Risk factors for viral hepatitis C infection in Rwanda: results from a nationwide screening program

The study consists of a secondary analysis of cross-sectional data collected during the 2018 screening campaign for HCV. All data used for analysis were collected at the time of viral hepatitis screening through use of a standardized laboratory request form which contained sociodemographic, comorbidities and viral hepatitis risk factors characteristics.

In response to the global and regional urgency to address HCV and improve understanding around HCV epidemiology, the Rwanda Biomedical Center (RBC) and partners prepared screening campaigns to identify infected patients to be linked to a free of charge treatment. In 2018, campaigns were specifically conducted in districts previously found to have higher prevalence of HCV among the general population and targeted individuals aged 25 years old and above from districts in Southern, Eastern and Northern Provinces previously found to have higher prevalence. The study population consists of voluntary participants of the 2018 campaigns. People who were not Rwandan by nationality or under 25 years old were excluded. Screening campaigns were conducted between March to October 2018 for 2 weeks in each district. Community awareness for viral hepatitis screening was done by radio advertisements and with the help of community health workers before and during the screening period. Individuals who belonged to targeted demographic groups and attended screening sites (health centers) were screened for HCV and included in the study population of this analysis.

Trained nurses and laboratory technicians, using a laboratory request form to record demographic, clinical, and behavior characteristics, collected samples after verbal consent of participants. Unlike previous campaigns, the 2018 campaign asked individuals about their exposure to a list of known risk factors for HCV including history of undergoing health treatments such as blood transfusions, surgical interventions and traditional operations or scarifications and comorbidities such as TB, diabetes and cancer. Testing was performed at 13 sites across Rwanda using Murex enzyme-linked immunosorbent assays (ELISA) for HCVAb (version 4.0; DiaSorin S.p.A, Italy). A team of laboratory technicians from the National Reference Laboratory supervised all testing activities. When laboratory results were available, the results and the contents of the lab request form were entered into an encrypted database (Microsoft Excel). The database was de-identified for the present study and no persons involved in the analysis of data were able to access the linked database.

The primary outcome of interest was HCVAb seroprevalence; it was a binary variable of either positive or negative as determined by the ELISA test. Independent variables included age. Age was considered as continuous variable during analysis then categorized 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. Then sex, screening district, marital status and socioeconomic status (Ubudehe category). Ubudehe is a development programme whereby citizens are placed into different socioeconomic categories. The lowest socioeconomic category is 1 and the highest is 4. Socioeconomic status was defined in accordance with the updated Ubudehe category by the Ministry of Local Government of Rwanda (MINALOC) [14]. The households that consume less than Rwandan Francs (RWF) 105,064 [equivalent to USD 120] per year are classified in Ubudehe Category 1 (poorest category), which includes people without houses and those affected by food insecurity. Households that consume between RWF 105,064 and RWF 159,375 (exclusively) [equivalent to USD 180] per year are in Ubudehe Category 2, which includes households subsisting on manual labor or temporary employment and those capable of renting or owning their own houses. Categories 1 and 2 receive government assistance. Households that consume more than or equal to RWF 159,375 are classified in Ubudehe Category 3 and 4 [15]. These categories are not considered poor and do not receive government assistance. Category 3 includes wealthy farmers and investors while Category 4 includes large business owners and highly ranked government officials [16]. For health insurance, only community-based health insurance (Mutuelle), la Rwandaise Assurance Maladie (RAMA), and Medical Military Insurance (MMI) were categorized separately; all other insurances were categorized as “private insurances”. The RAMA health insurance is a privately operated health insurance available to individuals formally employed in the both the public and private sectors. Marital status was categorized into three groups of married, single and widowed, separated or divorced. HIV status as well as comorbidities and exposures to HCV risk factors were self-reported. Self-reported comorbidities assessed included high blood pressure (HBP), diabetes, chronic renal failure (CRF), cancer, tuberculosis (TB). Risk factors assessed 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 risk factors assessed were number of sexual partners and self-reported presence of diagnosed viral hepatitis in a family member.

Data was de-identified and after data cleaning, data were transferred and analyzed using SPSS version 20.0. Pearson Chi-square tests were used to test for association between HCVAb seroprevalence and other categorical or binary variables. Potential determinants of HCV infection were assessed in bivariate and multivariable models using logistic regressions with HCVAb seroprevalence as the outcome variable. Multivariate analysis was used to determine socio-demographic, behavioral and clinical factors that were independently associated with HCVAb Seroprevalence.

The RBC of HIV/AIDS, STIs and Other Blood Borne Infections maintains the routinely collected program data analyzed for this study. The Medical Research Council of Rwanda governed the ethical procedures for the collection of these data and we obtained the authorization from the Ministry of Health to host the activities at different sites. The approval for utilization of data was obtained by Rwanda Biomedical Center (No 2407/RBC/2019).

The total number of individuals screened was 327,383; 326,263 (99.7%) received their results of which 22,183 (6.8%) screened positive for HCVAb. There were 1120 (0.3%) individuals without results due to drop-out??, insufficient blood sample, or indeterminate result. Socio-demographic characteristics of the study population are shown in Table 1. The mean age of participants was 44.8 years. There were 145,537 (45.8%) individuals older than 45 years of age, 224,382 (68.8%) whom were female, and 247,437 (77.5%) whom were married. 149,092 (45.5%) were in Ubudehe category 3. The vast majority of participants 303,206 (93.6%) were using community-based health insurance (Mutuelle). The province with the highest number of individuals screened was Eastern Province where 110,337 (35.0%) of participants were screened.

Table 2 shows self-reported clinical characteristics and historical exposures of participants. Among comorbidities, 1867 (0.6%) reported diabetes, 9510 (2.9%) reported high blood pressure (HBP), 578 (0.2%) reported chronic renal failure (CRF), 293 (0.2%) reported cancer, 6597 (2%) reported HIV-positive status, and 338 (0.1%) reported a history of tuberculosis. Among self-reported historical exposures to risk factors, 17,876 (5.6%) were surgically operated upon at least once, 5350 (1.6%) received a blood transfusion at least once, 54,097 (16.6%) had history of a traditional surgical practice, 8755 (2.7%) had multiple sex partners (either current or historical), and 6190 (1.9%) had a family member diagnosed with viral hepatitis. Among all variables, no variables had > 5% missing values.

In the multivariate analysis as shown in Table 3, being a male was statistically associated with HCVAb Seroprevalence [adjusted-OR (aOR) = 1.06, 95%CI:(1.03–1.10)]. Age greater than 65 years old [aOR = 4.87, 95%CI:(4.62–5.11)], and widowed/ separated and divorced marital status [aOR = 1.36, 95%CI:(1.26–1.47)] were both associated with HCV Ab Seroprevalence. Having RAMA as health insurance had lower odds of HCVAb seroprevalence compared to those on Community based health insurance [aOR = 0.78, 95%CI:(0.70–0.85)] and being in Ubudehe Category 3 and 4 had lower odds of HCVAB seroprevalence than being in Ubudehe category 1 [aOR = 0.92 95%CI:(0.88–0.96)]. Relative to the Northern Province, all other provinces had a significantly higher seroprevalence in the Western Province, Southern Province and Eastern Province [aOR = 1.37, 95%CI:(1.31–1.43)]. Self-reported co-morbidities found to be associated with HCVAb prevalence included high blood pressure (aOR = 1. 95%CI:(1.13–1.31)] and CRF (aOR = 1.29, 95%CI:(1.16–1.44)]. Self-reported risk factors associated with HCVAb prevalence were history of traditional surgical practices (aOR = 1.09, 95%CI:(1.05–1.14)] and history of a family member diagnosed with viral hepatitis (aOR = 1.27, 95%CI: (1.15–1.40)].