Association of hepatitis C virus infection and diabetes mellitus

Endocrinologist

Volumn 16, Issue 1, 2006, Pages 41-48

  Mugo, Maryann ^a   Matta, Ravina ^a   Kurukulasuriya, L Romayne ^a   Sowers, James R ^a,b  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Chronic hepatitis C infection; Diabetes mellitus type 2; Hepatic steatosis; Insulin resistance; Insulin signaling

Indexed keywords

ALPHA INTERFERON;

CANCER RISK; CHRONIC DISEASE; COMORBIDITY; DIABETES MELLITUS; DISEASE ASSOCIATION; FATTY LIVER; HEPATITIS C; HEPATITIS C VIRUS; HIGH RISK PATIENT; HUMAN; INSULIN RESISTANCE; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOPHYSIOLOGY; REVIEW; SCREENING; VIRUS INFECTION;

EID: 33748590792     PISSN: 10512144     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.ten.0000194250.94931.d0     Document Type: Review

References (91)

1. Alter MJ, Kruszon-Moran D, Nainan OV, et al. The prevalence of hepatitis C virus infection in the United States 1988 through 1994. N Engl J Med. 1999;3341:556-562.
2. Flamm SI. Chronic hepatitis C virus infection. JAMA. 2003;289:2413-2417.
3. Bahtiyar G, Shin JJ, Aytaman A, et al. Association of diabetes and hepatitis C infection: epidemiologic evidence and pathophysiologic insights. Current Diabetes Reports. 2004;4:194-198.
4. Knobler H, Schihmanter R. Increased risk of type-2 diabetes in noncirrhotic patients with chronic HCV infection. Mayo Clin Proc. 2000;75:355-359.
5. 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. 1996;24:645.
6. Brischetto R, Amore MG, Calcara G. Prevalence and significance of type-2 DM in chronic liver disease, correlated with HCV. Ann Ital Med. 2003;18:4-5.
7. Yang SQ, Chen HS, Ji LN, et al. Relationship between chronic hepatitis C and type 2 diabetes mellitus. Chinese Journal of Experimental and Clinical Virology. 2003;17:46-49.
8. Crania S, Taylor K, Tom BD, et al. Further evidence for an association between non-insulin-dependent DM and chronic hepatitis C virus infection. Hepatology. 1999;30:1059-1063.
9. Mehta S, Brancati F, Thomas D, et al. Hepatitis C virus infection and incident type-2 diabetes. Hepatology. 2003;38.
10. Tong MJ, El-Farra NS, Reikes AR, et al. Clinical outcomes after transfusion-associated hepatitis C. N Engl J Med. 1995;332:1463-1466.
11. Petrides AS, DeFronzo RA. Glucose and insulin metabolism in cirrhosis. J Hepatol. 1989;8:107-114.
12. Merli M, Leonetti F, Riggio O, et al. Glucose intolerance and insulin resistance in cirrhosis are normalized after liver transplantation. Hepatology. 1999;30:649-654.
13. Lecube A, Hernandez C, Genesca J, et al. High prevalence of glucose abnormalities in patients with hepatitis C virus infection. Diabetes Care. 27:1171-1175.
14. Gray H, Wreghitt T, et al. High prevalence of hepatitis C infection in Afro-Caribbean patients with type 2 diabetes mellitus and abnormal LFT. Diabetes Med. 1995;12:244-249.
15. Sotiropolous A, Peppas TA, Skrilos E, et al. Low prevalence of hepatitis C infection in Greek diabetic patients. Diabetes Med. 1999;16:250-252.
16. Tohda G, Oida K, Higashi S, et al. Interferon alpha and development of type 1 diabetes - a case without insulin resistance [Letter]. Diabetes Care. 1998;21:1774.
17. Schories M, Reincke M. Autoantibodies against islet cell antigens and type-1 diabetes after treatment with interferon alpha. Adaeutsche Medizinische. 2004;129:1120-1124.
18. Mangia A, Sciavone G, Lezzi G, et al. HCV and diabetes mellitus: evidence for a negative association. Am J Gastroenterol. 1998;93:2363-2367.
19. Picerno I, Di Pietro A, et al. Is Diabetes mellitus a risk factor for HCV infection? Annali di Igiene. 2002;14:473-477.
20. Rudoni S, Petit JM, Bour JB, et al. HCV infection and diabetes mellitus: influence of the use of fingerstick devices on nosocomial transmission. Diabetes Metab. 1999;25:502-505.
21. Thuluvath PJ, John PR. Association between hepatitis C, DM, and race, a case-control study. Am J Gastroenterol. 2003;98:438-441.
22. Harris MI, Flegal KM, Cowie CC, et al. Prevalence of diabetes, impaired fasting glucose tolerance in the US adults. The third national Health and Nutrition Examination Survey. 1988-1994. Diabetes Care. 1998;21:518-524.
23. Arao M, Murase K, Kusakabe A, et al. Prevalence of diabetes mellitus in Japanese patients infected chronically with hepatitis C virus. J Gastroenterol. 2003;38:355-360.
24. Wilson C. Hepatitis C infection and type 2 diabetes in American-Indian women. Diabetes Care. 27:2116-2119.
25. Mason AL, Lau JY, et al. Association of diabetes mellitus and chronic hepatitis C infection. Hepatology. 1999;29:328-333.
26. Labrapoulou-Karatza C, et al. High prevalence of diabetes mellitus among beta-thalassemic patients with chronic hepatitis C. Eur J Gastroenterol Hepatol. 1999;11:1033-1036.
27. White MF, Kahn CR. The insulin signaling system. J Biol Chem. 1994;269:1-4.
28. Sesti G, Federici M, Hribal ML, et al. Defects of the insulin receptor substrate (IRS) system in human metabolic disorders. FASEB J. 2001;15:2099-2111.
29. Dominici E, Hauck S, et al. Increased insulin sensitivity and up regulation of the insulin receptor, insulin receptor substrate (IRS)-1 and IRS-2 in liver of Ames dwarf mice. J Endocrinol. 2002;173:81-94.
30. Cantley LC. The phosphoinositol 3 kinase pathway. Science. 2002;296:1655-1657.
31. Aytug S, Reich D, Shapiro LE, et al. Impaired IRS-1 /PI3 -kinase signaling in patients with HCV: a mechanism for increased prevalence of type 2. Diabetes Hepatology. 2003;38:1384-1392.
32. Shintani Y, Fujie H, Miyoshi H, et al. Hepatitis C infection and diabetes: direct involvement of the virus in the development of insulin resistance. Gastroenterology. 2004;126:840-848.
33. McFarlane S, Banerji M, Sowers JR. Insulin resistance and cardiovascular disease. J Clin Endocrinol Metab. 2001;86:713-718.
34. Nelson DR, Lim HL Marousis CG, et al. Activation of tumor necrosis factor alpha system in chronic hepatitis C virus infection. Dig Dis Sci. 1997;42:2487-2494.
35. Hotamisligil GS. The role of TNF alpha and TNF receptors in obesity and insulin resistance. J Intern Med. 1999;245:621-625.
36. Hussain MJ, Lau JY, Williams R, et al. Hepatic expression of tumor necrosis factor alpha in chronic hepatitis B virus infection. J Clin Pathol. 1994;47:1112-1115.
37. Goodman ZD, Ishalk KG. Histopathology of hepatitis C virus infection. Semin Liver Dis. 1995;15:70-81.
38. Rubbia-Brandt L, Leandro G, Spahe L, et al. Liver steatosis in chronic hepatitis C; a morphological sign suggesting infection with HCV genotype 3. Histopathology. 2001;39:119-124.
39. Brunt EM, Ramrakhiani S, Cordes BG, et al. Concurrence of histologic features of steatohepatitis with other forms of chronic liver disease. Mod Pathol. 2003;16:49-56.
40. Petit JM, Bour JB, Galland J, et al. Risk factors for diabetes mellitus and early insulin resistance in chronic hepatitis C. J Hepatol. 2001;35:279-283.
41. Marchesini G, Brizi M, Bianchi G, et al. Non alcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes. 2001;50:1844-1850.
42. Sanyal AJ, Campbell-Sargent C, Mirshahi F, et al. Non alcoholic steatohepatitis; association of insulin resistance and mitochondrial abnormalities. Gastroenterology. 2001;120:1183-1192.
43. Marchesini G, Brizi M, Bianchi G, et al. Non alcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes. 2001;50:1844-1850.
44. Seppala-Lindroos A, Vehkavaara S, Hakkinen AM, et al. Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum fatty acids independent of obesity in normal men. J Clin Endocrinol Metab. 2002;87:3023-3028.
45. Lonardo A, Adinolfi LE, Loria P, et al. Steatosis and hepatitis C virus: mechanisms and significance for hepatic and extrahepatic disease. Gastroenterology. 2004;126:586-597.
46. Kim KJ, Fillmore JJ, Chen Y, et al. Tissue specific over expression of lipoprotein lipase causes tissue-specific insulin resistance. Proc Natl Acad Sci U S A. 2001;98:7522-7527.
47. Clarke SD. Non alcoholic steatosis and steato hepatitis: molecular mechanism for polyunsaturated fatty acid regulation of gene transcription. Am J Physiol Gastrointest Liver Physiol. 2001;281:G865-G869.
48. Kahn BB, Flier JS. Obesity and insulin resistance. J Clin Invest. 2000;106:473-481.
49. Mehta S, Brancati FL, Sulkowski MS, et al. Prevalence of diabetes Mellitus among persons with hepatitis C virus infection in the United States. Ann Intern Med. 2000;133:592-599.
50. Peterson KF, Befroy D, Dufour S, et al. Mitochondrial dysfunction in the elderly: possible role of insulin resistance. Science. 2003;300:1140-1142.
51. Hui JM, Sud A, Farrell GC, et al. Insulin resistance is associated with chronic hepatitis C virus infection fibrosis progression. Gastroenterology. 2003;125:1695-1704.
52. Paradis V, Perlemuter G, Bonvoust F, et al. High glucose and hyperinsulinemia stimulate connective tissue growth factor expression: a potential mechanism involved in progression to fibrosis in nonalcoholic steatohepatitis. Hepatology. 2001;34:738-774.
53. Ford E, Cogswell M. Diabetes and serum ferritin concentration among US adults. Diabetes Care. 1999;22:1978-1983.
54. Riggio O Montagnese F, Fiore P, et al. Iron overload in patients with chronic viral hepatitis: how common is it? Am J Gastroenterol. 1997;92:1298-1301.
55. Paris R. Association of hepatitis C and diabetes mellitus [Letter]. Ann Intern Med. 2001;135:141-142.
56. Hernandez C, Genesca J, Ignasi Esteban J, et al. Relationship between iron stores and diabetes mellitus in patients infected by hepatitis C virus: a case-control study. Med Clin. 2000;115:21-22.
57. Jehn M, Clark JM, Guallar E. Serum ferritin and risk of the metabolic syndrome in US adults. Diabetes Care. 2004;27:2422-2428.
58. Hassan M, Hwang LY, Chiq J, et al. Risk factors for hepatocellular carcinoma: synergism of alcohol with viral hepatitis and diabetes mellitus. Hepatology. 2002;36:1206-1213.
59. Sobel D, Ewel CH, Zeligs B, et al. Poly I:C induction of alpha-interferon in the diabetes-prone BB and normal Wistar rats: dose-response relationships. Diabetes. 1994;43:518-522.
60. Fabris P, Betterle C, Floreani A, et al. Development of type 1 diabetes during interferon alpha treatment for chronic HCV infection [Letter]. Lancet. 1992;340:548.
61. Koivisto VA, Pelkonen R, Cantel K, et al. Effect of interferon on glucose tolerance and insulin sensitivity. Diabetes. 1989;38:641-647.
62. Koivisto VA. Interferon alpha and development of type 2 diabetes [Letter]. Lancet. 1992;340:1236.
63. Di Cesare E, Previti M, Russo F. Interferon alpha therapy may induce insulin auto antibody development in patients with chronic viral hepatitis. Dig Dis Sci. 1996;41:1672-1677.
64. Grimbert S, Valens P, Levy-Marchal, et al. High prevalence of diabetes mellitus in patients with chronic hepatitis. A case control study. Gastroenterol Clin Biol. 1996;20:544-548.
65. Gowans EJ. Distribution of markers of hepatitis C infection throughout the body. Semin Liver Dis. 2000;20:85-102.
66. Yan FM, Chen AS, Hao F, et al. Hepatitis C virus may infect extra hepatic tissues in patients with hepatitis C. World J Gastroenterol. 2000;6:805-811.
67. El-Serag HB, Mason AC. Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med. 1999;340:745-750.
68. El-Serag HB, Mason AC, Key C. Trends in survival of patients with hepatocellular carcinoma between 1977 and 1996 in the United States. Hepatology. 2001;33:62-65.
69. El-Serag HB, Mason AC. Risk factors for the rising rates of primary liver cancer in the United States. Arch Intern Med. 2000;160:3227-3230.
70. El-Serag HB, Richardson PA, Everhart JE, et al. The role of diabetes in hepatocellular carcinoma: a case-control study among united states veterans. Am J Gastroenterol. 2001;96:2462-2467.
71. Yu MC, Tong MJ, Govindarajan S, et al. Non-viral risk factors for hepatocellular carcinoma in a low risk population, the non-Asians of Los Angeles county, California. J Natl Cancer Inst. 1991;83:1820-1826.
72. Tazawa J, Maeda M, Nakagawa M, et al. Diabetes mellitus may be associated with hepatocarcinogenesis in patients with chronic hepatitis C. Dig Dis Sci. 2002;47:4:710-715.
73. Yoshida H, Shiratori Y, Moriyama M, et al. Interferon therapy reduces the risk for hepatocellular carcinoma: national surveillance program of cirrhotic and non-cirrhotic patients with chronic hepatitis C in Japan. Ann Intern Med. 1999;131:174-181.
74. Toyoda H, Kumada T, Nakano S, et al. Impact of diabetes mellitus on the prognosis of patients with hepatocellular carcinoma. Cancer. 2001;91:957-963.
75. Chiba T, Matsuzaki Y, Abei M, et al. Multivariate analysis of risk factors for hepatocellular carcinoma in patients with hepatitis C virusrelated liver cirrhosis. J Gastroenterol. 1996;31:552-558.
76. Tazawa J, Maeda M, Nakagawa M, et al. Diabetes mellitus may be associated with hepatocarcinogenesis in patients with chronic hepatitis C. Dig Dis Sci. 2002;47:710-715.
77. Ueno Y, Moriyama M, Uchida T, et al. Irregular regeneration of hepatocytes is an important factor in the hepatocarcinogenesis of liver disease. Hepatology. 2001;33:357-362.
78. Bruno S, Silini E, Crosigiani A, et al. Hepatitis C virus genotypes and risk of hepatocellular carcinoma in cirrhosis: a prospective study. Hepatology. 1997;25:754-758.
79. Moriya K, Fujie H, Shintani Y, et al. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mouse. Nat Med. 1998;4:1065-1067.
80. Barba G, Harper F, Harada T, et al. Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci U S A. 1997;94:1200-1205.
81. Ohata K, Hamasaki K, Toriyama K, et al. Hepatic steatosis is a risk factor for hepatocellular carcinoma in patients with chronic hepatitis C virus infection. Cancer. 2003;97:3036-3043.
82. Moore MA, Park CB, Tsuda H. Implications of the hyperinsulinemia diabetes-cancer risk for preventive efforts. Eur J Cancer Prev. 1998;7:89-107.
83. Chiu B, Viira E, Tucker W, et al. Chlamydia pneumoniae, cytomegalovirus and herpes simplex virus in atherosclerosis of the carotid artery. Circulation. 1997;96:2144-2148.
84. Simo R, Hernandez C, Genesca J, et al. High prevalence of hepatitis C virus infection in diabetic patients. Diabetes Care. 1996;19:998-1000.
85. Fukui M, Nakamura N. Letter. JAMA. 2003;289:1245-1246.
86. Ludewig B, Freigang S, Jaggi M, et al. Linking immune-mediated arterial inflammation and cholesterol-induced atherosclerosis in a transgenic mouse model. Proc Natl Acad Sci U S A. 2000;97:12752-12757.
87. Sens YAS, Silva VDST, Malafronte P, et al. Posttransplant diabetes mellitus in renal transplant patients with hepatitis C virus. Transplant Proc. 2004;36:886-888.
88. Finni PES, Souza ERM, Rioja S, et al. Is hepatitis C a risk factor to posttransplant diabetes mellitus after renal transplantation in patients using tacrolimus? Transplant Proc. 2004;36:884-885.
89. Bigam DL, Pennington JJ, Croxford R, et al. Hepatitis C related cirrhosis: a predictor of diabetes after liver transplantation. Hepatology. 2000;32:87-90.
90. Al Dosary AA, Ramji AS, Elliot TG, et al. Post-liver transplantation diabetes mellitus: an association with hepatitis C. Liver Transplant. 2002;8:356-361.
91. Butt A, Fultz SL, Kwoh CK, et al. Risk of diabetes in HIV infected veterans pre- and post-HAART and the role of HCV co-infection. Hepatology. 2004;40:115-119.