Seroprevalence of hepatitis B virus/hepatitis C virus among human immunodeficiency virus-infected patients at a tertiary care teaching hospital in Mangalore, South India

Background: The human immunodeficiency virus (HIV) pandemic has continued to be a major public health problem even after more than three and a half decade of existence. According to the World Health Organization estimates,  36.7 million people were living with HIV by 2015 end while chronic infection of hepatitis B virus (HBV) and hepatitis C virus (HCV) occurs in 240 and 130–150 million people worldwide, respectively. Since the general modes of transmission are similar to HIV, coinfection of HIV with HBV/HCV is commonly found, being variable worldwide. Aims and Objectives: The aims and objectives of this study were (1) To investigate the seroprevalence of HBV/HCV in HIV-positive patients and (2) To analyze the demographic pattern and laboratory parameters. Settings and Design: This was a descriptive cross-sectional study. Materials and Methods: The serum samples from confirmed HIV-positive patients were screened and confirmed for HBV and HCV following standard operative procedures. The demographic pattern and laboratory parameters were also obtained. Statistical Analysis Used: SPSS software version 23.0 was used for statistical analysis. Results: The seroprevalence of HBV and HCV in HIV-positive patients was found to be 6.6% and 0.7%, respectively. Males (n = 7) were more commonly infected than females (n = 3) with the age group of 31–40 years being the most common and majority were married (n = 9). In HBV-HIV coinfection, the mean values of serum globulin, serum total bilirubin, conjugated bilirubin, aspartate amino-transferase, alanine aminotransferase (ALT), and alkaline phosphatase were increased, but in the only case of HCV-HIV coinfection, only hemoglobin and platelet count were decreased. A majority (n = 8) improved on discharge. Conclusions: The seroprevalence of HBV/HCV was high with laboratory test showing a significant correlation between HBV-HIV coinfection and serum globulin and ALT. Hence, creating awareness, understanding these diseases, and providing screening test in suspected individuals is the need of the hour which will improve the mortality rates related to them.

Keywords: Acquired immune deficiency syndrome, antiretroviral therapy, hepatitis B virus, hepatitis C virus, human immunodeficiency virus

The human immunodeficiency virus (HIV) pandemic has continued to be a major public health problem even after more than three and a half decade of existence. According to the World Health Organization (WHO) estimates, there were 36.7 million people living with HIV by 2015 end. In 2015, 1.1 million people died of AIDS-related illnesses.^[1] At the same time, it was also found that hepatitis B virus (HBV) chronically infects 240 million people worldwide, of which death due to complications occur in more than 686,000 every year.^[2] HBV is the leading cause of chronic liver disease worldwide, transmitted primarily through sexual contact, horizontal transmission, percutaneous and mucosal exposure to blood and body fluids, medical procedures, and tattooing and injecting drug, but in higher prevalence regions, the common routes of transmission include perinatal and early childhood exposures.^[3],[4],[5] Hepatitis C virus (HCV) chronically infects 130–150 million people worldwide, of which 700,000 people die of related liver diseases.^[6] It is transmitted by percutaneous exposure to blood and blood products, through sexual intercourse, and from a mother to her infant where HCV transmission is increased when mothers are HIV coinfected, reaching rates of 10% to 20%.^[7],[8] Since the general modes of transmission are similar to HIV, coinfection of HBV/HCV in HIV patients occurs and are commonly found in HIV-infected individuals. The coinfection rates of HBV/HCV reported in HIV-infected patients have been variable worldwide depending on the geographical region, risk groups, and types of exposure involved. The majority of cases occur in Asia and Africa.^[2],[8],[9] HBV/HCV coinfection in HIV has an enormous effect on the outcome of infected individuals and greatly complicates their management, resulting in greater mortality mainly due to liver cirrhosis and liver cancer than those infected with HIV alone. Moreover, reports suggest that the mortality is highest among those with multiple hepatitis infections.^[10] To the best of our knowledge, there is no published study conducted from in and around coastal Karnataka to evaluate the seroprevalence of coinfection of HBV/HCV in HIV-positive patients. Hence, this study was conducted in a tertiary care teaching hospital to determine the seroprevalence of HBV/HCV coinfection in HIV-positive patients and also to determine the relation of laboratory parameters in these infected individuals.

Objectives of the study

1. To investigate the seroprevalence of HBV/HCV in HIV-positive patients in a tertiary care teaching hospital in South India
2. To analyze the demographic pattern including age, sex, marital status, and the outcome of these cases
3. To determine the relation of hemoglobin (Hb), platelet count, and liver function test (LFT).

Study population

A prospective cross-sectional study was carried out in a tertiary care teaching hospital in South India by the Department of Microbiology for 2 years from August 2013 to July 2015, where approval from the Institutional Ethics Committee was obtained. Patients included in the study were those of confirmed known cases of HIV and those screened and confirmed as per National AIDS Control Organization (NACO) guidelines,^[11] who were admitted in the hospital, willing to participate in the study, and were then tested for HBV/HCV infection after counseling and obtaining informed consent. The information related to age, sex, and marital status, laboratory parameters including Hb levels, platelet count, LFT, and outcome were also noted.

Detection of cases was done by standard operative procedures: the serum samples from confirmed HIV-positive patients were screened for HBsAg by commercially available rapid test (Hepacard by Diagnostic enterprises) and confirmed by enzyme-linked immunosorbent assay (ELISA) kits (Hepalisa by J Mitra and Co. Pvt., Ltd) and another rapid test (SD Bioline HBsAg by Alere Medical Pvt., Ltd) for the presence of HBsAg while for HCV screening was done by commercially available rapid test (HCV Tridot by Diagnostic enterprises) and confirmed by ELISA kits (HCV Microlisa by J Mitra and Co. Pvt., Ltd) and another rapid test (SD Bioline HCV by Alere Medical Pvt., Ltd) for the presence of HCV antibodies.

Statistical analysis

The data were collected and then analyzed using IBM SPSS Statistics for Windows, version 23 (IBM Corp., Armonk, N.Y., USA), and Chi-square, Fisher’s exact, and Mann–Whitney U-tests were used to measure the association between the different variables.

P < 0.05 was considered statistically significant.

A total of 137 patients participated in the present study. The age distribution of the study population and those coinfected with HBV/HCV is shown in [Figure 1]. In the study including all participants, it was found that males 65.7% (n = 90) were more commonly infected than females 34.3% (n = 47), majority of whom were married 84.7% (n = 116) followed by single 13.1% (n = 18) and widowed 2.2% (n = 3). Of the total study population, 47.4% (n = 65) were known cases of HIV on admission and 36.5% (n = 50) were on antiretroviral therapy (ART). The mean and median cluster of differentiation (CD4) T-lymphocyte cell count of all the cases were recorded at 260 and 238 cells/μl, respectively.

The prevalence of HBV in HIV-positive patients was found to be 6.6% (n = 9). Males 66.7% (n = 6) were dominantly infected than females 33.3% (n = 3) and majority were married 88.9% (n = 8) followed by unmarried 11.1% (n = 1). Out of these nine cases, four were known cases of HIV and all were on ART. The mean and median CD4 counts were recorded at 212 and 200 cells/μl, respectively. It was also found that a majority, i.e. 77.8% (n = 7) improved on discharge from the hospital while 22.2% (n = 2) left against medical advice and outcome of these cases is unknown. The statistical analysis of HBV-HIV in coinfected individuals with the different variables is summarized in [Table 1], in which the predominant significant values were found for serum globulin and alanine aminotransferase (ALT).

The prevalence of HCV in HIV-positive patients was found to be 0.7% (n = 1). The patient in our study was a 38-year-old male who was married and a known case of HIV and was on ART treatment. The patient improved on discharge after 10 days of hospital stay. The laboratory parameters of the patient are summarized in [Table 1]. There was not even a single case of triple infection with HIV, HBV, and HCV in our study.

The latest estimates by the WHO in relation to HIV, HBV, and HCV speak for themselves, in having an enormous impact on the individuals affected and the community as a whole. In our study of 137 HIV-positive-confirmed individuals, it was found that majority were males and married which is in accordance with other studies in the Indian context.^{[12],[13],[14]} The age group most commonly affected is the 41–50 years which is different from majority of the studies where they reported 31–40 years as the most common.^[12],[14] We believe this to be due to the fact that a good number of individuals (36.5%) were already on ART on admission.

The seroprevalence of HBV in HIV-positive patients in the study was found to be 6.6% (n = 9), with males predominantly affected in the ratio of 2:1. Our findings are similar to a study conducted by Sarkar et al.^[15] The age group most commonly affected with HBV-HIV coinfection was that of 31–40 years which is similar to other studies.^{[16],[17],[18]} Comparison of studies conducted over the years with HBV/HCV coinfection in HIV is summarized in [Table 2].

The seroprevalence of HCV-HIV coinfection was very low with only one case detected at 0.7% only. The case was of a 38-year-old male, married, with known status of HIV positive on admission and on ART treatment, findings of which are similar to studies summarized in [Table 2] with the exception of Mahajan et al. where they did not report even a single case of HCV/HIV coinfection.^{[13],[16],[17],[19]}

The seroprevalence of HBV and HCV in HIV-infected individuals was reported to be higher in drug users with percentages as high as 100% for HBV and 92% with HCV in a study conducted in North East India in the year 2000,^[20] while a recent study from Mumbai by Shukla and Sharma ^[21] had shown higher rates of HBV and HCV when compared to HIV in intravenous drug users.

In relation to the CD4 counts of available study population, it was found that the mean and median CD4 counts of HBV-HIV coinfection were lower than those who were mono-infected with HIV. The mean hemoglobin level of 11.9 g/dl is on the lower side of the normal range which is similar to a study conducted by Sarkar et al.^[15] The mean platelet count was within the normal limits.

In our study, the LFT which is important in the diagnosis and prognosis of liver diseases was found having an insignificant P  value for majority of the parameters except for serum globulin and ALT in HBV/HIV coinfected individuals. The mean and median values of serum globulin, conjugated bilirubin, and aspartate amino-transferase (AST), while the mean values only of serum total bilirubin, ALT, and alkaline phosphatase were increased than the normal levels. Our findings are similar to other studies where AST and ALT were reported as the two most important parameters to determine the effect of these hepatic viruses on the liver.^[15],[18] In relation to HCV/HIV-coinfected individuals, the detection of only one case with low Hb and platelet levels and near-normal levels of LFT leaves us with the difficulty to interpret the findings and more research work is needed to arrive at a conclusion of such laboratory parameters in HCV/HIV-coinfected individuals.

The mean and median number of days of hospital stay were lower in HBV-HIV coinfection while higher in HCV-HIV-coinfected individuals when compared to HIV mono-infected individuals. The outcome of these HIV-coinfected individuals with HBV and HCV showed good outcome with 80% (n = 8) showing improvement on discharge while 20% (n = 2) with HBV/HIV coinfection left against medical advice and the outcome remains unknown.

The NACO guidelines regarding the treatment of HBV/HCV coinfection in HIV-infected individuals are as follows:^[22]

1. Without any evidence of chronic active hepatitis: ART to be started if CD4 <350 cells/mm ³
2. With documented evidence of chronic active hepatitis: ART to be started irrespective of CD4 count.

We suggest that future studies in coastal Karnataka on HIV-positive patients coinfected with HBV and HCV using molecular techniques such as polymerase chain reaction (PCR) and nucleic acid amplification test (NAAT) which are costly and not affordable in our set-up can be used to determine the seroprevalence, the different genotypes, and the viral load of these viruses in the population.

We conclude that in HIV-infected individuals, the seroprevalence of HBV coinfection is 6.6% and that of HCV coinfection is 0.7% where males are more commonly affected in the age group of 31–40 years and majority are married. The laboratory test showed that in HBV/HIV-coinfected individuals, there is a significant correlation between HBV-HIV coinfection and serum globulin and ALT; the mean values of Hb levels and CD4 count are below normal and the mean values of majority of the LFT are increased than the normal levels which included serum globulin, serum total bilirubin, conjugated bilirubin, AST, ALT, and alkaline phosphatase, while in the case of the only HCV-HIV coinfected patient, only Hb and platelet count are decreased from the normal while the LFT values are within the normal range. Majority of the HIV-positive patients coinfected with HBV/HCV showed improvement.

Hence, nongovernmental organizations and government agencies should come together in making people aware and understand these diseases, the “3Hs” (HIV, HBV, and HCV), especially the route of transmission and that vaccination is available for HBV. Both the government and private sectors should provide free screening test for these diseases in suspected individuals having a history of high-risk behavior including intravenous drug users and free vaccination for HBV for the community as a whole. Then only, we will be going in the right direction in combating these deadly diseases and improving the morbidity and mortality rates related to them of the country and the world.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ATMPH.ATMPH_131_17

[Figure 1]

[Table 1], [Table 2]