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Sero-Occurrence of HBV/HCV Co-
infection and Levels of Liver 
Enzymes among Patients at a 
Tertiary Care Hospital in Central 
India: a Pilot Study 

Prabha Desikan1, Aseem 
Rangnekar1, Zeba Khan1, Nikita 
Panwalkar1, Protiti Bose1, Hanni 
Vasudev Gulwani2, Sukhpreet 
Kaur2 
 
1Department of Microbiology, Bhopal 
Memorial Hospital and Research Centre, 
India; 
2Department of Pathology, Bhopal 
Memorial Hospital and Research Centre, 
India 

 
Vol. 8, No. 1 (2019)   |   ISSN 2166-7403 (online)  
DOI 10.5195/cajgh.2019.313 |   http://cajgh.pitt.edu 

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Abstract 

Introduction: Hepatitis B and C viral infections share common modes of transmission and account for a large proportion of liver 
disease burden across the globe. Patients with Hepatitis B (HBV) and Hepatitis C virus (HCV) co-infection may have more severe 
liver disease and are potentially at higher risk for developing hepatocellular carcinoma. The aim of this study was to assess the 
sero-occurrence of HBV/HCV co-infection by examining the medical records of tertiary care hospital patients in Central India and 
determine the extent of liver damage based on liver function tests (LFTs). 
Methods: Patients with a positive test for HBV surface antigen (HBsAg) over a period of 10 years were identified from laboratory 
records in a tertiary care facility in central India. Records of 51,075 consecutive non-duplicate blood samples were then screened 
for a positive HBV and HCV tests. LFT, liver enzymes, and bilirubin data were also extracted. Means and standard deviations were 
determined for continuous variables, and the difference in means was compared using a independent samples t-test. Associations 
between HBV/HCV co-infection status and demographic variables were calculated using Pearson’s Chi-squared test. A p-value 
less than 0.05 was considered statistically significant. 
Results: In this study, 1674 (3.27%) screened patients were positive for HBsAg and the sero-occurrence of co-infection with HCV 
in HBsAg positive patients was reported in 28 individuals (1.67%). There was no significant gender difference for HBV/HCV co-
infection (p>0.05). HBV/HCV co-infection was observed more frequently in the 31-60 year old age group (p=0.001). HBV/HCV 
co-infected patients had significantly higher levels of liver enzymes and bilirubin than those with HBsAg mono-infection (p=0.001). 
Conclusion: Liver function tests are potentially important predictors for HBV/HCV coinfection. Screening for HCV co-infection 
in HBsAg-positive patients is recommended in India. Detection of co-infection may enable timely preventive/therapeutic 
interventions aimed at preventing progression to hepatocellular carcinoma. 

Keywords: Hepatitis B; Hepatitis C; Co-infection; India 

Sero-Occurrence of HBV/HCV Co-
infection and Levels of Liver 
Enzymes among Patients at a 
Tertiary Care Hospital in Central 
India: a Pilot Study 

Prabha Desikan1, Aseem Rangnekar1, 
Zeba Khan1, Nikita Panwalkar1, 
Protiti Bose1, Hanni Vasudev 
Gulwani2, Sukhpreet Kaur2 
 
1Department of Microbiology, Bhopal 
Memorial Hospital and Research Centre, 
India; 
2Department of Pathology, Bhopal Memorial 
Hospital and Research Centre, India 

Research 

Introduction 

Chronic liver disease (CLD) results from an 
inflammatory injury to the liver, persisting for six or 
more months without complete resolution. CLD can 
result from a spectrum of diseases including chronic 
hepatitis, liver cirrhosis, and hepatocellular carcinoma 
(HCC)1. Chronic Hepatitis B virus (HBV) and Hepatitis 
C virus (HCV) infections are significant public health 
issues globally. Compared to HBV mono-infected 
patients, HBV/HCV co-infected patients have higher 
rates of cirrhosis (44% vs. 21%) and decompensated liver 
disease (24% vs. 6%). Similarly, HBV/HCV co-infected 
patients compared to HCV mono-infected patients, have 
a higher rate of cirrhosis (95% vs. 49%) and more 
advanced decompensated liver disease (Child-Pugh class 

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C 37% vs. 0%)2. Epidemiologic studies in patients with 
dual HBV/HCV infection demonstrated an increased risk 
of HCC, which has been confirmed by three published 
meta-analyses3-5. Evidence suggests that HBV is capable 
of initiating the neoplastic process, while HCV can act as 
a promoter, and that the two conditions may be 
synergistic in leading to HCC development3. 

The estimated global prevalence of 
HBV/HCV co-infection is approximately 5-20% in 
HBsAg positive patients and 2-10% in HCV positive 
patients6. In India, the prevalence of HBV and HCV co-
infection ranges from 1.89% to 56% depending on the 
region7,8, which may be related to a lack of awareness of 
HBV vaccine availability by the general public9. 
HBV/HCV co-infection is more frequent in high-risk 
populations of various ages, including intravenous drug 
users, patients receiving hemodialysis, patients 
undergoing organ transplantation, HIV-positive patients, 
and β-thalassemia patients10. Previous studies reported 
that age below 40, Asian race, injection drug use, a 
greater number of lifetime sexual partners, inadequate 
sterilization of medical equipment, unprotected sex, and 
the use of unscreened blood and blood products are 
independent risk factors for HBV/HCV dual 
infection10,11. In India, the most commonly reported 
modes of transmission of HBV and HCV are sexual 
transmission, blood transfusion, and intravenous drug 
use12. Moreover, because of the shared modes of 
transmission, HBV/HCV co-infections are common in 
endemic areas and among subjects with a high risk of 
parenteral transmission13,14 Study findings report a 
greater likelihood of the progression from chronic 
hepatitis to cirrhosis and HCC in patients with 
HBV/HCV co-infection compared to infection by HBV 
or HCV alone; this combination of cirrhosis and HCC 
is particularly difficult to clinically manage15. 

Measurement of liver enzymes function (i.e. 
Alanine transaminase (ALT), Aspartate transaminase 
(AST), and Alkaline Phosphatase (ALP)) is an 
inexpensive and non-invasive method of assessing 

liver disease. Measurement of liver enzymes reflect the 
activity of hepatotropic viruses and the degree of 
damage to the liver during therapy with various 
hepatotoxic drugs16. To our knowledge, very limited 
data about the sero-occurrence of HBV/HCV co-
infection are available from Central India. The 
objectives of this study are to (1) identify the 
prevalence of sero-occurrence of HBV/HCV co-
infection in a large tertiary care facility, and (2) 
determine the extent of liver damage in patients with 
HBV/HCV co-infection. 

 

Methods 

Study design and data collection: 

The study was carried out in the Department of 
Microbiology, Bhopal Memorial Hospital & Research 
Centre (BMHRC), Bhopal, and Madhya Pradesh, India.  
BMHRC is a tertiary care hospital and serves a 
population of more than two million residents. Records 
of patients and test results were maintained in lab 
registers as well as a hospital information system (HIS) 
of the BMHRC. Laboratory records from January 2006 
to December 2016 were reviewed retrospectively for 
demographic and HBsAg data. Lab records were also 
reviewed for anti-HCV sero-positivity among HBsAg 
positive samples. This study was limited to samples from 
patients who visited either outpatient (OPD) or inpatient 
departments (IPD) of BMHRC, and who were diagnosed 
as HBsAg and anti-HCV positive. Samples with 
incomplete liver function panel or demographic data 
were excluded. All the investigations for HBsAg and 
anti-HCV were completed by Enzyme Linked 
Immunosorbent Assay (ELISA) as part of routine 
laboratory work flow, in accordance with the 
manufacturer’s instructions. Liver enzyme tests were 
done by biochemical assays, and included Alanine 
transaminase (ALT), Aspartate transaminase (AST), 
Alkaline Phosphatase (ALP), bilirubin total (BT), 
bilirubin indirect (BI), and bilirubin direct (BD). The 

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study was approved by the Institutional Ethical 
Committee of BMHRC.  

Statistical analysis 

Data were analyzed using OpenEpi online 
software17. Differences in variable distribution were 
evaluated by Pearson’s chi-squared test, and a p-value of 
less than 0.05 was considered statistically significant. 
Means and standard deviations were reported for 
continuous variables, and differences in means were 
compared with an independent samples t-test. We 
defined abnormal liver enzyme cut-offs according to the 
National Health and Nutrition Examination Survey 
(NHANES) criteria III18. Abnormal values of liver 
enzymes and bilirubin levels were defined as 
ALT/AST≥50 IU/ml, ALP≥129 IU/ml.BT/BI ≥1.1 
mg/dl, and BD≥ 0.3 mg/dl.  

 

Results 

A total of 51,075 consecutive non-duplicate 
blood samples were collected over a period of ten years 

for HBsAg testing. Out of these samples, 1674 (3.27%) 
were positive for HBsAg, and 295 (0.57%) were found to 
be positive for anti-HCV. Among individuals positive for 
HBsAg or anti-HCV, 28 (1.67%) samples were identified 
as positive for both, HBsAg and anti-HCV. Sero-
occurrence rates are summarized in Table 1. Ages of 
patients positive for HBV ranged from 12-75 years of age 
(Median=54 years, IQR: 15), and 29-74 years of age 
(Median=45 years, IQR: 26) for HBV/HCV co-infected 
individuals. HBV/HCV co-infection was more frequent 
in males at 78.5% (n=22) than in females at 21.4% (n=6), 
but the difference was not statistically significant 
(p=0.80). A significantly higher prevalence of 
HBV/HCV co-infection was observed in the 31-60 years 
(46.4%) age group compared to the 1-30 years (25.0%) 
and >60 years (28.6%) age groups (p=0.001) (Table 1). 
The proportion of sero-occurrence of HBV/HCV co-
infection fluctuates between 2006 and 2016 with the 
highest prevalence in 2013 (Figure 1). 

Out of 1674 HBsAg positive samples, LFT results 
were available for 773 samples. The mean values of 
serum levels of Alanine transaminase (ALT), Aspartate

 

 
Figure 1. Trends of sero-positivity of HBsAg, anti-HCV, and HBV/HCV co-infection at Bhopal Memorial Hospital 
and Research Center in Central India 2006 – 2016.  

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Table 1. Demographic data on HBV/HCV distribution in the study population. 

transaminase (AST), Alkaline Phosphatase (ALP), 
bilirubin total (BT), bilirubin indirect (BI), and bilirubin 
direct (BD) were 114.4±403.8 IU/L, 94.7±344.8 IU/L, 
101.4±71.6 IU/ml, 1.4±2.9mg/dl, 0.7±2.7mg/dl, and 
0.7±1.7mg/dl respectively in HBsAg positive patients, 
and 100.25±201.4 IU/L, 106.3±265.7 IU/L, 114.7±65.9 
IU/ml, 1.7±2.7mg/dl, 1.05±2.7mg/dl, and 0.7±0.7mg/dl 
respectively in HBV/HCV co-infected patients. Levels of 
ALT, AST, ALP, and bilirubin were significantly 
different between HBV/HCV co-infected patients and 
HBsAg mono-infected patients (p <0.001) (Table2). 
 
Discussion 

In this study, sero-occurrence of HCV co-
infection in HBV patients was found to be low (1.67%) 
compared to global data, but higher than reported in other 
parts of India7,12,19. A large multicenter study from the 
United States assessed the prevalence of HBV/HCV co-
infection and found anti-HCV was present in 7% of 
chronic HBV carriers10. Tesfa et.al. reported a 6.39% 
prevalence of HBV/HCV co-infection in a hospital-based 
study conducted in Ethiopia20. Studies conducted in 
different regions of India have reported diverse 
prevalence rates of HBV/HCV co-infection in drug 
abusers having chronic liver disease (1.5 %), patients on 

hemodialysis (0.8%), and in patients with HIV infection 
(3.0%)7,21-22.  

While not statistically significant, we found that 
the seropositivity rate of HBV/HCV co-infection among 
males was higher than in females. This is an interesting 
finding, as it corroborates a previous report that male 
subjects are at a higher risk of developing HBV/HCV co-
infection compared to females23-24. The reason for a 
higher frequency of HBV/HCV co-infection among male 
patients could be a result of a higher level of exposure to 
risk factors associated with co-infection, including drug 
abuse, unprotected sex, and having more than one sexual 
partner25. 

Our study showed that HBV/HCV co-infection 
rates were highest among individuals in the age group of 
31-60 (46.4%), followed by the age group of 60 years and 
over (28.57%), which was similar to a previously 
published study in the United States10. A higher 
prevalence in the 31-60 years age group may be 
associated with increased exposure to risk factors for 
HBV/HCV co-infection.  

HBV/HCV co-infected patients in this study had 
significantly higher levels of ALT, AST, and ALP 
compared to HBsAg and anti-HCV mono-infected 
patients. Higher levels of liver enzymes have been

Demographic variables HBsAg positive (%) Anti-HCV positive (%) HBV/HCV co-infection (%) p-value* 

Sex     

Male 1,364 (81.4) 201 (68.1) 22 (78.5) 
p = 0.8 

Female  310 (18.5) 94 (31.8) 6 (21.4) 

Age      

1-30 257 (15.35) 75 (25.4) 7 (25) 

p = 0.001 31-60 754 (45.04) 105 (35.5) 13 (46.4) 

>60 663 (39.60) 115 (38.93) 8 (28.6) 

*Based on chi-squared test 

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Table 2. Liver function profile in HBV mono-infected patients and those with HBV/HCV co-infected patients. 

reported in HBV/HCV co-infected patients compared to 
those having HBV and HCV mono-infection26. Bilirubin 
concentrations were found to be highest in co-infected 
patients in this study. A study conducted in tribal 
populations of Central India also found an elevated level 
of bilirubin in HBV/HCV co-infected patients27-28. It is 
documented that elevated levels of liver enzymes in HBV 
infected patients are associated with higher risk of liver 
cirrhosis and HCC29. Once HBV infection is detected 
during a diagnostic workup of hepatitis, it is possible that 
hepatitis may be attributed to HBV infection alone and 
further etiological diagnoses may not be carried out. This 
may lead to underreporting of co-infection with HCV. 
Therefore, detection of co-infection may enable timely 
intervention to prevent progression to HCC. 

This pilot investigation is the first study to show 
sero-occurrence of HBV/HCV coinfection within the 
central zone of India, along with the comparison of liver 
enzymes data among these patients. Our findings indicate 
that there is a potentially higher level of liver damage in 

patients with HBV/HCV co-infection, warranting that 
those diagnosed with either HBV or HCV should also be 
tested for the other hepatitis virus. Screening of HBV 
infection can be made more widespread through 
molecular testing of HBV DNA by polymerase chain 
reaction to detect occult hepatitis B infection. 

There were several limitations to our study. 
There were no available data on occult HBV infection 
since HBV DNA assays were not performed. This might 
underestimate the real burden of HBV in this study 
population. The HBV immunization status of patients 
was also unknown, which is something we can address in 
our future investigations. In this study, the majority of 
HBsAg and anti-HCV cases were initially diagnosed by 
clinical suspicion of an underlying disease, which is 
likely to underestimate the total number of viral hepatitis 
infections in our population, due to the presence of 
subclinical or asymptomatic infections. This study is 
limited to the review of medical records; no information 
was gathered directly from the patients. 

Variables HBsAg mono infection HBV/HCV coinfection p value* 

ALT, mean±SD 114.4±403.8 100.25±201.4 0.001 

ALT Abnormal high (n%) 156 (20.1%) 14 (50.0%)  
AST, mean±SD 94.7±344.8 106.3±265.7 0.001 

AST Abnormal high (n%) 140 (18.1%) 8 (28.5%)  
ALP mean±SD 101.4 ± 71.6 114.7±65.9 0.001 

ALP Abnormal high (n%) 132 (17.7%) 11 (39.2%)  
Bilirubin total mean±SD 1.4±2.9 1.7±2.7 0.001 

Bilirubin total Abnormal high (n%) 151 (19.5%) 11 (39.2%)  
Bilirubin Direct mean±SD 0.7±2.7 1.05±2.7 0.001 

Bilirubin Direct Abnormal high (n%) 368 (47.6%) 15 (53.3%)  
Bilirubin Indirect mean±SD 0.7±1.7 0.7±1.7 0.001 

Bilirubin Indirect Abnormal high (n%) 110 (14.2%) 7 (25.0%)  
*Student’s t-test 

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Our results may be useful for making estimates 
and projections about future liver disease burden. A 
recently developed mathematical model by El-Bouzedi30, 
that uses available epidemiological data on viral hepatitis 
to estimate future consequences of hepatitis infection, 
can be incorporated in our future research. Such models 
will help to inform health policy, resource distribution, 
and healthcare delivery in India, as well as other 
countries. These types of studies can also lead to 
improved management of patients with viral hepatitis and 
inform health policy.  
 
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	Sero-Occurrence of HBV/HCV Co-infection and Levels of Liver Enzymes among Patients at a Tertiary Care Hospital in Central India: a Pilot Study
	Abstract
	Keywords: Hepatitis B; Hepatitis C; Co-infection; India
	Sero-Occurrence of HBV/HCV Co-infection and Levels of Liver Enzymes among Patients at a Tertiary Care Hospital in Central India: a Pilot Study
	Research

