi.org/10.1016/j.ijid.2010.06.013] [PMID: 20870439]
]. In a systematic review of studies on HIV and the viral hepatitis co-infections in sub-Saharan Africa, the authors reported that those who were HIV infected were estimated to be 60% higher risk of HCV coinfection compared to HIV seronegative people (RR = 1.60) [42Barth RE, Huijgen Q, Taljaard J, Hoepelman AI. Hepatitis B/C and HIV in sub-Saharan Africa: an association between highly prevalent infectious diseases. A systematic review and meta-analysis. Int J Infect Dis 2010; 14(12): e1024-31.http:// www.sciencedirect.com/ science/ article/ pii/ S1201971210024562
[http://dx.doi.org/10.1016/j.ijid.2010.06.013] [PMID: 20870439]
].

The limitations of our study are the fact that risky sexual behaviors are self-reported and subject to recall bias. We do not have the possibility to check the reliability of these responses. However, the study staff was well-trained to minimize this risk of bias and obtain quality data. Secondly, the RDS method used to recruit the FSW is an estimate of the population and does not account for the entire population of FSW in Ouagadougou. Thirdly, the cross-sectional nature of this study does not allow us to establish temporality between risky sexual behavior and HBV or HCV infection. We also do not know when the FSW contracted these diseases and if it was before or after they started sex work. Finally, a positive HBV or HCV antibody test does not confirm the stage of infection or the presence of the virus during the study.

CONCLUSION

Our study suggests that HBV and HCV infection are a public health concern among FSW. Comprehensive prevention for HBV and HCV among FSW should be implemented in order to meet the objectives of the viral hepatitis global program [43WHO. Global health sector strategy on viral hepatitis 2016-2021 [Internet]. WHO Available from: http:// wwwwhoint/ hepatitis/ strategy2016-2021 / ghss-hep/ en/ 2016 [cited 2018 May 23];]. These prevention programs must take into account their unique needs and behaviors that put them at increased vulnerability. We recommend vaccination against HBV, bloodborne exposure training, and sexual exposure training. Vaccination against HBV virus should be promoted to those at highest risk of blood and sexual exposures. In addition, sexual education to use barrier methods, such as condoms and avoid unprotected intercourse, is required. And finally, preventing blood exposures and encouraging treatment for HCV must be included in future public health program planning, particularly among FSW. With a comprehensive and inclusive HBV and HCV prevention program, this could also be part of HIV related programming and services among FSW in Burkina Faso.

LIST OF ABBREVIATIONS

CERS  = Ethics Committee for Health Research of Burkina Faso
CI  = Confidence Interval
ELISA  = Enzyme Linked Immunoassay
HBsAg  = Hepatitis B Virus Surface Antigen
HBV  = Hepatitis B Virus
HCV  = Hepatitis C Virus
HDV  = Hepatitis D Virus
HIV  = Human Immunodeficiency Virus
FSW  = Female Sex Worker
OR  = Odds Ratio
aOR  = Adjusted Odds Ratio
RDS  = Respondent Driven Sampling
RDSAT  = RDS Analysis Tool
USD  = United States Dollars

AVAILABILITY OF DATA AND MATERIAL

The datasets used during the current study are available from the corresponding author on reasonable request.

FUNDING

The biological sample and behavioral data are from Research to Prevention (R2P) project, which is funded by the US Agency for International Development under Contract No. GHH-I-00-0700, 032-00, supported by the USA President's Emergency Plan for AIDS Relief. The R2P Project is led by the Johns Hopkins Center for Global Health and managed by the Johns Hopkins Bloomberg School of Public Health Center for Communication Programs.

Reagents for hepatitis B, C, D virus testing were provided by Institut de Recherche en Sciences de la Santé (IRSS/CNRST), Ouagadougou, Burkina Faso.

AUTHORS' CONTRIBUTION

HGO, SK, NB, SB conceived and designed the study; HGO, BCS supervised data collection; HGO, CD, MC performed lab analysis; HGO prepared the manuscript and it was reviewed by SK, NB, SG, OK, HL, BCS, YT, SB.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

The study received ethical approval from the Ethics Committee for Health Research (CERS) of Burkina Faso and The Johns Hopkins Bloomberg School of Public Health Institutional Review Board.

HUMAN AND ANIMAL RIGHTS

No Animals were used in this research. All human research procedures followed were in accordance with the ethical standards of the committee responsible for human experimentation (institutional and national), and with the Helsinki Declaration of 1975, as revised in 2013.

CONSENT FOR PUBLICATION

Written informed consent was obtained from all the participants prior to publication.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

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.

REFERENCES

[1] WHO. Global hepatitis report, 2017. Geneva: World Health Organization. Report No: ISBN 978-92-4-156545-5 2017; 83.
[2] Alvarado-Mora MV, Locarnini S, Rizzetto M, Pinho JR. An update on HDV: virology, pathogenesis and treatment. Antivir Ther (Lond) 2013; 18(3 Pt B): 541-8.
[http://dx.doi.org/10.3851/IMP2598] [PMID: 23792471]
[3] Rizzetto M, Hepatitis D. Virus: Introduction and Epidemiology. Cold Spring Harb Perspect Med 2015; 5(7): a021576.https:// www.ncbi.nlm.nih.gov/ pmc /articles/ PMC4484953/
[http://dx.doi.org/10.1101/cshperspect.a021576] [PMID: 26134842]
[4] Spearman CW, Afihene M, Ally R, et al. Hepatitis B in sub-Saharan Africa: Strategies to achieve the 2030 elimination targets. Lancet Gastroenterol Hepatol 2017; 2(12): 900-9.
[http://dx.doi.org/10.1016/S2468-1253(17)30295-9] [PMID: 291327 59]
[5] Schweitzer A, Horn J, Mikolajczyk RT, Krause G, Ott JJ. Estimations of worldwide prevalence of chronic hepatitis B virus infection: A systematic review of data published between 1965 and 2013. Lancet 2015; 386(10003): 1546-55.http:// linkinghub.elsevier.com/ retrieve/ pii/ S014067361561412X
[http://dx.doi.org/10.1016/S0140-6736(15)61412-X] [PMID: 262314 59]
[6] Stockdale AJ, Chaponda M, Beloukas A, et al. Prevalence of hepatitis D virus infection in sub-Saharan Africa: A systematic review and meta-analysis. Lancet Glob Health 2017; 5(10): e992-e1003.https:// www.ncbi.nlm.nih.gov/ pmc/ articles/ PMC5599428/
[http://dx.doi.org/10.1016/S2214-109X(17)30298-X] [PMID: 289117 65]
[7] Rao VB, Johari N, du Cros P, Messina J, Ford N, Cooke GS. Hepatitis C seroprevalence and HIV co-infection in sub-Saharan Africa: A systematic review and meta-analysis. Lancet Infect Dis 2015; 15(7): 819-24.
[http://dx.doi.org/10.1016/S1473-3099(15)00006-7] [PMID: 259570 78]
[8] Rooney G, Gilson RJ. Sexual transmission of hepatitis C virus infection. Sex Transm Infect 1998; 74(6): 399-404.
[http://dx.doi.org/10.1136/sti.74.6.399] [PMID: 10195047]
[9] Bradshaw D, Matthews G, Danta M. Sexually transmitted hepatitis C infection: The new epidemic in MSM? Curr Opin Infect Dis 2013; 26(1): 66-72.
[PMID: 23242342]
[10] Terrault NA, Dodge JL, Murphy EL, et al. Sexual transmission of hepatitis C virus among monogamous heterosexual couples: The HCV partners study. Hepatology 2013; 57(3): 881-9.
[http://dx.doi.org/10.1002/hep.26164] [PMID: 23175457]
[11] Pitpitan EV, Kalichman SC, Eaton LA, Strathdee SA, Patterson TL. HIV/STI risk among venue-based female sex workers across the globe: A look back and the way forward. Curr HIV/AIDS Rep 2013; 10(1): 65-78.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3567216/
[http://dx.doi.org/10.1007/s11904-012-0142-8] [PMID: 23160840]
[12] Puga MAM, Bandeira LM, Weis SMDS, et al. High-risk behaviors for hepatitis B and C infections among female sex workers. Rev Soc Bras Med Trop 2018; 51(2): 198-202.http:// www.scielo.br/ scielo.php?script = sci _ abstract & pid = S0037-86822018000200198 & lng=en & nrm=iso & tlng = en
[http://dx.doi.org/10.1590/0037-8682-0231-2017] [PMID: 29768553]
[13] Moayedi-Nia S, Bayat Jozani Z, Esmaeeli Djavid G, et al. HIV, HCV, HBV, HSV, and syphilis prevalence among female sex workers in Tehran, Iran, by using respondent-driven sampling. AIDS Care 2016; 28(4): 487-90.
[http://dx.doi.org/10.1080/09540121.2015.1109582] [PMID: 265656 71]
[14] de Matos MA, França DD da S, Carneiro M. Viral hepatitis in female sex workers using the Respondent-Driven Sampling. Rev Saúde Pública [Internet] 201751 [cited 2018 Apr 28]; Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5477708/
[15] Niama FR, Loukabou Bongolo NC, Mayengue PI, et al. A study on HIV, syphilis, and hepatitis B and C virus infections among female sex workers in the Republic of Congo. Arch Public Health 2017; 75: 21. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5421326/
[http://dx.doi.org/10.1186/s13690-017-0189-5] [PMID: 28503303]
[16] Heckathorn DD. Respondent-Driven sampling: A new approach to the study of hidden populations. Soc Probl 1997; 44: 174-99. http://www.jstor.org/stable/3096941
[http://dx.doi.org/10.2307/3096941]
[17] McCreesh N, Copas A, Seeley J, et al. Respondent driven sampling: Determinants of recruitment and a method to improve point estimation. In: Eisele T, Ed. PLoS ONE [Internet] 20138 [cited 2016 Aug 4];: e78402. http://dx.plos.org/10.1371/journal.pone.0078402
[18] Holland CE, Kouanda S, Lougué M, et al. Using population-Size estimation and Cross-sectional survey methods to evaluate HIV service coverage among key populations in burkina faso and togo. Public Health Rep 2016; 131(6): 773-82.
[http://dx.doi.org/10.1177/0033354916677237] [PMID: 28123223]
[19] Heckathorn DD. Respondent-Driven sampling II: Deriving valid population estimates from Chain-Referral samples of hidden populations. Soc Probl 2002; 49: 11-34. https:// academic.oup.com/ socpro/ article-lookup/ doi/ 10.1525/ sp.2002.49.1.11
[http://dx.doi.org/10.1525/sp.2002.49.1.11]
[20] Heckathorn Douglas D. Respondent-Driven sampling: A new approach to the study of hidden populations. Univ Calif Press Behalf Soc Study Soc Probl 1997; 44: 174-99.
[21] Wirtz AL, Schwartz S, Ketende S, et al. Sexual violence, condom negotiation, and condom use in the context of sex work: Results from two west african countries. JAIDS J Acquir Immune Defic Syndr [Internet] 201568 [cited 2016 Jun 23];: S171-9. Available from: http://content.wkhealth.com/linkback/openurl?sid=WKPTLP:landingpage&an=00126334-201503011-00014
[22] Weller S, Davis K. Condom effectiveness in reducing heterosexual HIV transmission. Cochrane Database Syst Rev 2002; (1): CD003255.
[PMID: 11869658]
[23] Nagot N, Ouangré A, Ouedraogo A, et al. Spectrum of commercial sex activity in Burkina Faso: Classification model and risk of exposure to HIV. J Acquir Immune Defic Syndr 2002; 29(5): 517-21.
[http://dx.doi.org/10.1097/00042560-200204150-00013] [PMID: 119 81369]
[24] Lankoandé S, Meda N, Sangaré L, et al. Prevalence and risk of HIV infection among female sex workers in Burkina Faso. Int J STD AIDS 1998; 9(3): 146-50.
[http://dx.doi.org/10.1258/0956462981921909] [PMID: 9530899]
[25] Tiffany JS. Respondent-driven sampling in participatory research contexts: Participant-driven recruitment. J Urban Health 2006; 83(6)(Suppl.): i113-24. http:// link.springer.com/ 10.1007/ s11524 - 006 - 9107-9
[http://dx.doi.org/10.1007/s11524-006-9107-9] [PMID: 16933100]
[26] Sperandei S. Understanding logistic regression analysis. Biochem Med (Zagreb) 2014; 24(1): 12-8. https:// www.ncbi.nlm.nih.gov/ pmc/ articles/ PMC3936971/
[http://dx.doi.org/10.11613/BM.2014.003] [PMID: 24627710]
[27] Sanharawi ME, Naudet F. Comprendre la régression logistique. /data/revues/01815512/v36i8/S0181551213002490/ [Internet]. 2013 [cited 2018 Aug 23]; Available from: http:// www.em-consulte.com/ en/ article/ 842576
[28] Comparison of Stopping Rules in Forward Stepwise Discriminant Analysis: Journal of the American Statistical Association. 74(368) [cited 2018 Aug 23]; Available from: https:// www.tandfonline.com/ doi/ abs/ 10.1080/ 01621459.1979.10481030
[29] Etude ANRS. 12270 : prévalence du VHC/VHB en population générale au Burkina-Faso | Vih.org [Internet] [cited 2018 May 23]; Available from: http:// vih.org/ 20160423/ etude -anrs-12270-prevalence-du-vhcvhb-en-population-generale-au-burkina-faso/138077
[30] Hahn JA. Sex, drugs, and hepatitis C virus. J Infect Dis 2007; 195(11): 1556-9. https://academic.oup.com/jid/article/195/11/1556/943264
[http://dx.doi.org/10.1086/516792] [PMID: 17471423]
[31] Forbi JC, Onyemauwa N, Gyar SD, Oyeleye AO, Entonu P, Agwale SM. High prevalence of hepatitis B virus among female sex workers in Nigeria. Rev Inst Med Trop São Paulo 2008; 50(4): 219-21.
[http://dx.doi.org/10.1590/S0036-46652008000400006] [PMID: 1881 3761]
[32] Musa BM, Bussell S, Borodo MM, Samaila AA, Femi OL. Prevalence of hepatitis B virus infection in Nigeria, 2000-2013: A systematic review and meta-analysis. Niger J Clin Pract 2015; 18(2): 163-72.
[http://dx.doi.org/10.4103/1119-3077.151035] [PMID: 25665986]
[33] Ouedraogo HG, Kouanda S, Tiendrebeogo S, et al. Immune and Hepatitis B virus (HBV) infection status among children receiving hepatitis B immunization in Ouagadougou, Burkina Faso. J Pediatr Infect Dis 2013; 8: 167-73. https:// content.iospress.com/ articles/ journal-of-pediatric-infectious-diseases/ jpi00399
[34] Jacobs B, Mayaud P, Changalucha J, et al. Sexual transmission of hepatitis B in Mwanza, Tanzania. Sex Transm Dis 1997; 24(3): 121-6.
[http://dx.doi.org/10.1097/00007435-199703000-00001] [PMID: 9132 977]
[35] Lesi O. Hepatitis B in Africa: The challenges in controlling the scourge [Internet]. The Conversation [cited 2018 May 2]; Available from: http://theconversation.com/hepatitis-b-in-africa-the-challenges-in-controlling-the-scourge-43818
[36] Nelson NP, Easterbrook PJ, McMahon BJ. Epidemiology of hepatitis B virus infection and impact of vaccination on disease. Clin Liver Dis 2016; 20(4): 607-28. Available from: https:// www.ncbi.nlm.nih.gov/ pmc/articles/PMC5582972/
[http://dx.doi.org/10.1016/j.cld.2016.06.006] [PMID: 27742003]
[37] Tuaillon E, Kania D, Gordien E, Van de Perre P, Dujols P. Epidemiological data for hepatitis D in Africa. Lancet Glob Health 2018; 6(1): e33. https:// www.thelancet.com/ journals/ langlo/ article/ PIIS2214-109X(17)30463-1/ abstract
[http://dx.doi.org/10.1016/S2214-109X(17)30463-1] [PMID: 292416 11]
[38] Aceijas C, Rhodes T. Global estimates of prevalence of HCV infection among injecting drug users. Int J Drug Policy 2007; 18(5): 352-8. http://linkinghub.elsevier.com/retrieve/pii/S0955395907000916
[http://dx.doi.org/10.1016/j.drugpo.2007.04.004] [PMID: 17854722]
[39] Madhava V, Burgess C, Drucker E. Epidemiology of chronic hepatitis C virus infection in sub-Saharan Africa. Lancet Infect Dis 2002; 2(5): 293-302. https://www.thelancet.com/journals/laninf/article/PIIS1473-3099(02)00264-5/abstract
[http://dx.doi.org/10.1016/S1473-3099(02)00264-5] [PMID: 120629 95]
[40] Chan DPC, Sun H-Y, Wong HTH, Lee SS, Hung CC. Sexually acquired hepatitis C virus infection: A review. Int J Infect Dis 2016; 49: 47-58. http:// www.sciencedirect.com/ science/ article/ pii/ S1201971216310736
[http://dx.doi.org/10.1016/j.ijid.2016.05.030] [PMID: 27270138]
[41] Danta M, Rodger AJ. Transmission of HCV in HIV-positive populations. Curr Opin HIV AIDS 2011; 6(6): 451-8. https://insights.ovid.com/crossref?an=01222929-201111000-00003
[http://dx.doi.org/10.1097/COH.0b013e32834b4974] [PMID: 220018 90]
[42] Barth RE, Huijgen Q, Taljaard J, Hoepelman AI. Hepatitis B/C and HIV in sub-Saharan Africa: an association between highly prevalent infectious diseases. A systematic review and meta-analysis. Int J Infect Dis 2010; 14(12): e1024-31.http:// www.sciencedirect.com/ science/ article/ pii/ S1201971210024562
[http://dx.doi.org/10.1016/j.ijid.2010.06.013] [PMID: 20870439]
[43] WHO. Global health sector strategy on viral hepatitis 2016-2021 [Internet]. WHO Available from: http:// wwwwhoint/ hepatitis/ strategy2016-2021 / ghss-hep/ en/ 2016 [cited 2018 May 23];

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