Abstract
In a representative nationwide study, we have determined the prevalence of hepatitis B virus (HBV) and hepatitis C virus (HCV) coinfections among HIV-positive patients diagnosed during the period 2010–2014 in Bulgaria. Despite a relatively low rate of new HIV diagnoses, the rates of hepatitis B and C coinfections among these patients fell within the upper range reported in Europe. HBsAg and HCV antibodies (Ab) were found in 10.4% and 25.6% of the tested individuals, respectively. Importantly, high rates of active hepatitis infections were confirmed by detection of HBV DNA in 51.1% and HCV RNA in 78.1% of the tested individuals. Hepatitis coinfections affected mostly high risk groups and persons with multiple risk behavior, including people who inject drugs, men who have sex with men, prisoners, and Roma people.
B
Out of 934 HIV-1+ cases, 404 were heterosexual (HET), 312 were MSM, and 218 were PWIDs (Table 1). Together, prisoners and Roma people represented a significant share of 28.5%. ELISA tests for HBsAg and for HCV antibodies (Ab) were performed in almost 85% of the HIV/AIDS patients, yielding a positive result in 10.4% and 25.6% of the cases, respectively. In 31 patients, double HBV/HCV coinfection was detected. Polymerase chain reaction (PCR) tests were conducted for 57.3% of the HBsAg+ and 74.4% of the HCVAb+ patients. HBV DNA was detected in 51.1% and HCV RNA in 78.1% of the tested. Thus, the rates of HBV and HCV coinfections among people living with HIV (PLHIV) were much higher than the estimates for the general Bulgarian population and fell within the upper range reported in Europe. 3
HBV, hepatitis B virus; HCV, hepatitis C virus; HET, heterosexual individuals; MSM, men who have sex with men; PWIDs, persons who inject drugs.
While men prevailed among the new HIV/AIDS cases, HBV and HCV coinfections were not gender associated. Coinfections were most frequent in the capital city of Sofia (33% of HBsAg+ and 45% of HCVAb+ cases) and the second largest town of Plovdiv (28% and 27%, respectively). Positive serology results were much more frequent in PWIDs than in HET and MSM: 20.6% HBsAg+ and 87.4% HCVAb+ tests vs. 8.2% and 14.3% for HET and 8.4% and 3% for MSM, respectively (p < 0.001). Importantly, 44.4% of the PCR-tested PWID were HBV-DNA+ and 81.9% were HCV-RNA+, indicating a high level of active viral replication within this group. A significantly higher rate of active HCV infections was detected among HIV+ MSM injecting drugs, compared to MSM alone (88.9% vs. 50% of the tested). In contrast, the frequency of active HBV infection was highest among MSM (42% vs. 33% for PWIDs and 25% for HET) underlining the importance of follow-up for HBsAg+ MSM, including HBV DNA testing. Prisoners and Roma people were at increased risk for both HBV and HCV infection. Active HBV replication was significantly more frequent among prisoners compared to Roma people (75% vs. 42.1%, p < 0.001) despite similar rates of HBsAg-positivity (16.9% and 17.4%, respectively, p > 0.05), and close to that in MSM. The rates of active HCV infections were high in both risk groups (73.3% and 76.6%, respectively), and similar to those in PWID.
In conclusion, this nationwide representative study revealed unexpectedly high rates of HBV and HCV coinfections among PLHIV in Bulgaria. As a marker of parenteral drug use, high HCV rates indicated a PWID-driven epidemic among vulnerable groups with multirisk behavior, such as Roma people and prisoners. Since HBV and HCV coinfections in PLHIV are associated with disease progression and reduced survival, the adequate laboratory and epidemiological monitoring of these multirisk groups are essential for both patients' management and public health protection.
Ethics Statement
Studies were conducted during diagnostic process. All patients provided written informed consent to participate in this study approved by the Ethics Committee at the National Center of Infectious and Parasitic Diseases, Sofia, Bulgaria (NCIPD IRB IORG00006384).
Footnotes
Acknowledgments
This study was funded, in part, by Bulgarian Ministry of Health Directorate “Management of Specialized Donor-funded Programs” and National Center of Infectious and Parasitic Diseases, Sofia, Bulgaria. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the article.
Author Contributions
I.A., P.T., and M.N. conceived and designed the study; E.G.-M. and A.K. performed the experiments; I.A., P.T., M.A., I.E., P.T., E.G.-M., and M.N. analyzed the data; A.G., R.D., A.K., and E.G.-M. contributed with reagents/materials/analysis tools; and I.A., P.T., M.A., and M.N. wrote the article.
Author Disclosure Statement
No competing financial interests exist.