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Epidemiology
Original research
Role of unsafe medical practices and sexual behaviours in the hepatitis B and C syndemic and HIV co-infection in Rwanda: a cross-sectional study
  1. Jean Damascene Makuza1,
  2. Marie Paul Nisingizwe2,
  3. Jean Olivier Twahirwa Rwema3,
  4. Donatha Dushimiyimana1,
  5. Dominique Savio Habimana1,
  6. Sabine Umuraza4,
  7. Janvier Serumondo1,
  8. Alida Ngwije4,
  9. Muhamed Semakula1,5,
  10. Neil Gupta6,
  11. Sabin Nsanzimana7,
  12. Naveed Zafar Janjua2,8
  1. 1IHDPC, Rwanda Biomedical Center, Kigali, Kigali City, Rwanda
  2. 2School of Population and Public Health, The University of British Columbia, Vancouver, British Columbia, Canada
  3. 3Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health Center for Teaching and Learning, Baltimore, Maryland, USA
  4. 4Health Department, Clinton Health Access Initiative, Kigali, Rwanda
  5. 5I-Biostat Department of Sciences, Hasselt University, Hasselt, Limburg, Belgium
  6. 6Division of Global Health Equity, Brigham and Women’s Hospital, Boston, Massachusetts, USA
  7. 7Rwanda Biomedical Center, Kigali, Rwanda
  8. 8Clinical Prevention Services, British Columbia Center for Diseases Control, Vancouver, British Columbia, Canada
  1. Correspondence to Dr Jean Damascene Makuza; makorofr{at}gmail.com

Abstract

Objectives This study describes the burden of the hepatitis B, C and HIV co-infections and assesses associated risk factors.

Setting This analysis used data from a viral hepatitis screening campaign conducted in six districts in Rwanda from April to May 2019. Ten health centres per district were selected according to population size and distance.

Participants The campaign collected information from 156 499 participants (51 496 males and 104 953 females) on sociodemographic, clinical and behavioural characteristics. People who were not Rwandan by nationality or under 15 years old were excluded.

Primary and secondary outcomes The outcomes of interest included chronic hepatitis C virus (HCV) infection, chronic hepatitis B virus (HBV) infection, HIV infection, co-infection HIV/HBV, co-infection HIV/HCV, co-infection HBV/HCV and co-infection HCV/HBV/HIV. Multivariable logistic regressions were used to assess factors associated with HBV, HCV and HIV, mono and co-infections.

Results Of 156 499 individuals screened, 3465 (2.2%) were hepatitis B surface antigen positive and 83% (2872/3465) of them had detectable HBV desoxy-nucleic acid (HBV DNA). A total of 4382 (2.8%) individuals were positive for antibody-HCV (anti-HCV) and 3163 (72.2%) had detectable HCV ribo-nucleic acid (RNA). Overall, 36 (0.02%) had HBV/HCV co-infection, 153 (0.1%) HBV/HIV co-infection, 238 (0.15%) HCV/HIV co-infection and 3 (0.002%) had triple infection. Scarification or receiving an operation from traditional healer was associated with all infections. Healthcare risk factors—history of surgery or transfusion—were associated with higher likelihood of HIV infection with OR 1.42 (95% CI 1.21 to 1.66) and OR 1.48 (1.29 to 1.70), respectively, while history of physical traumatic assault was associated with a higher likelihood of HIV and HBV/HIV co-infections with OR 1.69 (95% CI 1.51 to 1.88) and OR 1.82 (1.08 to 3.05), respectively.

Conclusions Overall, mono-infections were common and there were differences in significant risk factors associated with various infections. These findings highlight the magnitude of co-infections and differences in underlying risk factors that are important for designing prevention and care programmes.

  • epidemiology
  • HIV & AIDS
  • public health
  • hepatology
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This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

http://dx.doi.org/10.1136/bmjopen-2019-036711

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    Strengths and limitations of this study

    • This study used serological markers and molecular tests for hepatitis C virus (HCV) and hepatitis B virus (HBV) testing to assess the burden of HBV, HCV and HIV infections among the general population in a developing country.

    • Although various risk factors were assessed, information on substance use was not available.

    • Participants were from only six districts. Therefore, the prevalence estimates and risk factors found to be associated with HCV, HBV, HIV and their co-infections may not be generalisable to the entire population.

    Background

    Globally, hepatitis B and C virus infections are among the leading causes of mortality with about 1 400 000 attributable deaths every year.1 Despite substantial improvements in HIV antiretroviral treatment roll-out, new HIV infections and HIV/AIDS-related deaths remain high, with 1.7 million new HIV infections and about 770 000 deaths in 2018 worldwide.2 Globally, 5%–20% of people living with HIV (PLHIV) are co-infected with HBV, though rates of chronic HBV in HIV-infected individuals vary significantly across regions and risk groups.3 Similarly, 6.2% (2 278 400) of all PLHIV have HIV–HCV co-infection, with the highest burden found in the African and South East Asia regions.4 People with all three co-infections have high morbidity and mortality compared with those who are negative for all infections or mono-infected.5 6 Similarly, studies have shown a higher risk of various comorbidities such as liver cirrhosis, liver cancer and end-stage renal disease among people with co-infection.7 8

    Despite high morbidity and mortality related with co-infections, limited data are available on co-infections with all three infections at the broader population level.9 Most studies on co-infection were conducted among people with HIV infection or in specific populations.4 10–15 Such data are especially scarce in developing countries with high burden of each of these infections, such as Rwanda.12 16 In 2015, Rwanda DHS showed that the prevalence of HIV in the general population was 3%, with a higher prevalence in urban than rural areas (6% vs 2.4%, respectively).17 Recent studies on HBV in Rwanda revealed that the prevalence of hepatitis B surface antigen (HBsAg) among people screened was 3.9%,18 19 while the prevalence of anti-HCV was between 6.2% and 6.6% with viremia of 52%.20 21 In 2017, a study conducted among PLHIV found that the prevalence of co-infections with HBV and HCV were 4.2% and 4.7%, respectively.16

    Rwanda is among few African countries that have committed to fight HBV and HCV, in addition to HIV, and to eliminate them before 2030.22 Scale-up of treatments for HBV, HCV and HIV has the potential to reduce morbidity and mortality. However, for co-infections, treatment decisions and outcomes differ, thus, there is a need to better characterise the burden of co-infections of these diseases in the general population in Rwanda. Quantifying the burden of these co-infections will inform effective screening, diagnosis and treatment programmes.

    HBV, HCV and HIV share transmission routes, and their co-occurrence depends on the presence of shared risk factors and community prevalence rates. Furthermore, the presence of multiple risk factors can interact with each other to increase the risk of infection transmission, a concept also known as a syndemic.23 Some of these risk factors, as well as the infection, may also enhance morbidity and mortality caused by all or one of these three viruses. For instance, in British Columbia, Canada, substance use was associated with a higher risk of triple infection and HCV–HIV co-infection, while men having sex with men had a higher risk of HIV and HIV–HBV co-infection.9 In a study on HBV, HCV and HIV in Libya, co-infection prevalence was low (HCV/HIV: 0.15%, HCV/HBV: 0.04%, HBV/HIV: 0.03%). HIV, HCV and their co-infection were related to substance use and hemodialysis, while HBV infection was associated with family history and contact with person living with HBV.9 This pattern is unlike in Sub-Saharan Africa, where HBV is commonly transmitted during childhood between siblings long before infection of HIV and HCV.11 Risk factors might be different in different countries due to differences in the characteristics of general population; therefore, it is crucial to identify risk factors associated with these co-infections in Rwanda. Characterisation of risk factors and their relationships in high prevalence subpopulations could inform the optimisation of services for various population groups at risk of and affected by HBV, HCV, HIV as well as other bloodborne infections.

    Thus, this study aims to address these gaps by assessing the burden of the HBV, HCV HIV and their co-infections and characterising underlying factors among people tested during the 2019 mass screening in six districts of Rwanda.

    Methods

    Study design

    The study is a secondary analysis of cross-sectional data collected during the 2019 screening campaign for viral hepatitis through the use of a standardised laboratory request form which contained sociodemographic, comorbidities and known viral hepatitis risk factors. HBV DNA and HCV RNA were also assessed.

    Setting

    The campaign was conducted at 60 health centres across six districts (10 by each district). Three districts were in Kigali which, in 2016, had a high prevalence of HIV infection (6%),17 HIV/HBsAg co-infection (5.0%) and HIV/anti-HCV co-infection (4%).16 One district was from Northern Province which, in 2017, was shown to have a high viremia rate of HCV (61.43%) among 9.11% screened anti-HCV positives.20 Two districts were from Western Province, which in 2016 had prevalence of 3% for both co-infection HIV/HBsAg and HIV/anti-HCV.16

    Patient and public involvement

    This analysis is performed on data collected as part of screening campaign. Patients/public were not involved in the design and interpretation of analyses presented in this paper.

    Study population and recruitment of participants

    At each of the 10 screening site health centres, individuals 15 years of age and older were invited to participate in viral hepatitis screening. Health centres were selected according to population size so that participants did not need to travel more than 2 km to the closest screening site. People who were not Rwandan by nationality or were under 15 years old were excluded. From April to May 2019, screening campaigns were conducted for 2 weeks in each district. This study included individuals who met the screening criteria of the targeted demographic groups and attended screening sites (health centres) for HCV and HBV testing. Patients who were diagnosed with one or more of these infections were referred to care and treatment services for further management.

    Data collection procedures

    After obtaining verbal consent, and verbal assent from parents or guardians of children aged 15–18 years, data on demographic, clinical and behaviour characteristics were obtained by trained nurses and laboratory technicians using a laboratory request form. Information regarding exposure to known risk factors of these infections included history of blood transfusions, surgical interventions, and traditional operations or scarifications. Other comorbidities, such as cardiovascular diseases, diabetes and cancer, were also collected.

    Testing methods

    Laboratory testing was performed using SD Bioline Rapid tests for anti-HCV with sensitivity of 98.9% and specificity of 99.7%24 and HBsAg with sensitivity of 90% and specificity of 99.5%.25 A team of laboratory technicians trained on viral hepatitis testing from the National Reference Laboratory supervised all testing activities. When laboratory results were available, the results and the contents of the laboratory request form were immediately entered in a password-protected database (Microsoft Excel database). Each day, blood samples from individuals testing positive on the HCV and/or HBV screening test collected at health centres were transferred immediately to HCV RNA and HBV DNA testing sites. HCV RNA and HBV DNA testing were performed at seven accredited laboratories serving as hubs of the National Reference. HCV RNA and HBV DNA testing were conducted using COBAS AmpliPrep/COBAS TaqMan HCV and HBV Test, V.2.0: Quantitative (Roche) with a lower limit of quantification of 15 IU/mL. HIV results were self-reported at screening site, but all participants who tested positive for HCV and HBV were retested for HIV using Alere HIV-Combo-Determine (Alere, Waltham) as the screening test and confirmed by HIV ½ STAT-PAK (Medford, NY, USA) if reactive. Results from these testing sites were entered into the database. The database was de-identified for the present study and the study team did not have access to patient identification information.

    Variables

    The outcomes of interest included chronic HCV infection, chronic HBV infection, HIV infection, co-infection HIV/HBV, co-infection HIV/HCV, co-infection HBV/HCV and co-infection HCV/HBV/HIV.

    Data were collected on sociodemographic characteristics including age, sex, urbanicity, socioeconomic status (Ubudehe category) and marital status. Age was categorised into five groups: less than 35 years old, 35–44 years old, 45–54 years old, 55–64 years old and over 65 years old. Urbanicity was defined as living in town or not. Socioeconomic status was categorised based on ‘Ubudehe’, a mechanism of the Rwanda Ministry of Local Government, whereby citizens are placed into different socioeconomic categories ranging from 1 to 4.26 27 The lowest socioeconomic category is 1 (poorest) and the highest is 4 (richest). For health insurance, only community-based health insurance (Mutuelle), la Rwandaise Assurance Maladie (RAMA) and Medical Military Insurance (MMI) were categorised separately; all other insurances were categorised as ‘private insurances’. The RAMA health insurance is a public-operated health insurance available to individuals currently and formally employed in both public and private sectors. Marital status was categorised into three groups of married, single and widowed, separated or divorced. Self-reported comorbidities assessed included cardiovascular diseases, diabetes, chronic renal failure and cancer.

    Assessed risk factors that were associated with parenteral routes of transmission included history of health facility–based surgical operation, traditional surgical operation and transfusion. Traditional surgical operation practices are defined as scarifications, male circumcision, tattoos, traditional dental extraction or uvulectomy done by a community member or traditional practitioner. Other assessed factors included the number of sexual partners and self-reported presence of diagnosed viral hepatitis of a family member. All these exposures to viral hepatitis risk factors were self-reported.

    The Medical Research Council of Rwanda controlled the ethical procedures for data collection and the authorisation to conduct these activities in different sites was obtained from the Ministry of Health. The approval for utilisation of these data was obtained by Rwanda Biomedical Center (No. 2048/RBC/2019) as this study concerned data collected during viral hepatitis screening and testing.

    Statistical methods and data analysis

    Data cleaning and analysis was conducted in SPSS V.20.0. In univariate analysis, we estimated the prevalence of mono-infections and co-infections, and described characteristics of study population. In bivariate analysis, Pearson χ2 test was used to test for association between categorical or binary variables and the seven outcomes of interest. Potential determinants for each outcome of interest were assessed in bivariable and multivariable models using logistic regressions.

    All variables in bivariate analyses were considered for inclusion in multivariable regression model if their inclusion was conceptually logical regardless of statistical significance or if their corresponding p value was <0.1. Variables were kept in the final model if they were significant at 5% level of significance. We reported ORs with their corresponding CIs.

    Results

    Data regarding participant characteristics and results for all three infections were available for 156 499 of the 164 225 campaign participants (95.3%). Those who were excluded was due to lack of data or not being in the target population.

    Sample characteristics

    Sociodemographic characteristics of participants included in the analysis are shown in table 1. The median age of participants was 35 years (IQR 18–58), with most participants (24.3%) in the group aged 25–34 years as shown in table 1. Most of the participants (67.1%) were female and 59.0% of participants were married. Half (50.2%) of participants were in Ubudehe category 3, and nearly all (94.0%) participants were enrolled in the community-based health insurance (Mutuelle). Over half (52.7%) were from rural districts. Among all participants, 4.4% had a history of operation at least once, and 10.2% had a history of traditional surgical and scarification practice while 5.2% of participants experienced physical trauma assault at least once.

    View this table:
    Table 1

    Descriptive characteristics of sociodemographic for participants tested

    Infection prevalence

    Overall, 3465 (2.2%) were HBsAg positive and of those, 2872 (82.9%) had HBV DNA detectable with median of 751 copies/mL (IQR 400–2500) of HBV DNA (figure 1). In addition, 4382 (2.8%) were anti-HCV positive and among them 3163 (72.2%) had HCV RNA detectable with a median of 567 000 copies/mL (IQR 300 000–580 000) of HCV RNA (figure 2). Overall, 4154 (2.7%) people reported being HIV positive. The highest prevalence of HBV infection (3.0%) was found in the group aged 35–44 years, the highest prevalence for HIV (5.2%) was found in the group aged 45–54 years and for HCV infection it was found in 65 years old and above (14.0%) (table 1). The highest prevalence of HIV was found in people who had more than one lifetime sexual partner, people who had experience of surgery and people who had been transfused with 8.1%, 6.9% and 6.5%, respectively. The highest prevalence of HBV was found in people who had a family relative or ever been diagnosed and in people who had experience of surgery with 4.9%, 3.6% and 3.3%, respectively. Finally, HCV was more common in people who had a family relative with HCV history and in people who had experience of traditional operation or scarification with 3.6% and 3.5%, respectively (table 2).

    View this table:
    Table 2

    Descriptive characteristics of risk factors and comorbidities for participants tested

    Figure 1
    Figure 1

    Distribution of quantity of hepatitis B virus (HBV) DNA copies by population. VL, viral load.

    Figure 2
    Figure 2

    Distribution of quantity of hepatitis C virus (HCV) RNA copies by population. VL, viral load.

    Characteristics of people with co-infection

    HIV/HBV co-infection was found in 158 participants (0.1%), HIV/HCV in 238 participants (0.15%) and HCV/HBV in 38 participants (0.02%). The triple infection HIV/HCV/HBV was found in three individuals (0.002%) of all participants. The highest prevalence for HBV/HCV/HIV co-infection (0.06%) and HBV/HIV co-infection (0.2%) were among people aged 35–44 years. The highest prevalence for HCV/HBV co-infection (0.07%), HCV/HIV co-infection (0.4%) and HBV/HIV co-infection (0.2%) was found in group of widows, divorced and separated. More details are shown in table 1.

    Factors associated with various infections

    Significant associations with HBV infection were being male (OR 1.77, 95% CI 1.64 to 1.90), living in town (OR 1.57, 95% CI 1.46 to 1.69), ever been diagnosed with liver disease (OR 1.92, 95% CI 1.53 to 2.40), history of surgical operation (OR 1.50, 95% CI 1.30 to 1.74), exposure to traditional operational practices and scarification (OR 1.57, 95% CI 1.41 to 1.74), and having a person in the family with viral hepatitis (OR 1.48, 95% CI 1.27 to 1.73).

    Significant association with HCV infection were being male (OR 1.17, 95% CI 1.07 to 1.27); being divorced, separated and widowed (OR 1.29, 95% CI 1.06 to 1.57); using other private insurance company (OR 3.15, 95% CI 2.26 to 4.39); ever been diagnosed with liver disease (OR 1.78, 95% CI 1.36 to 2.34); history of surgical operation (OR 1.39, 95% CI 1.19 to 1.63); and exposure to traditional operational practices and scarification (OR 1.44, 95% CI 1.29 to 1.60).

    Significant associations with HIV infection were being female (OR 1.18, 95% CI 1.09 to 1.27); living in town (OR 2.23, 95% CI 1.88 to 2.17); being in group of divorced, separated and widowed (OR 2.37, 95% CI 1.98 to 2.83), using other private insurance company (OR 3.08, 95% CI 2.25 to 4.21); ever been diagnosed with liver disease (OR 1.82, 95% CI 1.39 to 2.38); history of surgical operation (OR 1.42, 95% CI 1.21 to 1.66); history of physical traumatic assault (OR 1.69, 95% CI 1.51 to 1.88); and exposure to traditional operational practices and scarification (OR 1.48, 95% CI 1.33 to 1.65).

    HBV/HIV co-infections were significantly associated with living in town (OR 2.15, 95% CI 1.50 to 3.07), using other private insurance company (OR 6.41, 95% CI 3.10 to 13.24), ever been diagnosed with liver disease (OR 3.68, 95% CI 1.89 to 7.15), history of surgical operation (OR 2.06, 95% CI 1.25 to 3.40), exposure to traditional operational practices and scarification (OR 2.02, 95% CI 1.28 to 3.18), having more than one lifetime sexual partner (OR 2.02, 95% CI 1.28 to 3.18) and history of physical trauma assault (OR 1.82, 95% CI 1.08 to 3.05). HIV/HCV co-infection was associated with using other private insurance company (OR 3.24, 95% CI 1.32 to 7.94), ever been diagnosed with liver disease (OR 6.67, 95% CI 4.17 to 10.67), history of surgical operation (OR 2.01, 95% CI 1.32 to 3.07), and exposure to traditional operational practices and scarification (OR 1.50, 95% CI 1.07 to 2.12).

    However, lower odds were found for HBV and HCV infection in people who were transfused (OR 0.69, 95% CI 0.54 to 0.87 and OR 0.73, 95% CI 0.57 to 0.94, respectively). We also found lower odds for HIV/HBV co-infection and HIV infection in Ubudehe category 2 compared with category 1. Having civil servant health insurances and being in Ubudehe categories 3 and 4 (RAMA and MMI) were associated with a reduced odds of HIV infection. Lastly, people living in town were less likely to have HBV/HCV co-infection. More details on risk factors associated with all these co-infections are illustrated in table 3.

    View this table:
    Table 3

    ORs derived from a multivariable multivariate logistic regression model characterising the association of demographic, risk factor and comorbidity variables with HBV, HCV infection groups and their confections with HIV

    Discussion

    In this large population-based study in Rwanda, we characterised HBV, HCV and HIV co-infections. Overall, mono-infection with any of these viruses was more common and only 0.3% of people tested had double or triple co-infections with HIV/HBV, HIV/HCV or HIV/HBV/HCV. In addition to differences in the patterns of infections, we also found different patterns of risk factors for the different mono-infections and co-infections. For instance, having more than one lifetime sexual partner, being wounded by physical assault, healthcare exposures and urbanicity were associated with higher odds of HIV and HBV/HIV co-infection. On the other hand, rural residence and being in higher wealth category (Ubudehe categories 2, 3, 4) were associated with lower odds of HIV and HBV/HIV co-infection. Scarification, operation from traditional healers and surgical operations were associated with HCV. Lastly, HBV mono-infection risk was associated with family history of infection, urbanicity, operation from traditional healers and surgical operations. These data highlight that although there are some overlaps in risk factors, there are distinct patterns of transmission of these infections indicated by relatively low co-infection levels.

    In this study, we found low levels of the different co-infections of the three viruses. This is different from findings from other high-income or low-income and middle-income countries that showed higher rates of these co-infections. For instance, a study conducted in China among people with HIV found that 8.7% of participants had HBV/HIV co-infection, 18.2% had HCV/HIV co-infection and 3.3% triple infection.5 Another study in British Columbia found co-infection rates higher than those estimated in this study with HCV/HBV at 4.0%; HBV/HIV, 0.7%; HCV/HIV, 3.4%; and co-infection HBV/HCV/HIV at 1.2%.9 In contrast, a previous study conducted in Rwanda found very low prevalence of HBV/HCV/HIV among PLHIV (0.002%).16 In addition to Rwanda, our findings are also similar to findings of a study conducted in Libya that found low co-infections of HCV/HIV, HCV/HBV, HBV/HIV and HBV/HCV/HIV at 0.15%, 0.04%, 0.03% and 0.02%, respectively.11 This may relate to differences in patterns of risk factors in various population groups in which specific infections have high prevalence or differences in testing patterns of people with different risk profiles. It may also be due to who shows up for testing at the clinics (self-selection).

    Increased odds of HIV and HBV/HIV co-infections were associated with having more than one lifetime sexual partner, while decreased odds were associated with belonging to higher wealth category. Furthermore, living in urban area was also associated with HIV, HBV and HBV/HIV. These findings highlight that individuals with low socioeconomic status, those who live in urban areas and those having more than one lifetime sexual partner are at higher risk of HIV, HBV and their co-infections. Findings from another study conducted among HIV pregnant women in Rwanda showed that women from urban areas were more affected by HIV/HBV co-infection than those from rural areas.28 HIV shares the same mode of transmission as HBV infection, but the fact that they also share contextual risk factors including urbanicity and low socioeconomic status provides valuable information for their prevention, screening and treatment efforts in Rwanda. It means that strategies that work for one may be effective for both.

    Male sex was associated with higher risk of HCV and HBV. This may be due to greater mobility or involvement in armed conflict in this region of Africa. For HCV, this finding might be due to a greater number of traditional healing/surgeries and tattoos practised more by males than females. Higher odds for HBV were associated with higher frequencies of sexual encounters and, perhaps, more exposure to casual sex workers through mobile employment. These findings are similar to other studies done in Rwanda18 21 29 and in Burkina Faso.30 Contrary to HIV and HBV, HCV infection was more common in rural areas, and this is consistent with previous findings from Rwanda and other African countries.16 20 30 A study conducted in Kenya among people who inject drugs found higher prevalence of HCV and HCV/HIV co-infection in Coastal Kenya compared with Nairobi.31 The higher burden of unsafe medical practices by licensed practitioners and traditional healers could explain the higher prevalence of HCV in rural areas. Unsafe medical practices are known to be associated with HBV, HCV and HIV infections in different settings globally.32 33 The association of scarification and unsafe medical practices by traditional healers with higher odds of HBV and HCV has been previously described in Rwanda.21 29 Unfortunately, these unsafe practices are still highly prevalent in Rwanda. One notable example is male circumcision performed outside of a healthcare facility. The recent Demographic and Health Survey (DHS 2015) found that 10% of men across all age groups had been circumcised through unsafe practices.17 Taken together, these data show that there is an urgent need for improvement in infection control practices in the non-community setting.34 Although highly effective curative and suppressive therapy could treat infections and reduce the prevalence and new infections, optimising prevention of these infections is essential to achieve hepatitis elimination goal.

    This study has several limitations. First, the demographic profile of the sample population of voluntary participants differed from the Rwandan population at large, with a substantially greater proportion of women (67.1%) than the general population. Moreover, participants were from six districts only. Therefore, the prevalence estimates and risk factors found to be associated with HCV, HBV, HIV and their co-infections may not be generalisable to the entire Rwandan population and may have been underestimated. The study did not include data on certain known risk factors such as exposure to wars and other conflict resulting in sexual violence or refugee status, occupational risk and injection drug use. However, unlike high-income countries, the number of individuals who inject drugs are low in Rwanda.35

    Lastly, this study relied on routinely collected and self-report data to assess clinical variables (eg, history of diabetes) or historical exposure which may have led to misclassification due to imperfect recall. However, since infection status was not known at the time of interview, it is likely that recall is non-differential.

    Conclusions

    To conclude, prevalence of HBV, HCV and HIV infections in Rwanda are higher than many other countries. Overall, the majority of people with an infection had single infection with one of these viruses, with less than 0.3% having co-infections of HIV/HBV or HIV/HCV or HIV/HBV/HCV. Patterns of risk factors for mono-infection and co-infections differ. HIV and related co-infections are associated with high risk of sexual behaviours, urbanicity and healthcare risk factors, while HCV and related co-infections mostly are associated with rurality and unsafe medical practices. The findings from this study identify areas for strengthening prevention of bloodborne infections in Rwanda which is critical to achieving WHO elimination goals. These findings will also be informative for other countries in Sub-Saharan Africa that may have a context similar to Rwanda.

    Acknowledgments

    This study would not be possible without the contribution of participants in this campaign who provided the data used in this study, healthcare providers from health centres and hospitals where the screening took place. We would like to thank them. We also bring our thanks to the Ministry of Health and Rwanda Biomedical Center (RBC) staff and different partners for their special contribution and support to this study. Our thanks go also to Buller Taylor Terri for proof-reading this manuscript.

    References

    1. ↵
      1. Jefferies M,
      2. Rauff B,
      3. Rashid H, et al
      . Update on global epidemiology of viral hepatitis and preventive strategies. World J Clin Cases 2018;6:589–99.doi:10.12998/wjcc.v6.i13.589pmid:http://www.ncbi.nlm.nih.gov/pubmed/30430114
      OpenUrlPubMed
    2. ↵
      1. United Nations Programme on HIV/AIDS (UNAIDS)
      . UNAIDS data 2018, 2018: 1–376.
    3. ↵
      1. Singh KP,
      2. Crane M,
      3. Audsley J, et al
      . HIV–hepatitis B virus coinfection: epidemiology, pathogenesis, and treatment. AIDS 2017;31:2035–52.doi:10.1097/QAD.0000000000001574pmid:28692539
      OpenUrlCrossRefPubMed
    4. ↵
      1. Platt L,
      2. Easterbrook P,
      3. Gower E, et al
      . Prevalence and burden of HCV co-infection in people living with HIV: a global systematic review and meta-analysis. Lancet Infect Dis 2016;16:797–808.doi:10.1016/S1473-3099(15)00485-5pmid:http://www.ncbi.nlm.nih.gov/pubmed/26922272
      OpenUrlCrossRefPubMed
    5. ↵
      1. Zhang F,
      2. Zhu H,
      3. Wu Y, et al
      . HIV, hepatitis B virus, and hepatitis C virus co-infection in patients in the China national free antiretroviral treatment program, 2010–12: a retrospective observational cohort study. Lancet Infect Dis 2014;14:1065–72.doi:10.1016/S1473-3099(14)70946-6pmid:25303841
      OpenUrlCrossRefPubMed
    6. ↵
      1. Thornton AC,
      2. Jose S,
      3. Bhagani S, et al
      . Hepatitis B, hepatitis C, and mortality among HIV-positive individuals. AIDS 2017;31:2525–32.doi:10.1097/QAD.0000000000001646pmid:http://www.ncbi.nlm.nih.gov/pubmed/28926400
      OpenUrlCrossRefPubMed
    7. ↵
      1. Sullivan PS,
      2. Jones JS,
      3. Baral SD
      . The global north: HIV epidemiology in high-income countries. Curr Opin HIV AIDS 2014;9:199–205.doi:10.1097/COH.0000000000000039pmid:http://www.ncbi.nlm.nih.gov/pubmed/24445370
      OpenUrlCrossRefPubMed
    8. ↵
      1. WHO
      . Guidelines for the care and treatment of persons diagnosed with chronic hepatitis C virus infection. WHO, 2018.
    9. ↵
      1. McKee G,
      2. Butt ZA,
      3. Wong S, et al
      . Syndemic characterization of HCV, HBV, and HIV co-infections in a large population based cohort study. EClinicalMedicine 2018;4-5:99–108.doi:10.1016/j.eclinm.2018.10.006pmid:http://www.ncbi.nlm.nih.gov/pubmed/31193601
      OpenUrlPubMed
    10. ↵
      1. Japhet M,
      2. Adewumi M,
      3. Olufisayo A
      . PO 8585 HIV, HBV and HCV prevalence, co-infections, risk factors and awareness among students in a Nigerian University. BMJ Glob Health 2019;4:A59.1–A59.doi:10.1136/bmjgh-2019-EDC.155
      OpenUrl
    11. ↵
      1. Daw MA,
      2. Shabash A,
      3. El-Bouzedi A, et al
      . Seroprevalence of HBV, HCV & HIV co-infection and risk factors analysis in Tripoli-Libya. PLoS One 2014;9:e98793. doi:10.1371/journal.pone.0098793pmid:http://www.ncbi.nlm.nih.gov/pubmed/24936655
      OpenUrlPubMed
    12. ↵
      1. Ionita G,
      2. Malviya A,
      3. Rajbhandari R, et al
      . Seroprevalence of hepatitis B virus and hepatitis C virus co-infection among people living with HIV/AIDS visiting antiretroviral therapy centres in Nepal: a first nationally representative study. Int J Infect Dis 2017;60:64–9.doi:10.1016/j.ijid.2017.04.011pmid:http://www.ncbi.nlm.nih.gov/pubmed/28483724
      OpenUrlPubMed
    13. ↵
      1. Azevedo TCL,
      2. Zwahlen M,
      3. Rauch A, et al
      . Hepatitis C in HIV-infected individuals: a systematic review and meta-analysis of estimated prevalence in Africa. J Int AIDS Soc 2016;19:20711. doi:10.7448/IAS.19.1.20711pmid:http://www.ncbi.nlm.nih.gov/pubmed/27293220
      OpenUrlPubMed
    14. ↵
      1. Noubiap JJN,
      2. Aka PV,
      3. Nanfack AJ, et al
      . Hepatitis B and C co-infections in some HIV-positive populations in Cameroon, West central Africa: analysis of samples collected over more than a decade. PLoS One 2015;10:e0137375. doi:10.1371/journal.pone.0137375pmid:http://www.ncbi.nlm.nih.gov/pubmed/26371878
      OpenUrlPubMed
    15. ↵
      1. Rusine J,
      2. Ondoa P,
      3. Asiimwe-Kateera B, et al
      . High seroprevalence of HBV and HCV infection in HIV-infected adults in Kigali, Rwanda. PLoS One 2013;8:e63303. doi:10.1371/journal.pone.0063303pmid:http://www.ncbi.nlm.nih.gov/pubmed/23717409
      OpenUrlCrossRefPubMed
    16. ↵
      1. Umutesi J,
      2. Simmons B,
      3. Makuza JD, et al
      . Prevalence of hepatitis B and C infection in persons living with HIV enrolled in care in Rwanda. BMC Infect Dis 2017;17:1–7.doi:10.1186/s12879-017-2422-9
      OpenUrlCrossRefPubMed
    17. ↵
      1. National Institute of Statistics of Rwanda (NISR) [Rwanda], Ministry of Health (MOH) [Rwanda], and I International
      . Rwanda Demographic and Health Survey 2014–15, 2015.
    18. ↵
      1. Makuza JD,
      2. Rwema JOT,
      3. Ntihabose CK, et al
      . Prevalence of hepatitis B surface antigen (HBsAg) positivity and its associated factors in Rwanda. BMC Infect Dis 2019;19:1–10.doi:10.1186/s12879-019-4013-4
      OpenUrl
    19. ↵
      1. Republic of Rwanda, Ministry of Health, Rwanda Biomedical Center, U
      . National HIV/AIDS targets 2018-2020-2030: towards ending the AIDS epidemic in Rwanda by 2030, 2015: 1–29.
    20. ↵
      1. Umutesi J,
      2. Liu CY,
      3. Penkunas MJ, et al
      . Screening a nation for hepatitis C virus elimination: a cross-sectional study on prevalence of hepatitis C and associated risk factors in the Rwandan general population. BMJ Open 2019;9:e029743. doi:10.1136/bmjopen-2019-029743pmid:http://www.ncbi.nlm.nih.gov/pubmed/31272986
      OpenUrlAbstract/FREE Full Text
    21. ↵
      1. Makuza JD,
      2. Liu CY,
      3. Ntihabose CK, et al
      . Risk factors for viral hepatitis C infection in Rwanda: results from a nationwide screening program. BMC Infect Dis 2019;19:1–10.doi:10.1186/s12879-019-4322-7
      OpenUrl
    22. ↵
      1. Umutesi G,
      2. Shumbusho F,
      3. Kateera F, et al
      . Rwanda launches a 5-year national hepatitis C elimination plan: a landmark in sub-Saharan Africa. J Hepatol 2019;70:1043–5.doi:10.1016/j.jhep.2019.03.011pmid:http://www.ncbi.nlm.nih.gov/pubmed/30948269
      OpenUrlPubMed
    23. ↵
      1. Mendenhall E
      . Syndemics: a new path for global health research. Lancet 2017;389:889–91.doi:10.1016/S0140-6736(17)30602-5pmid:http://www.ncbi.nlm.nih.gov/pubmed/28271827
      OpenUrlPubMed
    24. ↵
      1. Shivkumar S,
      2. Peeling R,
      3. Jafari Y, et al
      . Accuracy of rapid and point-of-care screening tests for hepatitis C: a systematic review and meta-analysis. Ann Intern Med 2012;157:558–66.doi:10.7326/0003-4819-157-8-201210160-00006pmid:http://www.ncbi.nlm.nih.gov/pubmed/23070489
      OpenUrlCrossRefPubMed
    25. ↵
      1. Amini A,
      2. Varsaneux O,
      3. Kelly H, et al
      . Diagnostic accuracy of tests to detect hepatitis B surface antigen: a systematic review of the literature and meta-analysis. BMC Infect Dis 2017;17:698. doi:10.1186/s12879-017-2772-3pmid:http://www.ncbi.nlm.nih.gov/pubmed/29143619
      OpenUrlPubMed
    26. ↵
      1. National Institute of Statistics of Rwanda (NISR), M. of F. and E. P. (MINECOFIN) [Rwanda]
      . Rwanda Household, Integrated Survey, Living Conditions, 2015.
    27. ↵
      1. National Institute of Statistics of Rwanda (NISR) [Rwanda]
      . Rwanda Integrated Household Survey (EICV) 2013/2014, 2015.
    28. ↵
      1. Mutagoma M,
      2. Balisanga H,
      3. Malamba SS, et al
      . Hepatitis B virus and HIV co-infection among pregnant women in Rwanda. BMC Infect Dis 2017;17:618. doi:10.1186/s12879-017-2714-0pmid:http://www.ncbi.nlm.nih.gov/pubmed/28893207
      OpenUrlPubMed
    29. ↵
      1. Makuza JD,
      2. Liu CY,
      3. Ntihabose CK, et al
      . Risk factors for viral hepatitis C infection in Rwanda: results from a nationwide screening program. BMC Infect Dis 2019;19:688. doi:10.1186/s12879-019-4322-7pmid:http://www.ncbi.nlm.nih.gov/pubmed/31382901
      OpenUrlPubMed
    30. ↵
      1. Meda N,
      2. Tuaillon E,
      3. Kania D, et al
      . Hepatitis B and C virus seroprevalence, Burkina Faso: a cross-sectional study. Bull World Health Organ 2018;96:750–9.doi:10.2471/BLT.18.208603pmid:http://www.ncbi.nlm.nih.gov/pubmed/30455530
      OpenUrlPubMed
    31. ↵
      1. Akiyama MJ,
      2. Cleland CM,
      3. Lizcano JA, et al
      . Prevalence, estimated incidence, risk behaviours, and genotypic distribution of hepatitis C virus among people who inject drugs accessing harm-reduction services in Kenya: a retrospective cohort study. Lancet Infect Dis 2019;19:1255–63.doi:10.1016/S1473-3099(19)30264-6
      OpenUrl
    32. ↵
      1. Janjua NZ,
      2. Hamza HB,
      3. Islam M, et al
      . Health care risk factors among women and personal behaviours among men explain the high prevalence of hepatitis C virus infection in Karachi, Pakistan. J Viral Hepat 2010;17:317–26.doi:10.1111/j.1365-2893.2009.01230.xpmid:http://www.ncbi.nlm.nih.gov/pubmed/20002559
      OpenUrlPubMed
    33. ↵
      1. Kandeel AM,
      2. Talaat M,
      3. Afifi SA, et al
      . Case control study to identify risk factors for acute hepatitis C virus infection in Egypt. BMC Infect Dis 2012;12:1. doi:10.1186/1471-2334-12-294
    34. ↵
      1. Janjua NZ,
      2. Butt ZA,
      3. Mahmood B, et al
      . Towards safe injection practices for prevention of hepatitis C transmission in South Asia: challenges and progress. World J Gastroenterol 2016;22:5837.doi:10.3748/wjg.v22.i25.5837pmid:http://www.ncbi.nlm.nih.gov/pubmed/27433097
      OpenUrlPubMed
    35. ↵
      1. Rwanda Biomedical Center/Institute of HIV/AIDS, Disease Prevention and Control Department (RBC/IHDPC), S. & of Public Health (SPH), UNAIDS, and I. I
      . Estimating the size of populations through a household survey, 2012.

    Footnotes

    • Twitter @makuza_jean

    • Contributors JDM is the principal author of this manuscript in all phases from the conception to the submission, data collection, data analysis and manuscript writing. JDM, MPN, JOTR, DSH and SN elaborated the study protocol and study design. JDM, DD, SU, AN and JS collected data. NZJ, MPN and MS contributed significantly in design of analysis presented in this paper. JDM, MPN, MS and NZJ carried out the data analysis and developed the figure and tables. All authors participated in interpretation of the data. JDM and NZJ conducted the literature review and wrote the first draft of the manuscript. MPN, JOTR, DSH, SU, JS, AN, MS, NG and NZJ reviewed and provided critique of the manuscript.

    • Funding The Screening of hepatitis B and C virus was funded by the Government of Rwanda, but the realisation of this study was conducted by authors without any additional funding.

    • Competing interests None declared.

    • Patient and public involvement Patients and/or the public were involved in the design, or conduct, or reporting, or dissemination plans of this research. Refer to the Methods section for further details.

    • Patient consent for publication Not required.

    • Ethics approval The ethical procedures for data collection were controlled by the Medical Research Council of Rwanda and the Ministry of Health gave authorisations for hosting sites. The approval from the ethical committees was not necessary as this study used secondary data and the authorisation to use data was given by Rwanda Biomedical Center.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Data availability statement The data sets generated during the current study are not publicly available, but are available from the corresponding author on reasonable request.