HBV and HCV infections are widespread among the HIV-infected individuals in Nepal. The goals of this study were to investigate the epidemiological profile and risk factors for acquiring HBV and/or HCV coinfection in disadvantaged HIV-positive population groups in Nepal. We conducted a retrospective study on blood samples from HIV-positive patients from the National Public Health Laboratory at Kathmandu to assay for HBsAg, HBeAg, and anti-HCV antibodies, HIV viral load, and CD4+ T cell count. Among 579 subjects, the prevalence of HIV-HBV, HIV-HCV, and HIV-HBV-HCV coinfections was 3.62%, 2.93%, and 0.34%, respectively. Multivariate regression analysis indicated that spouses of HIV-positive migrant labourers were at significant risk for coinfection with HBV infection, and an age of >40 years in HIV-infected individuals was identified as a significant risk factor for HCV coinfection. Overall our study indicates that disadvantaged population groups such as intravenous drug users, migrant workers and their spouses, female sex workers, and men who have sex with HIV-infected men are at a high and persistent risk of acquiring viral hepatitis. We conclude that Nepalese HIV patients should receive HBV and HCV diagnostic screening on a regular basis.
Globally, as of 2015, 240 million people are living with chronic HBV infection [
Many individuals in disadvantaged population groups lack awareness of and are poorly educated about preventive measures for infection-avoidance. Unfortunately, the postinfection clinical and health status for many of these individuals is unknown. Contemporary data regarding infection and health status inside these populations of HIV-infected individuals is poor. The collection and analysis of an increased amount of scientifically sound data are imperative to inform the design of public-health policies and to help establish more effective outreach programs. This current study aims to investigate the epidemiological features of HBV and/or HCV coinfection among HIV-infected populations and thereby help identify risk factors for coinfection.
A retrospective study was conducted using blood samples collected from HIV-positive individuals at the Nepalese National Public Health Laboratory (NPHL), Nepal, during January–December 2015. With consent from NPHL officials, 682 samples were retrieved blindly from the blood sample archive, and 579 were deemed fit for our study. Relevant demographic information and laboratory values were retrieved from the clinical record files of each individual patient. Exclusion criteria included age below 18 years, plasma sample volume <50
At the time of patient visit, 5 ml venous blood was drawn by a certified phlebotomist and collected in EDTA tubes (BD, USA). The collected whole blood (1/3rd) underwent CD4+ T cell count, and the remainder was centrifuged at 3000 rpm for 5 min at RT. After centrifugation, blood plasma (2/3rd) was used for routine biochemical and HIV viral load assays, while the remaining plasma (1/3rd) was transferred to 1.8 ml cryo-vial (Abdos, India) and stored at −20°C until further analysis.
Twenty microliters of Tritest CD3/CD4/CD45 reagent (BD, USA) along with 50
HIV RNA was isolated from 140
Plasma samples stored at −20°C were thawed to room temperature (25°C) and used for HBsAg, HBeAg, and anti-HCV antibody detection by ELISA (Wantai Co., China). All ELISA was performed under sterile condition according to manufacturer’s instructions. Positive and negative controls were supplied in the kit and the cut-off values for the respective tests were defined according to the manufacturer’s instructions.
All data was analysed using SPSS software version 23.0. Frequencies were calculated for categorical variables and mean ± SD were calculated for quantitative variables.
Of the 579 HIV-positive patients enrolled in this study, 72.19% were men and 0.34% transgender, with a male/female ratio of 2.6 : 1. The age-range of the study subjects was 18–65 years with a mean of 39.13. The prevalence of HIV-HBV, HIV-HCV, and HIV-HBV-HCV coinfections was found to be 3.62%, 2.93%, and 0.34%, respectively. HIV-positive males were coinfected with either HBV or HCV at a higher rate (2.2%) than HIV-positive females (1.3%). Adults 21–59 years of age were observed to be at increased risk of HBV and/or HCV coinfection compared to those in younger (18–20 years) and older (60–65 years) age groups (
Epidemiological characteristics of HBV and HCV infections in 579 HIV-infected patients in Nepal.
Characteristic | Anti-HBsAg+ |
Anti-HCV IgM+ |
---|---|---|
|
||
<20 | 5 (0.86) | 1 (0.17) |
21–40 | 7 (1.20) | 6 (1.03) |
41–59 | 8 (1.38) | 8 (1.38) |
>60 | 1 (0.17) | 2 (0.34) |
Total | 21 | 17 |
|
4.422 | 7.853 |
|
0.219 |
|
|
||
Male | 13 (2.24) | 13 (2.24) |
Female | 8 (1.38) | 4 (0.69) |
Transgender | — | — |
|
1.292 | 0.203 |
|
0.524 | 0.903 |
|
403.19 ± 328.53 | 272.04 ± 181.82 |
Marital status | ||
Married | 13 (2.24) | 14 (2.41) |
Unmarried | 8 (1.38) | 2 (0.34) |
Divorced | — | 1 (0.17) |
Widowed | — | — |
|
5.583 | 10.304 |
|
0.134 |
|
|
||
Postsecondary school | 3 (0.51) | 1 (0.17) |
Secondary school | 9 (1.55) | 8 (1.38) |
Primary school | 4 (0.69) | 3 (0.51) |
Illiterate | 5 (0.86) | 5 (0.86) |
|
2.965 | 5.468 |
|
0.397 | 0.141 |
|
||
Labour migrants | 3 (0.51) | — |
Blood transfusion | 1 (0.17) | — |
Female sex worker | 2 (0.34) | — |
Intravenous drug user | 3 (0.51) | 15 (2.59) |
Male sex worker | 5 (0.86) | 2 (0.34) |
Spouse of labour migrants | 5 (0.86) | — |
Transvertical | 2 (0.34) | — |
|
20.83 | 51.564 |
|
0.022 |
|
The subject’s age, body mass index, sex, geographical location, current ART regime, key population category, HIV viral load, education level, marital status, ART duration, and CD4+ T cell count were included in a univariate logistic regression model, where HIV/HCV and HIV/HBV coinfection were dependent variables. The univariate analysis showed that being a spouse of a migrant labourer (OR: 4.33, 95% CI: 1.03–21.65), female sex worker (OR: 4.96 95% CI: 0.62–31.61), intravenous drug user (OR: 1.45, 95% CI: 0.26–7.96), male sex worker (OR: 2.01 95% CI: 0.49–10.13), or having an HCV positive status (OR: 3.81, 95% CI: 0.57–14.84) positively correlated with HIV/HBV coinfection. Additionally, an age > 40 years (OR: 1.04, 95% CI: 1.00–1.09) or male gender (OR: 1.24, 95% CI: 0.43–4.46) positively correlated with HIV/HCV coinfection (
Univariate analysis of factors affecting HBV and HCV infection in 579 HIV-infected subjects in Nepal.
Parameters | HIV HBV coinfection | HIV HCV coinfection | ||
---|---|---|---|---|
OR |
|
OR |
|
|
|
||||
≤40 | 1 | 1 | ||
>40 |
|
0.888 |
|
|
|
|
0.864 |
|
0.209 |
|
||||
F | 1 | 1 | ||
M |
|
0.275 |
|
0.707 |
Transgender | 0.99 | — | 0.991 | |
|
||||
Baglung | 1 | 1 | ||
Banke |
|
0.377 | — | |
Chitwan |
|
0.0778 | — | |
Kailali |
|
0.1633 | — | |
Kaski |
|
0.1973 | — | |
Kathmandu |
|
0.1496 | — | |
Tanahun |
|
0.5506 | — | |
|
||||
1st | 1 | 1 | ||
2nd |
|
|
|
0.439 |
|
||||
Labour migrants | 1 | 1 | 1 | |
Blood transfusion | — | — | 1 | |
Female sex worker |
|
0.0883 | — | 1 |
Intravenous drug user |
|
0.6519 | — | 0.99 |
Male sex worker | 2.01 (0.49–10.13) | 0.33 | — | 0.99 |
Spouse of labour migrants |
|
|
— | 1 |
Transvertical |
|
0.1253 | — | 1 |
|
|
|
0.707 | |
|
||||
Negative |
|
|||
Positive |
|
0.0896 | ||
|
||||
Negative |
|
|||
Positive |
|
0.0896 | ||
|
||||
Illiterate |
|
|
||
Postsecondary |
|
0.457 |
|
0.131 |
Primary |
|
0.511 |
|
0.316 |
Secondary |
|
0.517 |
|
0.674 |
|
||||
Divorced | 1 |
|
||
Married |
|
|
||
Unmarried |
|
0.0808 | ||
Widowed | — | 1 | — | 0.9894 |
|
|
|
|
0.946 |
|
||||
<200 | 1 | 1 | ||
>200 |
|
0.214 |
|
|
Risk factors observed by the univariate model were then analysed in a multivariate logistic regression model using stepwise regression analysis. Multivariate analysis showed a higher prevalence of HIV/HBV coinfection in certain key population groups, such as female sex worker (OR: 5.25, 95% CI: 0.82–33.60) and spouses of migrant labourers (OR: 4.01, 95% CI: 0.92–17.40), than in other at-risk population groups (Table
Multivariate analysis of factors affecting HBV and HCV infection in 579 HIV-infected subjects in Nepal.
HIV HBV | HIV HCV | ||||||
---|---|---|---|---|---|---|---|
Parameters | OR | 95% CI |
|
OR | 95% CI |
|
|
Blood transfusion | 0.24 | 0.12–0.44 | — |
|
1.04 | 1.00–1.09 |
|
Female sex worker | 5.25 | 0.82–33.60 | 0.0797 | Marital status (married) | 0.18 | 0.01–2.82 | 0.2263 |
General population | 0.0000 | — | Marital status (unmarried) | 0.23 | 0.01–5.14 | 0.3560 | |
Housewife | 0.0000 | — | Marital status (widowed) | — | — | 0.9905 | |
Intravenous drug user | 1.45 | 0.28–7.35 | 0.6512 | CD4 count > 200 cells/mm3 | 0.19 | 0.06–0.52 |
|
Male sex worker | 2.08 | 0.48–8.89 | 0.3230 | ||||
General spouse | 0.0000 | — | |||||
Spouse of intravenous drug user | 0.0000 | — | 0.9953 | ||||
Spouse of migrant | 4.01 | 0.92–17.40 |
|
In South Asia, the prevalence of HBV and/or HCV seropositivity among HIV-positives varies distinctively by location. In North India, HBV seropositive cases are reported as high as 6.2% and HCV seropositive cases as low as 1.56% among HIV-infected individuals [
Among HIV-positives worldwide, key disadvantaged populations have a more frequent exposure to HBV and HCV infection due to engagement in high-risk behaviours, weak family and social support systems, and inadequate access to healthcare services [
A study carried out in Nepal during 2010-2011 reported that the prevalence of HBV and HCV confections among the HIV-positive population was 4.4% and 19%, respectively [
Our study shows that coinfection with HBV and/or HCV is a serious health concern for HIV-infected members of disadvantaged population groups in Nepal. Further, our study suggests that spouses of migrant workers and female sex workers have increased risk of acquiring HBV and/or HCV. We highly recommend improved measures to ensure routine screening for HBV and HCV infection among HIV patients and their family members in Nepal. Such a diagnostic strategy could serve to decrease overall disease prevalence and promote better health among both at-risk groups and the general population.
Hepatitis B virus
Hepatitis C virus
Acquired immunodeficiency syndrome
Sexually transmitted diseases
Female sex worker
Intravenous drug user
Male sex worker
Human immunodeficiency virus
Intravenous drug user
Antiretroviral therapy
Cluster of differentiation
Body mass index
Ethylene diamine tetra acetic acid
Room temperature
Fluorescence activated cell sorter
Complementary deoxyribose nucleic acid
T helper 17 cell.
This study was approved by the Ethical Committee of Nepal Health Research Council (NHRC) [Ref. no. 172/2015]. All the data from human subjects were gathered and conducted for this publication under an NHRC IRB approved protocol.
The authors declare that there are no conflicts of interest regarding the publication of this paper.
Jagat Bahadur Baniya and Nirmal Aryal enrolled patients and performed the lab work. Manjula Bhattarai designed the study, analysed and interpreted the data, and drafted the manuscript. Anurag Adhikari, Bimal Shrestha, Ramanuj Rauniyar, Pratik Koirala, Pardip Kumar Oli, Ram Deo Pandit, David A. Stein, and Birendra Prasad Gupta analysed and interpreted the data and drafted the manuscript. Manjula Bhattarai and Jagat Bahadur Baniya contributed equally to this work.
The authors would like to thank the staff of the National Public Health Laboratory (NPHL) for their cooperation and expertise during data acquisition.