Dual Infection with Hepatitis B Virus and Hepatitis C Virus Correlated with Type 2 Diabetes Mellitus
received06 September 2018
revised11 October 2018
accepted 09 November 2018
17 January 2019 (online)
Background Conflicting data exist regarding the relationship between dual infection of hepatitis B virus (HBV) and hepatitis C virus (HCV) with type 2 diabetes mellitus (T2DM). We assessed dual infection of HBV and HCV with the levels of blood glucose and development of DM.
Methods A total of 9621 participants in a community-based study were enrolled from 18 towns in Maoli county of Taiwan. Blood samples were collected and tested for hepatitis B surface antigen (HBsAg) and antibodies (HBsAb), antibodies against hepatitis C virus (anti-HCV) and fasting plasma glucose. DM was defined as fasting plasma glucose≥126 mg per 100 ml.
Results Only 0.7% of total participants had HBV/HCV coinfection. The prevalence of HBV and HCV monoinfection were 9.9 and 5.7%, respectively. Adjusted blood glucose levels and development risk of T2DM (odds ratio [OR], 2.55; p<0.001) were significantly high among HBV/HCV coinfection group using multivariate linear regression adjusted for age, gender, education, race and BMI. Furthermore, using multivariate logistic regression models adjusted for covariates, HCV mono-and HBV/ HCV coinfection significantly increased on blood glucose levels.
Conclusions Our study shows HBV/HCV coinfection was significantly correlated with blood glucose levels. A significant proportion (28%) of participants with HBV/HCV coinfection developed T2DM. Although the precise mechanisms of dual positive infection of HBV and HCV are unclear, there is increasing evidence that dual infection of HCV and HBV is strongly associated with the development of T2DM.
- 1 Liu Z, Hou J. Hepatitis B virus (HBV) and hepatitis C virus (HCV) dual infection. Int J Med Sci 2006; 3: 57-62
- 2 Freeman AJ, Dore GJ, Law MG. et al. Estimating progression to cirrhosis in chronic hepatitis C virus infection. Hepatology (Baltimore, Md) 2001; 34: 809-816 doi:10.1053/jhep.2001.27831
- 3 Dai CY, Yu ML, Chuang WL. et al. Influence of hepatitis C virus on the profiles of patients with chronic hepatitis B virus infection. J Gastroenterol Hepatol 2001; 16: 636-640
- 4 Chu CJ, Lee SD. Hepatitis B virus/hepatitis C virus coinfection: epidemiology, clinical features, viral interactions and treatment. J Gastroenterol Hepatol 2008; 23: 512-520 doi:10.1111/j.1440-1746.2008.05384.x
- 5 Desbois AC, Cacoub P. Diabetes mellitus, insulin resistance and hepatitis C virus infection: A contemporary review. World J Gastroenterol 2017; 23: 1697-1711 doi:10.3748/wjg.v23.i9.1697
- 6 Huang JF, Dai CY, Hwang SJ. et al. Hepatitis C viremia increases the association with type 2 diabetes mellitus in a hepatitis B and C endemic area: an epidemiological link with virological implication. Am J Gastroenterol 2007; 102: 1237-1243 doi:10.1111/j.1572-0241.2007.01181.x
- 7 Li WC, Lee YY, Chen IC. et al. Association between the hepatitis B and C viruses and metabolic diseases in patients stratified by age. Liver international : Official journal of the international association for the study of the liver 2013; 33: 1194-1202 doi:10.1111/liv.12224
- 8 Naing C, Mak JW, Ahmed SI. et al. Relationship between hepatitis C virus infection and type 2 diabetes mellitus: Meta-analysis. World J Gastroenterol 2012; 18: 1642-1651 doi:10.3748/wjg.v18.i14.1642
- 9 Antonelli A, Ferri C, Fallahi P. et al. Hepatitis C virus infection: Evidence for an association with type 2 diabetes. Diabetes care 2005; 28: 2548-2550
- 10 Guo X, Jin M, Yang M. et al. Type 2 diabetes mellitus and the risk of hepatitis C virus infection: a systematic review. Scientific reports 2013; 3: 2981 doi:10.1038/srep02981
- 11 Hui JM, Sud A, Farrell GC. et al. Insulin resistance is associated with chronic hepatitis C virus infection and fibrosis progression [corrected]. Gastroenterology 2003; 125: 1695-1704
- 12 Bose SK, Ray R. Hepatitis C virus infection and insulin resistance. World J Diabetes 2014; 5: 52-58 doi:10.4239/wjd.v5.i1.52
- 13 Lee JG, Lee S, Kim YJ. et al. Association of chronic viral hepatitis B with insulin resistance. World J Gastroenterol 2012; 18: 6120-6126 doi:10.3748/wjg.v18.i42.6120
- 14 Serfaty L, Capeau J. Hepatitis C, insulin resistance and diabetes: Clinical and pathogenic data. Liver international : Official journal of the International Association for the Study of the Liver 2009; 29 (Suppl. 02) 13-25 doi:10.1111/j.1478-3231.2008.01952.x
- 15 Wang CC, Tseng TC, Kao JH. Hepatitis B virus infection and metabolic syndrome: Fact or fiction?. J Gastroenterol Hepatol 2015; 30: 14-20 doi:10.1111/jgh.12700
- 16 American Diabetes A. Diagnosis and classification of diabetes mellitus. Diabetes care 2010; 33 (Suppl. 01) S62-S69 doi:10.2337/dc10-S062
- 17 Fabiani S, Fallahi P, Ferrari SM. et al. Hepatitis C virus infection and development of type 2 diabetes mellitus: Systematic review and meta-analysis of the literature. Rev Endocr Metab Disord 2018; DOI: 10.1007/s11154-017-9440-1.
- 18 Allison ME, Wreghitt T, Palmer CR. et al. Evidence for a link between hepatitis C virus infection and diabetes mellitus in a cirrhotic population. J Hepatol 1994; 21: 1135-1139
- 19 Zhang J, Shen Y, Cai H. et al. Hepatitis B virus infection status and risk of type 2 diabetes mellitus: A meta-analysis. Hepatology research : The official journal of the Japan Society of Hepatology 2015; 45: 1100-1109 doi:10.1111/hepr.12481
- 20 Moucari R, Asselah T, Cazals-Hatem D. et al. Insulin resistance in chronic hepatitis C: Association with genotypes 1 and 4, serum HCV RNA level, and liver fibrosis. Gastroenterology 2008; 134: 416-423 doi:10.1053/j.gastro.2007.11.010
- 21 Hung CH, Lee CM, Lu SN. Hepatitis C virus-associated insulin resistance: Pathogenic mechanisms and clinical implications. Expert review of anti-infective therapy 2011; 9: 525-533 doi:10.1586/eri.11.33
- 22 Chao LT, Wu CF, Sung FY. et al. Insulin, glucose and hepatocellular carcinoma risk in male hepatitis B carriers: Results from 17-year follow-up of a population-based cohort. Carcinogenesis 2011; 32: 876-881 doi:10.1093/carcin/bgr058
- 23 Mena A, Pedreira JD, Castro A. et al. Metabolic syndrome association with fibrosis development in chronic hepatitis B virus inactive carriers. J Gastroenterol Hepatol 2014; 29: 173-178 doi:10.1111/jgh.12432
- 24 Pais R, Rusu E, Ratziu V. The impact of obesity and metabolic syndrome on chronic hepatitis B and drug-induced liver disease. Clinics in liver disease 2014; 18: 165-178 doi:10.1016/j.cld.2013.09.015
- 25 Douglas MW, George J. Molecular mechanisms of insulin resistance in chronic hepatitis C. World J Gastroenterol 2009; 15: 4356-4364
- 26 Chiang CH, Lai JS, Hung SH. et al. Serum adiponectin levels are associated with hepatitis B viral load in overweight to obese hepatitis B virus carriers. Obesity (Silver Spring, Md) 2013; 21: 291-296 doi:10.1002/oby.20000