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Original Article

Seroprevalence of hepatitis B and C Virus Infections among type 2

diabetic patients in a tertiary care diabetic centre in Dhaka City

Md. Golam Azam, Tareq M Bhuiyan, Md. Nazmul Hoque, Md. Anisur Rahman, A K Azad Khan

ABSTRACT

Aims: This study was carried out to explore the prevalence of HBV and HCV

infections among type 2 diabetes mellitus (T2DM) patients and risk factors. This cross-

sectional study was conducted at BIRDEM General Hospital, Dhaka, Bangladesh

between January 2012 and March 2013.

Subjects and Methods: A total of 1024 type 2 diabetics were included. Well-

structured questionnaire was used to collect demographic profile and history of the

study populations. Venous blood samples were collected to screen HBV, HCV

infections and to estimate other biochemical tests. Data analysis was carried out using

SPSS version 16.0. Descriptive analysis was performed and results expressed as

means±SD and n (%). P <0.05 was considered significant.

Results: Prevalence of HBV in type 2 diabetics was 3.0% (31/1024) and HCV was

0.48% (5/1024). Among all subjects, mean±SD of body mass index (BMI) was

24.9±3.8, fasting blood sugar mmol/L was 10.7±4.6, post prandial blood sugar mmol/L

was 17.6±7.2, fasting cholesterol mg/dl was 198.5±81.3, haemoglobin gm/dl was

13.1±1.5, serum ALT IU/L was 40.5±36.0. Mean serum ALT was significantly higher

among HBV-positive T2DM participants (57.7 IU/L) than HBV-negative participants

(36.2 IU/L) (P=0.001).

Conclusions: The seroprevalence of HBV was higher than that of HCV in T2DM

patients. T2DM patients should take necessary preventive measures like prophylactic

vaccination to reduce the risk of HBV infection and its consequences.

INTRODUCTION

Diabetes mellitus is a leading cause of death and disability

worldwide.1,2 Its global prevalence was about 8% in 2011 and is

predicted to rise 10% by 2030.3 Nearly 80% of people with

diabetes live in low- and middle-income countries.3 Asia and the

Eastern Pacific region are particularly affected:3–8 in 2011,

China was home to the largest number of adults with diabetes

(i.e. 90.0 million, or 9% of the population), followed by India

(61.3 million, or 8% of the population) and Bangladesh (8.4

million, or 10% of the population).3 In Bangladesh, the overall

age-adjusted prevalence of diabetes and prediabetes is 9.7% and

22.4%, respectively.4 Among urban residents, the age-adjusted

prevalence of diabetes is 15.2% compared with 8.3% among

rural residents.4

Diabetes mellitus is considered to be an immuno-compromised

state.5,6 Moreover, frequent needle application needed for blood

testing as well as treatment with injections predispose to a risk

factor for transmission of hepatitis B and hepatitis C viruses.

Globally two billion people are infected with HBV, and 350

millions of them have chronic (lifelong) infections, who are at

high risk of death from liver cirrhosis and liver cancer that kill

more than one million people globally each year.7 Different

studies in Bangladesh showed that seroprevalence of hepatitis B

is 3.1%.8 A recent report showed 5.5% HBsAg positivity among

the general population living in Savar, a semi-urban area on the

outskirts of Dhaka.9

HCV infections is also a major global health problem with an

estimated 170 million people chronically infected and 3-4

International Journal of Gastroenterology, Hepatology,

Transplant & Nutrition

Department of gastrointestinal, hepatobiliary and pancreatic disorders

(GHPD), BIRDEM General Hospital,

Dhaka, Bangladesh

Address for Correspondence:

Dr. Md. Golam Azam

E-mail: drgolamazam@gmail.com

Access this article online

QR Code

Website:

www.journal.pghtn.com

Key words: dif Diabetes mellitus, hepatitis B, hepatitis C, prevalence

Azam et al. Int J Gastroenterol Hepatol Transpl Nutr 2016;1(iv): 17-22

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18

million people get new infections each year.10 A recent study

among rural population in Bangladesh showed only 0.5%

subjects were positive for anti-HCV antibodies.11

Hepatitis B and hepatitis C many a times are responsible for

chronic hepatitis which culminates into cirrhosis of liver, liver

failure and hepatocellular carcinoma. Non-alcoholic

steatohepatitis (NASH) is present in higher rates among diabetic

patients as a consequence of metabolic disorders. NASH is also

responsible for chronic liver disease as viral infections. In

BIRDEM general hospital, we observed that among indoor

patients with end-stage liver disease, etiology are due to non-B

and non-C in 50% cases (data on record).

Various studies have reported on the prevalence of HBV and

HCV in T2DM patients in different parts of the world.12-17 So

far, there is a paucity of data on the prevalence of HBV and

HCV infections among diabetics in Bangladesh. To enable

better management of T2DM patients, especially to prevent such

add on infections and its morbid consequences, it is judicious to

study the seroprevalence of HBV and HCV infection in T2DM

as well as its associated factors. Thus, the aim of this study was

to explore the seroprevalence of HBV and HCV infections

among newly detected diabetic patients.

MATERIALS AND METHODS

Study area and subjects

This cross-sectional prospective study was conducted between

January 2012 and March 2013 at the outpatient department of

BIRDEM general hospital. A total of 1024 participants with

confirmed type 2 diabetes were recruited. A structured

questionnaire was administered to collect demographic and

clinical information of patients. Type 1 diabetics, organ

transplant recipients and dialysis patients were excluded from

the study.

Ethical consent

This study was approved by ethical committee of Bangladesh

Diabetic Samity (BADAS). Informed consent was sought from

the participants before recruitment into the study.

Anthropometric measurements

The height (to the nearest 0.1 cm) without footwear, weight (to

the nearest 0.1 kg) in light clothing were measured. The body

mass index (BMI) was then calculated as the ratio of the weight

(kg) and the square of the height (m2).

Blood sample collection

About 3 ml venous blood was drawn from each study

participant after an overnight fast (12-14 h). 2 ml was dispensed

into a serum separator tube and centrifuged at 1500 rpm for 5-10

min. The serum was dispensed into cryovials and aliquots stored

at -80°C until assayed. The remaining 1 ml was dispensed into

fluoride oxalate anticoagulated tubes for estimation of blood

glucose.

Serological tests

The serum was analyzed for the detection of hepatitis B surface

antigen (HBsAg) using enzyme linked immunosorbent assay

(ELISA) (Murex HBsAg Version 3 DiaSorin S.p.A. UK), and

anti-HCV antibodies using ELISA (Murex anti-HCV version

4.0 DiaSorin S.p.A. UK).

Biochemical tests

Blood glucose, haemoglobin and serum ALT estimation were

carried out at the laboratory of BIRDEM general hospital using

standard diagnostic reagents as per manufacturer’s instruction.

Statistical analysis

Data analysis was carried out using the statistical package for

social science (SPSS) version 16.0 (Chicago IL, USA).

Descriptive analysis with frequency distribution tables was

performed and the results expressed as means (SD) and n (%).

The t-test, Chi-square and ANOVA test were used for

comparisons as appropriate. P < 0.05 was considered significant.

RESULTS

Of the total population, prevalence of HBV in type 2 diabetics

was 3.0% (31/1024) and HCV was 0.48% (5/1024). The

prevalence of HBV infection in the type 2 diabetes mellitus

(T2DM) participants was higher 3.0% than that of HCV 0.4%.

Tables 1 and 2 describe the demographic and clinical

characteristics of T2DM participants in relation to gender. Of

the total number of males, 38.7% (216/557) were in their fifth

decade of life and 48.3% (270/557) had secondary education.

There were a significant difference in level of education,

occupation, history of surgery and history of blood transfusion

(P <0.001; P <0.001 P <0.001; P < 0.001 respectively) when

compared between males and females. There were no significant

differences among male and female in the history of dental

procedure and hepatitis B vaccination (P <0.401; P < 0.517

respectively).

A total of 34.6% T2DM patients (353/1024) were overweight,

of which 50.6% (179/557) were males and 49.4% (174/447)

were females. There were a significant difference in

haemoglobin and serum ALT levels among male and female

patients (P <0.001; P < 0.001 respectively). Fasting and post

prandial blood sugar levels were not significantly differed

among sexes (P <0.525; P < 0.748 respectively).

Table 3 shows the demographic, clinical, and biochemical

characteristics of participants, relative to hepatitis B status.

Mean age was significantly higher among positive subjects than

the negatives (P <0.006). Serum ALT level was also

significantly raised among positive cases (P <0.017). Other

variables were not significant among positive and negative

cases.

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Table 1: Demographic characteristics of the study populations

Variables T2DM patients P

Total

(n=1024)

Male

(n=557)

Female

(n=447)

Age (years)

≤30 82(8.1) 38(45.8) 45(54.2) 0.015

31-40 295(28.8) 153(51.9) 142(48.1)

41-50 379(37.0) 216(57.0) 163(43.0)

51-60 202(19.7) 127(62.9) 75(37.1)

≥60 65(6.3) 43(66.2) 22(33.8)

Level of education

Illiterate 98(9.6) 22(22.4) 76(77.6) <0.001

Basic 105(10.3) 42(40.0) 63(60.0)

Primary 168(16.4) 78(46.4) 90(53.6)

Secondary 453(44.2) 270(59.6) 183(40.4)

Tertiary 200(19.5) 165(82.5) 3517.5)

Occupation

House wife 389(38.0) 0.0 389(100.0) <0.001

Regular job 338(33.0) 313(92.6) 25(7.4)

Self-employment 147(14.4) 112(76.2) 35(23.8)

Business 150(14.6) 140(93.3) 10(6.7)

H/O surgery

Yes 295 (29.1) 122 (41.4) 173 (58.6) <0.001

No 729 (70.9) 452 (62.2) 277 (37.8)

H/O blood transfusion

Yes 78 (7.7) 17 (21.8) 61 (78.2) <0.001

No 946 (92.3) 560 (60.1) 386 (39.9)

H/O dental procedure

Yes 408 (41.0) 223 (54.7) 185 (45.3) 0.401

No 586 (59.0) 339 (58.0) 246 (42.0)

Hepatitis B vaccination

Yes 48 (4.7) 29 (59.6) 19 (40.4) 0.517

No 976 (95.3) 546 (56.2) 430 (43.8)

Data are presented as n (%). P<0.05 were considered as significant. DM: Diabetes mellitus, T2DM: Type 2 diabetes mellitus.

Table 2: Clinical and biochemical characteristics of the study populations

Variables Total

(n=1024)

T2DM patients P

Male

(n=557)

Female

(n=447)

BMI (kg/m2)

Underweight 34 (3.3) 15 (44.1) 19 (55.9) <0.001

Normal 532 (52.0) 344 (64.8) 188 (35.3)

Overweight 353 (34.6) 179 (50.6) 174 (49.4)

Obese 105 (10.1) 58 (55.5) 47 (44.5)

Hb (gm/dl) 13.1±1.5 13.8±1.4 12.3±1.3 <0.001

Serum ALT (U/L) 40.6±36.5 45.2±42.6 34.4±24.9 <0.001

Fasting blood sugar (mmol/L)

10.7±4.6 10.8±4.6 10.6±4.6 0.525

Post prandial blood sugar (mmol/L) 17.6±7.2 17.7±6.8 17.5±7.6 0.748

Data are presented as n (%) and mean±SD where applicable. P<0.05 were considered as significant.

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Table 3: Demographic, clinical, and biochemical characteristics of patients relative to Hepatitis B status

Variables Total

(n=1024)

HBsAg status P

Positive

(n=31)

Negative

(n=993)

Age of subjects

(years)

45.0±10.5 39.8±7.8 45.1±10.5 0.006

H/O surgery

Yes 297 (29.0) 8 (2.7) 289 (97.3) 0.905

No 727 (71.0) 23 (3.2) 704 (96.8)

H/O blood transfusion

Yes 78 (7.6) 2 (2.6) 76 (97.4) 1.000

No 946 (92.4) 29 (3.1) 917 (96.9)

H/O dental procedure

Yes 408 (40.9) 12 (2.9) 396 (97.1) 0.948

No 606 (59.1) 19 (3.1) 587 (96.8)

Family h/o liver disease

Yes 92 (9.0) 9 (9.7) 83 (90.2) 0.003

No 932 (91.0) 22 (2.3) 910 (97.6)

BMI (kg/m2) 24.8±3.8 24.2±3.4 24.9±3.8 0.378

Hb (gm/dl) 13.1±1.5 13.9±1.4 13.1±1.5 0.325

Serum ALT (U/L) 40.6±36.5 57.4±56.3 39.9±35.4 0.017

Fasting blood sugar (mmol/L) 10.7±4.6 10.5±4.8 10.7±4.6 0.779

Post prandial blood sugar (mmol/L) 17.6±7.2 18.2±9.3 17.6±7.1 0.685

Data are presented as n (%) and mean±SD where applicable. BMI: Body mass Index.

P<0.05 were considered as significant.

DISCUSSION

In our study mean age was significantly higher among HBsAg

positive subjects than the negatives (P <0.006). This can be

explained by prolonged time of exposure to an endemic zone of

hepatitis B virus in Bangladesh. Family history of liver disease

also significantly higher among HBsAg positive subjects

(P <0.003). Serum ALT level was also significantly raised

among positive cases (P <0.017). Serum ALT level sometimes

increases in non alcoholic fatty liver disease (NAFLD) patients,

a common scenario among diabetic cases. But if the underlying

cause of raised ALT is viral hepatitis, then it requires special

management. Other variables were not significant among

positive and negative cases.

Seroprevalence of hepatitis B virus varied among different study

populations in previous published data in Bangladesh. Out of

43,213 Bangladeshi job seekers, 4.4% of individuals were

positive for hepatitis B surface antigen,18 3.5% pregnant women

were found to be HBsAg positive in a tertiary care hospital in

Dhaka,19 among recipients of multiple blood transfusion of

thalassaemic children in Bangladesh, HBsAg and anti-HCV

were highly prevalent than that of the healthy children (13.8%

vs 6.5%, p<0.04 and 12.5% vs 0.9%, p<0.0001 respectively).20

A recent report showed 5.5% HBsAg positivity among the

general population living in Savar, a semi-urban area on the

outskirts of Dhaka.9 Another study among rural population in

Bangladesh showed only 0.5% subjects were positive for anti-

HCV antibodies.11 Ashraf et al found 5.8% were HBsAg

positive and 0.5% were anti-HCV positive among impoverished

urban community in Dhaka, Bangladesh.21

In a study conducted at Multan, Prevalence rate of 13.7% for

HCV infection was recorded among subjects having T2DM with

seropositivity rate of 4.9% among the control group of volunteer

blood donors without diabetes. The patients with T2DM were

more likely to have HCV infection as compared to the control

group (OR = 3.03, 95%CI = 2.64-3.48, p =0.001).14 Ephraim et

al found prevalence of HBV in type 2 diabetics was 5.5%

(6/110).12 However no type 2 diabetic was positive for HCV in

this study. Chen et al found that the prevalence of hepatitis B

was similar to that of the control group.22

Prevalence of HCV viremia showed significant difference

between T2DM and non-T2DM subjects (6.9% vs 4.5%,

P<0.001), whereas anti-HCV seropositivity showed borderline

significance (7.8% vs 6.3%, P=0.047).13 In the diabetes cohort,

4.2% of patients were found to be infected with HCV compared

with 1.6% of control patients (P =0.02). HCV genotype 2a was

observed in 29% of HCV-RNA-positive diabetic patients versus

3% of local HCV-infected controls (P <0.005).15 In India, Out of

the 192 T2DM patients screened, prevalence rate of HCV sero-

positivity is found to be 5.7% (11/192), higher in males.16 In

China, the seroprevalence of HBsAg was 21.30% in T2DM

patients (72/338), which was significantly higher than in non-

diabetics (15.53%).17

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This study estimated the seroprevalence of HBV and HCV

infections among T2DM patients. It also explored possibility of

associated factors with these infections. The prevalence of HBV

infection was low, but higher than that HCV in type 2 diabetics.

Seroprevalence of HBV in this study (3.0%) is similar to other

studies carried out in Bangladesh.9,18-21 However, the results are

contrary to other studies conducted in various countries,12,17 all

of which reported a higher seroprevalence rate of HBV in

diabetic patients than in nondiabetics. Seroprevalence of anti-

HCV antibody (0.48%) was very low in our study which is

similar to a study in general population of Bangladesh.11 The

seroprevalence of hepatitis C in the T2DM patients is in

consonance with a study conducted in Nigeria,23 which recorded

no prevalence of HCV infection among T2DM individuals, in a

descriptive case-control study.

The complex interaction of chronic HBV and HCV infections

with the host hepatic glucose and lipid metabolism, however,

has not been fully understood and remains to be determined.

This study has some limitations. We could not confirm the

results of screening by polymerase chain reaction to detect HBV

and HCV might have led to many false-negatives.

CONCLUSION

The seroprevalence of HBV was higher than that of HCV in

T2DM patients. T2DM patients would require necessary

preventive measures like prophylaxis, to reduce the risk of HBV

infection and its ramifications.

ACKNOWLEDGEMENT

This work was done with financial contribution from Roche

Bangladesh. We pay gratitude to the patients and staff of the

department of GHPD and health education of BIRDEM General

hospital.

DECLARATION

Part of this work was presented at the APASL annual meeting in

Singapore in 2013.

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