Journal of Hepatology
Volume 49, Issue 5 , Pages 831-844 , November 2008

Hepatitis C infection and risk of diabetes: A systematic review and meta-analysis

  • Donna L. White

      Affiliations

    • Sections of Gastroenterology and Hepatology and Health Services Research, Baylor College of Medicine, Michael E. DeBakey VA Medical Center, Houston, TX 77030, USA
    • Houston Center for Quality of Care and Utilization Studies and Section of Gastroenterology, Michael E. DeBakey VA Medical Center, Houston, TX 77030, USA
    • ,
  • Vlad Ratziu

      Affiliations

    • Université Pierre et Marie Curie and Assistance Publique, Hôpitaux de Paris, Service d’Hépatogastroentérologie, Groupe Hospitalier Pitié Salpêtrière, Paris, France
    • ,
  • Hashem B. El-Serag

      Affiliations

    • Sections of Gastroenterology and Hepatology and Health Services Research, Baylor College of Medicine, Michael E. DeBakey VA Medical Center, Houston, TX 77030, USA
    • Houston Center for Quality of Care and Utilization Studies and Section of Gastroenterology, Michael E. DeBakey VA Medical Center, Houston, TX 77030, USA
    • Corresponding Author InformationCorresponding author.

References 

  1. NIH Consensus Statement on Management of Hepatitis C: 2002. NIH Consens State Sci Statements 2002;19:1–46.
  2. Zignego AL, Ferri C, Pileri SA, Caini P, Bianchi FB. Extrahepatic manifestations of Hepatitis C Virus infection: a general overview and guidelines for a clinical approach. Dig Liver Dis. 2007;39:2–17
  3. Romero-Gomez M, Del Mar Viloria M, Andrade RJ, Salmeron J, Diago M, Fernandez-Rodriguez CM, et al. Insulin resistance impairs sustained response rate to peginterferon plus ribavirin in chronic hepatitis C patients. Gastroenterology. 2005;128:636–641
  4. Hui JM, Sud A, Farrell GC, Bandara P, Byth K, Kench JG, et al. Insulin resistance is associated with chronic hepatitis C virus infection and fibrosis progression [corrected]. Gastroenterology. 2003;125:1695–1704
  5. Antonelli A, Ferri C, Fallahi P, Pampana A, Ferrari SM, Goglia F, et al. Hepatitis C virus infection: evidence for an association with type 2 diabetes. Diabetes Care. 2005;28:2548–2550
  6. Antonelli A, Ferri C, Fallahi P, Sebastiani M, Nesti C, Barani L, et al. Type 2 diabetes in hepatitis C-related mixed cryoglobulinaemia patients. Rheumatology (Oxford). 2004;43:238–240
  7. Chen HF, Li CY, Chen P, See TT, Lee HY. Seroprevalence of hepatitis B and C in type 2 diabetic patients. J Chin Med Assoc. 2006;69:146–152
  8. Howard AA, Klein RS, Schoenbaum EE. Association of hepatitis C infection and antiretroviral use with diabetes mellitus in drug users. Clin Infect Dis. 2003;36:1318–1323
  9. Li-Ng M, Tropp S, Danoff A, Bini EJ. Association between chronic hepatitis B virus infection and diabetes among Asian Americans and Pacific Islanders. Dig Liver Dis. 2007;39:549–556
  10. Mason AL, Lau JY, Hoang N, Qian K, Alexander GJ, Xu L, et al. Association of diabetes mellitus and chronic hepatitis C virus infection. Hepatology. 1999;29:328–333
  11. Sangiorgio L, Attardo T, Gangemi R, Rubino C, Barone M, Lunetta M. Increased frequency of HCV and HBV infection in type 2 diabetic patients. Diabetes Res Clin Pract. 2000;48:147–151
  12. Okan V, Araz M, Aktaran S, Karsligil T, Meram I, Bayraktaroglu Z, et al. Increased frequency of HCV but not HBV infection in type 2 diabetic patients in Turkey. Int J Clin Pract. 2002;56:175–177
  13. Simo R, Hernandez C, Genesca J, Jardi R, Mesa J. High prevalence of hepatitis C virus infection in diabetic patients. Diabetes Care. 1996;19:998–1000
  14. Bigam DL, Pennington JJ, Carpentier A, Wanless IR, Hemming AW, Croxford R, et al. Hepatitis C-related cirrhosis: a predictor of diabetes after liver transplantation. Hepatology. 2000;32:87–90
  15. El-Zayadi AR, Selim OE, Hamdy H, Dabbous H, Ahdy A, Moniem SA. Association of chronic hepatitis C infection and diabetes mellitus. Trop Gastroenterol. 1998;19:141–144
  16. Mehta SH, Brancati FL, Strathdee SA, Pankow JS, Netski D, Coresh J, et al. Hepatitis C virus infection and incident type 2 diabetes. Hepatology. 2003;38:50–56
  17. Imazeki F, Yokosuka O, Fukai K, Kanda T, Kojima H, Saisho H. Prevalence of diabetes mellitus and insulin resistance in patients with chronic hepatitis C: comparison with hepatitis B virus-infected and hepatitis C virus-cleared patients. Liver Int. 2008;28:355–362
  18. Butt AA, Khan UA, McGinnis KA, Skanderson M, Kent KC. Co-morbid medical and psychiatric illness and substance abuse in HCV-infected and uninfected veterans. J Viral Hepatitis. 2007;14:890–896
  19. El-Serag HB, Hampel H, Yeh C, Rabeneck L. Extrahepatic manifestations of hepatitis C among United States male veterans. Hepatology. 2002;36:1439–1445
  20. Ledergerber B, Furrer H, Rickenbach M, Lehmann R, Elzi L, Hirschel B, et al. Factors associated with the incidence of type 2 diabetes mellitus in HIV-infected participants in the Swiss HIV Cohort Study. Clin Infect Dis. 2007;45:111–119
  21. Akbar DH, Siddique AM, Ahmed MM. Prevalence of Type-2 diabetes in patients with hepatitis C and B virus infection in Jeddah, Saudi Arabia. Med Prin Pract. 2002;11:82–85
  22. Papatheodoridis GV, Chrysanthos N, Savvas S, Sevastianos V, Kafiri G, Petraki K, et al. Diabetes mellitus in chronic hepatitis B and C: prevalence and potential association with the extent of liver fibrosis. J Viral Hepatitis. 2006;13:303–310
  23. Picerno I, Di Pietro A, Spataro P, Di Benedetto A, Romano G, Scoglio ME. Is diabetes mellitus a risk factor for HCV infection?. Ann Ig. 2002;14:473–477
  24. Costa LM, Mussi AD, Brianeze MR, Souto FJ. Hepatitis C as a risk factor for diabetes type 2: lack of evidence in a hospital in central-west Brazil. Braz J Infect Dis. 2008;12:24–26
  25. Stapleton JT, Bennett K, Bosch RJ, Polgreen PM, Swindells S. Effect of antiretroviral therapy and hepatitis c co-infection on changes in lipid levels in HIV-Infected patients 48 weeks after initiation of therapy. HIV Clin Trials. 2007;8:429–436
  26. Butt AA, Evans R, Skanderson M, Shakil AO. Comorbid medical and psychiatric conditions and substance abuse in HCV infected persons on dialysis. J Hepatol. 2006;44:864–868
  27. Lecube A, Hernandez C, Genesca J, Esteban JI, Jardi R, Simo R. High prevalence of glucose abnormalities in patients with hepatitis C virus infection: a multivariate analysis considering the liver injury. Diabetes Care. 2004;27:1171–1175
  28. Mehta SH, Brancati FL, Sulkowski MS, Strathdee SA, Szklo M, Thomas DL. Prevalence of type 2 diabetes mellitus among persons with hepatitis C virus infection in the United States. Hepatology. 2001;33:1554
  29. Butt AA, Fultz SL, Kwoh CK, Kelley D, Skanderson M, Justice AC. Risk of diabetes in HIV infected veterans pre- and post-HAART and the role of HCV coinfection. Hepatology. 2004;40:115–119
  30. Huang JF, Dai CY, Hwang SJ, Ho CK, Hsiao PJ, Hsieh MY, 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
  31. Jain MK, Aragaki C, Fischbach L, Gibson S, Arora R, May L, et al. Hepatitis C is associated with type 2 diabetes mellitus in HIV-infected persons without traditional risk factors. HIV Med. 2007;8:491–497
  32. Noto H, Raskin P. Hepatitis C infection and diabetes. J Diabetes Complicat. 2006;20:113–120
  33. Mehta SH, Strathdee SA, Thomas DL. Association between hepatitis C virus infection and diabetes mellitus. Epidemiol Rev. 2001;23:302–312
  34. Fabrizi F, Martin P, Dixit V, Bunnapradist S, Kanwal F, Dulai G. Post-transplant diabetes mellitus and HCV seropositive status after renal transplantation: meta-analysis of clinical studies. Am J Transpl. 2005;5:2433–2440
  35. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283:2008–2012
  36. Petiti DB. Meta-analysis, decision analysis and cost-effectiveness analysis. Methods for quantitative synthesis in medicine. 2nd ed.. New York: Oxford University Press; 2000;
  37. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539–1558
  38. Dersimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–188
  39. Peduzzi P, Concato J, Kemper E, Holford TR, Feinstein AR. A simulation study of the number of events per variable in logistic regression analysis. J Clin Epidemiol. 1996;49:1373–1379
  40. Egger M, Davey SG, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629–634
  41. Arao M, Murase K, Kusakabe A, Yoshioka K, Fukuzawa Y, Ishikawa T, et al. Prevalence of diabetes mellitus in Japanese patients infected chronically with hepatitis C virus. J Gastroenterol. 2003;38:355–360
  42. Boschi-Pinto C, Stuver S, Okayama A, Trichopoulos D, Orav EJ, Tsubouchi H, et al. A follow-up study of morbidity and mortality associated with hepatitis C virus infection and its interaction with human T lymphotropic virus type I in Miyazaki, Japan. J Infect Dis. 2000;181:35–41
  43. Brar I, Shuter J, Thomas A, Daniels E, Absalon J. A comparison of factors associated with prevalent diabetes mellitus among HIV-infected antiretroviral-naive individuals versus individuals in the National Health and Nutritional Examination Survey cohort. J Acq Immun Def Synd. 2007;45:66–71
  44. Caronia S, Taylor K, Pagliaro L, Carr C, Palazzo U, Petrik J, et al. Further evidence for an association between non-insulin-dependent diabetes mellitus and chronic hepatitis C virus infection. Hepatology. 1999;30:1059–1063
  45. Qureshi H, Ahsan T, Mujeeb SA, Jawad F, Mehdi I, Ahmed W, et al. Diabetes mellitus is equally frequent in chronic HCV and HBV infection. J Pak Med Assoc. 2002;52:280–283
  46. Wang CS, Wang ST, Yao WJ, Chang TT, Chou P. Hepatitis C virus infection and the development of type 2 diabetes in a community-based longitudinal study. Am J Epidemiol. 2007;166:196–203
  47. Marzouk D, Sass J, Bakr I, El Hosseiny M, Abdel-Hamid M, Rekacewicz C, et al. Metabolic and cardiovascular risk profiles and hepatitis C virus infection in rural Egypt. Gut. 2007;56:1105–1110
  48. Miyamoto H, Moriishi K, Moriya K, Murata S, Tanaka K, Suzuki T, et al. Involvement of the PA28gamma-dependent pathway in insulin resistance induced by hepatitis C virus core protein. J Virol. 2007;81:1727–1735
  49. Kawaguchi T, Nagao Y, Tanaka K, Ide T, Harada M, Kumashiro R, et al. Causal relationship between hepatitis C virus core and the development of type 2 diabetes mellitus in a hepatitis C virus hyperendemic area: a pilot study. Int J Mol Med. 2005;16:109–114
  50. Masini M, Campani D, Boggi U, Menicagli M, Funel N, Pollera M, et al. Hepatitis C virus infection and human pancreatic beta-cell dysfunction. Diabetes Care. 2005;28:940–941
  51. Shintani Y, Fujie H, Miyoshi H, Tsutsumi T, Tsukamoto K, Kimura S, et al. Hepatitis C virus infection and diabetes: direct involvement of the virus in the development of insulin resistance. Gastroenterology. 2004;126:840–848
  52. Petrides AS, Vogt C, Schulze-Berge D, Matthews D, Strohmeyer G. Pathogenesis of glucose intolerance and diabetes mellitus in cirrhosis. Hepatology. 1994;19:616–627
  53. Taura N, Ichikawa T, Hamasaki K, Nakao K, Nishimura D, Goto T, et al. Association between liver fibrosis and insulin sensitivity in chronic hepatitis C patients. Am J Gastroenterol. 2006;101:2752–2759
  54. Harrison SA. Correlation between insulin resistance and hepatitis C viral load. Hepatology. 2006;43:1168–1169
  55. Petit JM, Bour JB, Galland-Jos C, Minello A, Verges B, Guiguet M, et al. Risk factors for diabetes mellitus and early insulin resistance in chronic hepatitis C. J Hepatol. 2001;35:279–283
  56. Alter MJ. Epidemiology of viral hepatitis and HIV co-infection. J Hepatol. 2006;44(Suppl. 1):S6–S9
  57. Soriano V, Puoti M, Garcia-Gasco P, Rockstroh JK, Benhamou Y, Barreiro P, et al. Antiretroviral drugs and liver injury. AIDS. 2008;22:1–13
  58. Song F, Easterwood A, Gilbody S, Duley L, Sutton AJ. Publication bias. In:  Stevens A,  Abrams K,  Brazier J,  Fitzpatrick R,  Lilford R editor. Handbook of research methods for evidence-based health care – insights from the NHS HTA programme. London: Sage Publications; 2001;
  59. Simo R, Lecube A, Genesca J, Esteban JI, Hernandez C. Sustained virological response correlates with reduction in the incidence of glucose abnormalities in patients with chronic hepatitis C virus infection. Diabetes Care. 2006;29:2462–2466

☆ The authors declare that they do not have anything to disclose regarding funding from industries or conflict of interest with respect to this manuscript. H.B. El-Serag received funding from NIH NIDDK K-24-04-107.

PII: S0168-8278(08)00503-5

doi: 10.1016/j.jhep.2008.08.006

Journal of Hepatology
Volume 49, Issue 5 , Pages 831-844 , November 2008

Article Tools

* Image Usage & Resolution