Relationship between hepatitis C virus infection and type 2 diabetes mellitus: Meta-analysis

World Journal of Gastroenterology

Volumn 18, Issue 14, 2012, Pages 1642-1651

  Naing, Cho ^a   Mak, Joon Wah ^a   Ahmed, Syed Imran ^a   Maung, Mala ^a  

^a INTERNATIONAL MEDICAL UNIVERSITY   (Malaysia)

Author keywords

Hepatitis C; Meta analysis; Observational studies; Type 2 diabetes mellitus

Indexed keywords

ARTICLE; BODY MASS; DISEASE ASSOCIATION; FAMILY HISTORY; HEPATITIS B; HEPATITIS C; HIGH RISK PATIENT; HUMAN; META ANALYSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; OBSERVATIONAL STUDY; PROSPECTIVE STUDY; SELF REPORT; SENSITIVITY ANALYSIS;

EID: 84859966387     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v18.i14.1642     Document Type: Article

References (71)

1. Lauer GM, Walker BD. Hepatitis C virus infection. N Engl J Med 2001; 345: 41-52
2. Mauss S, Berg T, Rockstroh J, Sarrazin C, Wedemeyer H, editors. Hepatology - A Clinical Textbook. 2nd ed. Dusseldorf: Flying publisher, 2010: 19-27
3. Allison ME, Wreghitt T, Palmer CR, Alexander GJ. Evidence for a link between hepatitis C virus infection and diabetes mellitus in a cirrhotic population. J Hepatol 1994; 21: 1135-1139
4. Purcell R. The hepatitis C virus: overview. Hepatology 1997; 26: 11S-14S
5. Mason AL, Lau JY, Hoang N, Qian K, Alexander GJ, Xu L, Guo L, Jacob S, Regenstein FG, Zimmerman R, Everhart JE, Wasserfall C, Maclaren NK, Perrillo RP. Association of diabetes mellitus and chronic hepatitis C virus infection. Hepatology 1999; 29: 328-333
6. Mangia A, Schiavone G, Lezzi G, Marmo R, Bruno F, Villani MR, Cascavilla I, Fantasia L, Andriulli A. HCV and diabetes mellitus: evidence for a negative association. Am J Gastroenterol 1998; 93: 2363-2367
7. Papatheodoridis GV, Chrysanthos N, Savvas S, Sevastianos V, Kafiri G, Petraki K, Manesis EK. Diabetes mellitus in chronic hepatitis B and C: prevalence and potential association with the extent of liver fibrosis. J Viral Hepat 2006; 13: 303-310
8. Chehadeh W, Abdella N, Ben-Nakhi A, Al-Arouj M, Al-Nakib W. Risk factors for the development of diabetes mellitus in chronic hepatitis C virus genotype 4 infection. J Gastroenterol Hepatol 2009; 24: 42-48
9. Negro F. Insulin resistance and HCV: will new knowledge modify clinical management? J Hepatol 2006; 45: 514-519
10. Negro F, Alaei M. Hepatitis C virus and type 2 diabetes. World J Gastroenterol 2009; 15: 1537-1547
11. Serfaty L, Capeau J. Hepatitis C, insulin resistance and diabetes: clinical and pathogenic data. Liver Int 2009; 29 Suppl 2: 13-25
12. Azócar J. Adult Onset Diabetes Mellitus in Hepatitis C Virus Infection. Hepatitis C Support Project. 2003. Available from: URL: http://www.hcvadvocate.org/hcsp/articles/Azocar-1.html. Accessed 25 April 2011.
13. Shepard CW, Finelli L, Alter MJ. Global epidemiology of hepatitis C virus infection. Lancet Infect Dis 2005; 5: 558-567
14. White DL, Ratziu V, El-Serag HB. Hepatitis C infection and risk of diabetes: a systematic review and meta-analysis. J Hepatol 2008; 49: 831-844
15. Higgins JPT, Green S, editors. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [updated March 2011]. The Cochrane Collaboration, 2011. Available from: URL: www.cochrane-handbook.org
16. Review Manager (RevMan) [Computer program] Version 5.1. Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2011
17. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. Ann Intern Med 2009; 151: W65-94
18. Hourigan LF, Macdonald GA, Purdie D, Whitehall VH, Shorthouse C, Clouston A, Powell EE. Fibrosis in chronic hepatitis C correlates significantly with body mass index and steatosis. Hepatology 1999; 29: 1215-1219
19. Hsu CS, Liu CH, Liu CJ, Wang CC, Chen CL, Lai MY, Chen PJ, Chen DS, Kao JH. Association of lipid profiles with hepatitis C viral load in chronic hepatitis C patients with genotype 1 or 2 infection. Am J Gastroenterol 2009; 104: 598-604
20. AlDosary AA, Ramji AS, Elliott TG, Sirrs SM, Thompson DM, Erb SR, Steinbrecher UP, Yoshida EM. Post-liver transplantation diabetes mellitus: an association with hepatitis C. Liver Transpl 2002; 8: 356-361
21. Ma Y, Yan WW. Chronic hepatitis C virus infection and post-liver transplantation diabetes mellitus. World J Gastroenterol 2005; 11: 6085-6089
22. Jain MK, Aragaki C, Fischbach L, Gibson S, Arora R, May L, Vardhineni K, Lee WM. Hepatitis C is associated with type 2 diabetes mellitus in HIV-infected persons without traditional risk factors. HIV Med 2007; 8: 491-497
23. Antonelli A, Ferri C, Fallahi P, Sebastiani M, Nesti C, Barani L, Barale R, Ferrannini E. Type 2 diabetes in hepatitis C-related mixed cryoglobulinaemia patients. Rheumatology (Oxford) 2004; 43: 238-240
24. Labropoulou-Karatza C, Goritsas C, Fragopanagou H, Repandi M, Matsouka P, Alexandrides T. High prevalence of diabetes mellitus among adult beta-thalassaemic patients with chronic hepatitis C. Eur J Gastroenterol Hepatol 1999; 11: 1033-1036
25. Chuang LM, Tsai ST, Huang BY, Tai TY. The status of diabetes control in Asia--a cross-sectional survey of 24 317 patients with diabetes mellitus in 1998. Diabet Med 2002; 19: 978-985
26. Ponce-De-Leon A, Garcia-Garcia Md Mde L, Garcia-Sancho MC, Gomez-Perez FJ, Valdespino-Gomez JL, Olaiz-Fernandez G, Rojas R, Ferreyra-Reyes L, Cano-Arellano B, Bobadilla M, Small PM, Sifuentes-Osornio J. Tuberculosis and diabetes in southern Mexico. Diabetes Care 2004; 27:1584-1590
27. Huang ZS, Huang TS, Wu TH, Chen MF, Hsu CS, Kao JH. Asymptomatic chronic hepatitis B virus infection does not increase the risk of diabetes mellitus: a ten-year observation. J Gastroenterol Hepatol 2010; 25: 1420-1425
28. Khokhar N. Association of chronic hepatitis C virus infection and diabetes mellitus. Pakistan J Med Res 2002; 41. Available from: URL: http://www.pmrc.org.pk/association.htm
29. Samantray J, Zambare S, Seyoum B, Abou-Samra AB. Glucose control and lipid metabolism in African American patients with type 2 diabetes mellitus and chronic hepatitis C viral infection. Endocr Pract 2011; 17: 363-368
30. Fartoux L, Poujol-Robert A, Guéchot J, Wendum D, Poupon R, Serfaty L. Insulin resistance is a cause of steatosis and fibrosis progression in chronic hepatitis C. Gut 2005; 54: 1003-1008
31. 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
32. Grimbert S, Valensi P, Lévy-Marchal C, Perret G, RichardetJP, Raffoux C, Trinchet JC, Beaugrand M. High prevalence of diabetes mellitus in patients with chronic hepatitis C. A case-control study. Gastroenterol Clin Biol 1996; 20: 544-548
33. Zein NN, Abdulkarim AS, Wiesner RH, Egan KS, Persing DH. Prevalence of diabetes mellitus in patients with endstage liver cirrhosis due to hepatitis C, alcohol, or cholestatic disease. J Hepatol 2000; 32: 209-217
34. Kwon SY, Kim SS, Kwon OS, Kwon KA, Chung MG, Park DK, Kim YS, Koo YS, Kim YK, Choi DJ, Kim JH. Prognostic significance of glycaemic control in patients with HBV and HCV-related cirrhosis and diabetes mellitus. Diabet Med 2005; 22: 1530-1535
35. Kobashi-Margáin RA, Gutiérrez-Grobe Y, Ponciano-Rodríguez G, Uribe M, Méndez-Sánchez N. Prevalence of type 2 diabetes mellitus and chronic liver disease: a retrospective study of the association of two increasingly common diseases in Mexico. Ann Hepatol 2010; 9: 282-288
36. Sotiropoulos A, Peppas TA, Skliros E, Apostolou O, Kotsini V, Pappas SI. Low prevalence of hepatitis C virus infection in Greek diabetic patients. Diabet Med 1999; 16: 250-252
37. Ali SS, Ali IS, Aamir AH, Jadoon Z, Inayatullah S. Frequency of hepatitis C infection in diabetic patients. J Ayub Med Coll Abbottabad 2007; 19: 46-49
38. Wilson C. Hepatitis C infection and type 2 diabetes in American-Indian women. Diabetes Care 2004; 27: 2116-2119
39. Mehta SH, Brancati FL, Strathdee SA, Pankow JS, Netski D, Coresh J, Szklo M, Thomas DL. Hepatitis C virus infection and incident type 2 diabetes. Hepatology 2003; 38: 50-56
40. 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 Princ Pract 2002; 11: 82-85
41. Antonelli A, Ferri C, Fallahi P, Pampana A, Ferrari SM, Goglia F, Ferrannini E. Hepatitis C virus infection: evidence for an association with type 2 diabetes. Diabetes Care 2005; 28: 2548-2550
42. Arao M, Murase K, Kusakabe A, Yoshioka K, Fukuzawa Y, Ishikawa T, Tagaya T, Yamanouchi K, Ichimiya H, Sameshima Y, Kakumu S. Prevalence of diabetes mellitus in Japanese patients infected chronically with hepatitis C virus. J Gastroenterol 2003; 38: 355-360
43. Boschi-Pinto C, Stuver S, Okayama A, Trichopoulos D, Orav EJ, Tsubouchi H, Mueller N. 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
44. 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
45. Caronia S, Taylor K, Pagliaro L, Carr C, Palazzo U, Petrik J, O'Rahilly S, Shore S, Tom BD, Alexander GJ. Further evidence for an association between non-insulin-dependent diabetes mellitus and chronic hepatitis C virus infection. Hepatology 1999; 30: 1059-1063
46. 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
47. Gulcan A, Gulcan E, Toker A, Bulut I, Akcan Y. Evaluation of risk factors and seroprevalence of hepatitis B and C in diabetic patients in Kutahya, Turkey. J Investig Med 2008; 56: 858-863
48. 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
49. Huang JF, Dai CY, Hwang SJ, Ho CK, Hsiao PJ, Hsieh MY, Lee LP, Lin ZY, Chen SC, Hsieh MY, Wang LY, Shin SJ, Chang WY, Chuang WL, Yu ML. 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
50. 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
51. Jadoon NA, Shahzad MA, Yaqoob R, Hussain M, Ali N. Seroprevalence of hepatitis C in type 2 diabetes: evidence for a positive association. Virol J 2010; 7: 304
52. Kaabia N, Ben Jazia E, Slim I, Fodha I, Hachfi W, Gaha R, Khalifa M, Hadj Kilani A, Trabelsi H, Abdelaziz A, Bahri F, Letaief A. Association of hepatitis C virus infection and diabetes in central Tunisia. World J Gastroenterol 2009; 15: 2778-2781
53. Knobler H, Schihmanter R, Zifroni A, Fenakel G, Schattner A. Increased risk of type 2 diabetes in noncirrhotic patients with chronic hepatitis C virus infection. Mayo Clin Proc 2000; 75: 355-359
54. Lecube A, Hernández C, Genescà J, Esteban JI, Jardí R, Simó 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
55. 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
56. Marzouk D, Sass J, Bakr I, El Hosseiny M, Abdel-Hamid M, Rekacewicz C, Chaturvedi N, Mohamed MK, Fontanet A. Metabolic and cardiovascular risk profiles and hepatitis C virus infection in rural Egypt. Gut 2007; 56: 1105-1110
57. 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. Ann Intern Med 2000; 133: 592-599
58. Nwokediuko SC, Oli JM. Hepatitis C virus infection in Nigerians with diabetes mellitus. Niger J Clin Pract 2008; 11: 94-99
59. Okan V, Araz M, Aktaran S, Karsligil T, Meram I, Bayraktaroglu Z, Demirci F. Increased frequency of HCV but not HBV infection in type 2 diabetic patients in Turkey. Int J Clin Pract 2002; 56: 175-177
60. Olokoba AB, Badung LH, Abdurrahman MB, Salawu FK, Danburam A, Aderibigbe S, Midala J, Tidi SK. Hepatitis C virus infection in Nigerians with diabetes mellitus. Am J Sci Ind Res 2010; 1: 135-138
61. Qureshi H, Ahsan T, Mujeeb SA, Jawad F, Mehdi I, Ahmed W, Alam SE. Diabetes mellitus is equally frequent in chronic HCV and HBV infection. J Pak Med Assoc 2002; 52: 280-283
62. Rouabhia S, Malek R, Bounecer H, Dekaken A, Bendali Amor F, Sadelaoud M, Benouar A. Prevalence of type 2 diabetes in Algerian patients with hepatitis C virus infection. World J Gastroenterol 2010; 16: 3427-3431
63. Ryu JK, Lee SB, Hong SJ, Lee S. Association of chronic hepatitis C virus infection and diabetes mellitus in Korean patients. Korean J Intern Med 2001; 16: 18-23
64. 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
65. Simó R, Lecube A, Genescà J, Esteban JI, Hernández 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
66. 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
67. Wang LF, Wu CH, Shan Y, Fan XH, Huo N, Lu HY, Xu XY. Prevalence of abnormal glycometabolism in patients with chronic hepatitis C and related risk factors in China. Chin Med J (Engl) 2011; 124: 183-188
68. Weyer C, Bogardus C, Mott DM, Pratley RE. The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus. J Clin Invest 1999; 104: 787-794
69. Maheshwari A, Thuluvath PJ. Endocrine diseases and the liver. Clin Liver Dis 2011; 15: 55-67
70. Everhart J. A confluence of epidemics: does hepatitis C cause type 2 diabetes? Hepatology 2001; 33: 762-763
71. Shintani Y, Fujie H, Miyoshi H, Tsutsumi T, Tsukamoto K, Kimura S, Moriya K, Koike K. Hepatitis C virus infection and diabetes: direct involvement of the virus in the development of insulin resistance. Gastroenterology 2004; 126: 840-848