Interferon therapy in hepatitis C leading to chronic type 1 diabetes

World Journal of Gastroenterology

Volumn 21, Issue 1, 2015, Pages 233-239

  Zornitzki, Taiba ^a   Malnick, Stephen ^a   Lysyy, Lyudmila ^a   Knobler, Hilla ^a  

^a HEBREW UNIVERSITY   (Israel)

Author keywords

Autoimmune diseases; Hepatitis C; Interferon; Pancreatic autoantibodies; Type 1 diabetes

Indexed keywords

AUTOANTIBODY; INTERFERON; ANTIDIABETIC AGENT; ANTIVIRUS AGENT; INSULIN;

ADULT; AGED; ARTICLE; AUTOIMMUNE DISEASE; CAUCASIAN; CONTROLLED STUDY; DIABETIC KETOACIDOSIS; DISEASE COURSE; FEMALE; HEPATITIS C; HUMAN; HYPERGLYCEMIA; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN TREATMENT; JAPANESE (PEOPLE); MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; ONSET AGE; PREVALENCE; THYROID DISEASE; YOUNG ADULT; ASIAN CONTINENTAL ANCESTRY GROUP; AUTOIMMUNITY; CHEMICALLY INDUCED; DIABETES MELLITUS, TYPE 1; ETHNOLOGY; HEPATITIS C, CHRONIC; IMMUNOLOGY; PANCREAS; PROGNOSIS; RISK FACTOR; TIME;

ADULT; AGE OF ONSET; AGED; ANTIVIRAL AGENTS; ASIAN CONTINENTAL ANCESTRY GROUP; AUTOANTIBODIES; AUTOIMMUNITY; DIABETES MELLITUS, TYPE 1; EUROPEAN CONTINENTAL ANCESTRY GROUP; HEPATITIS C, CHRONIC; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; INTERFERONS; MIDDLE AGED; PANCREAS; PREVALENCE; PROGNOSIS; RISK FACTORS; TIME FACTORS; YOUNG ADULT;

EID: 84920887641     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v21.i1.233     Document Type: Article

References (58)

1. Fried MW . Side effects of therapy of hepatitis C and their management. Hepatology 2002; 36: S237-S244 [PMID: 12407599 DOI: 10.1053/jhep.2002.36810]
2. Hashemi N, Rossi S, Navarro VJ, Herrine SK. Safety of peginterferon in the treatment of chronic hepatitis C. Expert Opin Drug Saf 2008; 7: 771-781 [PMID: 18983223 DOI: 10.1517/14740330802423291]
3. Fattovich G, Giustina G, Favarato S, Ruol A. A survey of adverse events in 11,241 patients with chronic viral hepatitis treated with alfa interferon. J Hepatol 1996; 24: 38-47 [PMID: 8834023]
4. 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 [PMID: 11033586]
5. 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 [PMID: 10761489 DOI: 10.4065/75.4.355]
6. Naing C, Mak JW, Ahmed SI, Maung M. Relationship between hepatitis C virus infection and type 2 diabetes mellitus: meta-analysis. World J Gastroenterol 2012; 18: 1642-1651 [PMID: 22529694 DOI: 10.3748/wjg.v18.i14.1642]
7. Lecube A, Hernández C, Genescà J, Simó R. Proinflammatory cytokines, insulin resistance, and insulin secretion in chronic hepatitis C patients: A case-control study. Diabetes Care 2006; 29: 1096-1101 [PMID: 16644643 DOI: 10.2337/ diacare.2951096]
8. del Campo JA, García-Valdecasas M, Rojas L, Rojas Á, Romero-Gómez M. The hepatitis C virus modulates insulin signaling pathway in vitro promoting insulin resistance. PLoS One 2012; 7: e47904 [PMID: 23133528 DOI: 10.1371/ journal.pone.0047904]
9. Knobler H, Zhornicky T, Sandler A, Haran N, Ashur Y, Schattner A. Tumor necrosis factor-alpha-induced insulin resistance may mediate the hepatitis C virus-diabetes association. Am J Gastroenterol 2003; 98: 2751-2756 [PMID: 14687828 DOI: 10.1111/j.1572-0241.2003.08728.x]
10. Fabris P, Betterle C, Floreani A, Greggio NA, de Lazzari F, Naccarato R, Chiaramonte M. Development of type 1 diabetes mellitus during interferon alfa therapy for chronic HCV hepatitis. Lancet 1992; 340: 548 [PMID: 1354296]
11. Nakamura K, Kawasaki E, Imagawa A, Awata T, Ikegami H, Uchigata Y, Kobayashi T, Shimada A, Nakanishi K, Makino H, Maruyama T, Hanafusa T. Type 1 diabetes and interferon therapy: a nationwide survey in Japan. Diabetes Care 2011; 34: 2084-2089 [PMID: 21775762]
12. Schreuder TC, Gelderblom HC, Weegink CJ, Hamann D, Reesink HW, Devries JH, Hoekstra JB, Jansen PL. High incidence of type 1 diabetes mellitus during or shortly after treatment with pegylated interferon alpha for chronic hepatitis C virus infection. Liver Int 2008; 28: 39-46 [PMID: 18031478 DOI: 10.1111/j.1478-3231.2007.01610.x]
13. Eibl N, Gschwantler M, Ferenci P, Eibl MM, Weiss W, Schernthaner G. Development of insulin-dependent diabetes mellitus in a patient with chronic hepatitis C during therapy with interferon-alpha. Eur J Gastroenterol Hepatol 2001; 13: 295-298 [PMID: 11293453]
14. Cozzolongo R, Betterle C, Fabris P, Paola Albergoni M, Lanzilotta E, Manghisi OG. Onset of type 1 diabetes mellitus during peginterferon alpha-2b plus ribavirin treatment for chronic hepatitis C. Eur J Gastroenterol Hepatol 2006; 18: 689-692 [PMID: 16702861]
15. Mofredj A, Howaizi M, Grasset D, Licht H, Loison S, Devergie B, Demontis R, Cadranel JF. Diabetes mellitus during interferon therapy for chronic viral hepatitis. Dig Dis Sci 2002; 47: 1649-1654 [PMID: 12141831]
16. Bhatti A, McGarrity TJ, Gabbay R. Diabetic ketoacidosis induced by alpha interferon and ribavirin treatment in a patient with hepatitis C. Am J Gastroenterol 2001; 96: 604-605 [PMID: 11232722 DOI: 10.1111/j.1572-0241.2001.03571.x]
17. Tosone G, Borgia G, Gentile I, Cerini R, Conte MC, Orlando R, Piazza M. A case of pegylated interferon alpha-related diabetic ketoacidosis: can this complication be avoided? Acta Diabetol 2007; 44: 167-169 [PMID: 17721757 DOI: 10.1007/s00592-007-0259-1]
18. Soultati AS, Dourakis SP, Alexopoulou A, Deutsch M, Archimandritis AJ. Simultaneous development of diabetic ketoacidosis and Hashitoxicosis in a patient treated with pegylated interferon-alpha for chronic hepatitis C. World J Gastroenterol 2007; 13: 1292-1294 [PMID: 17451219]
19. Bosi E, Minelli R, Bazzigaluppi E, Salvi M. Fulminant autoimmune Type 1 diabetes during interferon-alpha therapy: a case of Th1-mediated disease? Diabet Med 2001; 18: 329-332 [PMID: 11437866]
20. Recasens M, Aguilera E, Ampurdanés S, Sánchez Tapias JM, Simó O, Casamitjana R, Conget I. Abrupt onset of diabetes during interferon-alpha therapy in patients with chronic hepatitis C. Diabet Med 2001; 18: 764-767 [PMID: 11606177]
21. Scavone G, Zaccardi F, Manto A, Caputo S, Pitocco D, Ghirlanda G. A case of chronic hepatitis C developing insulin-dependent diabetes, thyroid autoimmunity and stiffperson syndrome as complications of interferon therapy. Diabetes Res Clin Pract 2010; 89: e36-e38 [PMID: 20541278 DOI: 10.1016/j.diabres.2010.05.006]
22. Popescu C, Popescu GA, Arama V. Type 1 diabetes mellitus with dual autoimmune mechanism related to pegylated interferon and ribavirin treatment for chronic HCV hepatitis. J Gastrointestin Liver Dis 2013; 22: 101-104 [PMID: 23539399]
23. Alsabbagh ME, Eisa N, Alraiyes AH, Alraies MC. Chronic hepatitis C therapy: a rare complication revisited. BMJ Case Rep 2013; 2013: bcr2013200514 [PMID: 23893287 DOI: 10.1136/bcr-2013-200514]
24. Oka R, Hiroi N, Shigemitsu R, Sue M, Oshima Y, Yoshida-Hiroi M. Type 1 Diabetes Mellitus Associated with Pegylated Interferon-α Plus Ribavirin Treatment for Chronic Hepatitis C: Case Report and Literature Review. Clin Med Insights Endocrinol Diabetes 2011; 4: 39-45 [PMID: 22879793 DOI: 10.4137/CMED.S7815]
25. Yagyu H, Okada K, Sato S, Yamashita Y, Okada N, Osuga J, Nagasaka S, Sugano K, Ishibashi S. Pegylated interferon-α2b and ribavirin combination therapy induces Hashitoxicosis followed by type 1 diabetes mellitus. Diabetes Res Clin Pract 2012; 95: e52-e54 [PMID: 22154462 DOI: 10.1016/j.diabres.2011.11.016]
26. Yamazaki M, Sato A, Takeda T, Komatsu M. Distinct clinical courses in type 1 diabetes mellitus induced by peg-interferon-alpha treatment for chronic hepatitis C. Intern Med 2010; 49: 403-407 [PMID: 20190473]
27. Shiba T, Morino Y, Tagawa K, Fujino H, Unuma T. Onset of diabetes with high titer anti-GAD antibody after IFN therapy for chronic hepatitis. Diabetes Res Clin Pract 1995; 30: 237-241 [PMID: 8861464]
28. Hayashi M, Kataoka Y, Tachikawa K, Koguchi H, Tanaka H. Dual onset of type 1 diabetes mellitus and Graves' disease during treatment with pegylated interferon alpha-2b and ribavirin for chronic hepatitis C. Diabetes Res Clin Pract 2009; 86: e19-e21 [PMID: 19744739 DOI: 10.1016/j.diabres.2009.08.009]
29. Fujioka T, Honda M, Yoshizaki T, Ogawa M, Matsuno H, Shimokawa K, Koyama K. A case of type 1 diabetes onset and recurrence of Graves' disease during pegylated interferon-α plus ribavirin treatment for chronic hepatitis C. Intern Med 2010; 49: 1987-1990 [PMID: 20847504]
30. Kawazoe T, Araki M, Lin Y, Ogawa M, Okamoto T, Yamamura T, Wakakura M, Murata M. New-onset type 1 diabetes mellitus and anti-aquaporin-4 antibody positive optic neuritis associated with type 1 interferon therapy for chronic hepatitis C. Intern Med 2012; 51: 2625-2629 [PMID: 22989839]
31. Karvonen M, Viik-Kajander M, Moltchanova E, Libman I, LaPorte R, Tuomilehto J. Incidence of childhood type 1 diabetes worldwide. Diabetes Mondiale (DiaMond) Project Group. Diabetes Care 2000; 23: 1516-1526 [PMID: 11023146]
32. Kawasaki E, Matsuura N, Eguchi K. Type 1 diabetes in Japan. Diabetologia 2006; 49: 828-836 [PMID: 16568259 DOI: 10.1007/s00125-006-0213-8]
33. Uonaga T, Yoshida K, Harada T, Shimodahira M, Nakamura Y. Case of type 1 diabetes mellitus following interferon β -1a treatment for multiple sclerosis. Intern Med 2012; 51: 1875-1877 [PMID: 22821104]
34. Zimmet PZ, Rowley MJ, Mackay IR, Knowles WJ, Chen QY, Chapman LH, Serjeantson SW. The ethnic distribution of antibodies to glutamic acid decarboxylase: presence and levels of insulin-dependent diabetes mellitus in Europid and Asian subjects. J Diabetes Complications 1993; 7: 1-7 [PMID: 8481544]
35. Buzzetti R, Di Pietro S, Giaccari A, Petrone A, Locatelli M, Suraci C, Capizzi M, Arpi ML, Bazzigaluppi E, Dotta F, Bosi E. High titer of autoantibodies to GAD identifies a specific phenotype of adult-onset autoimmune diabetes. Diabetes Care 2007; 30: 932-938 [PMID: 17392553 DOI: 10.2337/dc06-1696]
36. Betterle C, Fabris P, Zanchetta R, Pedini B, Tositti G, Bosi E, de Lalla F. Autoimmunity against pancreatic islets and other tissues before and after interferon-alpha therapy in patients with hepatitis C virus chronic infection. Diabetes Care 2000; 23: 1177-1181 [PMID: 10937518]
37. Fabris P, Floreani A, Tositti G, Vergani D, De Lalla F, Betterle C. Type 1 diabetes mellitus in patients with chronic hepatitis C before and after interferon therapy. Aliment Pharmacol Ther 2003; 18: 549-558 [PMID: 12969081]
38. Fabbri C, Jaboli MF, Giovanelli S, Azzaroli F, Pezzoli A, Accogli E, Liva S, Nigro G, Miracolo A, Festi D, Colecchia A, Montagnani M, Roda E, Mazzella G. Gastric autoimmune disorders in patients with chronic hepatitis C before, during and after interferon-alpha therapy. World J Gastroenterol 2003; 9: 1487-1490 [PMID: 12854147]
39. Sylvestre DL, Disston AR, Bui DP. Vogt-Koyanagi-Harada disease associated with interferon alpha-2b/ribavirin combination therapy. J Viral Hepat 2003; 10: 467-470 [PMID: 14633182]
40. Anderson P, Höglund M, Rödjer S. Pulmonary side effects of interferon-alpha therapy in patients with hematological malignancies. Am J Hematol 2003; 73: 54-58 [PMID: 12701122 DOI: 10.1002/ajh.10319]
41. Congeni JP, Kirkpatrick RB. Pegylated interferon induced myasthenia crisis - a case report. J Clin Neuromuscul Dis 2013; 14: 123-125 [PMID: 23492465 DOI: 10.1097/CND.0b013e318285257f]
42. Kim GW, Jwa SW, Song M, Kim HS, Kim BS, Kim MB, Ko HC. Extensive psoriasis induced by pegylated interferon alfa-2a and ribavirin in the treatment of chronic hepatitis C. Ann Dermatol 2013; 25: 479-482 [PMID: 24371397 DOI: 10.5021/ad.2013.25.4.479]
43. Mohokum M, Hartmann P, Schlattmann P. Association of Raynaud's syndrome with interferons. A meta-analysis. Int Angiol 2012; 31: 408-413 [PMID: 22990501]
44. Huang X, Yuang J, Goddard A, Foulis A, James RF, Lernmark A, Pujol-Borrell R, Rabinovitch A, Somoza N, Stewart TA. Interferon expression in the pancreases of patients with type I diabetes. Diabetes 1995; 44: 658-664 [PMID: 7540571]
45. Foulis AK, Farquharson MA, Meager A. Immunoreactive alpha-interferon in insulin-secreting beta cells in type 1 diabetes mellitus. Lancet 1987; 2: 1423-1427 [PMID: 2891993]
46. Chehadeh W, Weill J, Vantyghem MC, Alm G, Lefèbvre J, Wattré P, Hober D. Increased level of interferon-alpha in blood of patients with insulin-dependent diabetes mellitus: relationship with coxsackievirus B infection. J Infect Dis 2000; 181: 1929-1939 [PMID: 10837172 DOI: 10.1086/315516]
47. Devendra D, Eisenbarth GS. Interferon alpha - a potential link in the pathogenesis of viral-induced type 1 diabetes and autoimmunity. Clin Immunol 2004; 111: 225-233 [PMID: 15183143 DOI: 10.1016/j.clim.2004.01.008]
48. Foulis AK, Farquharson MA, Hardman R. Aberrant expression of class II major histocompatibility complex molecules by B cells and hyperexpression of class I major histocompatibility complex molecules by insulin containing islets in type 1 (insulin-dependent) diabetes mellitus. Diabetologia 1987; 30: 333-343 [PMID: 3301484]
49. Stewart TA, Hultgren B, Huang X, Pitts-Meek S, Hully J, MacLachlan NJ. Induction of type I diabetes by interferonalpha in transgenic mice. Science 1993; 260: 1942-1946 [PMID: 8100367]
50. El-Serag HB, Davila JA, Petersen NJ, McGlynn KA. The continuing increase in the incidence of hepatocellular carcinoma in the United States: an update. Ann Intern Med 2003; 139: 817-823 [PMID: 14623619]
51. Wiese M, Fischer J, Löbermann M, Göbel U, Grüngreiff K, Güthoff W, Kullig U, Richter F, Schiefke I, Tenckhoff H, Zipprich A, Berg T, Müller T. Evaluation of liver disease progression in the German hepatitis C virus (1b)-contaminated anti-D cohort at 35 years after infection. Hepatology 2014; 59: 49-57 [PMID: 23929603 DOI: 10.1002/hep.26644]
52. Wiese M, Grüngreiff K, Güthoff W, Lafrenz M, Oesen U, Porst H. Outcome in a hepatitis C (genotype 1b) single source outbreak in Germany - a 25-year multicenter study. J Hepatol 2005; 43: 590-598 [PMID: 16237783]
53. Poynard T, Ratziu V, Charlotte F, Goodman Z, McHutchison J, Albrecht J. Rates and risk factors of liver fibrosis progression in patients with chronic hepatitis c. J Hepatol 2001; 34: 730-739 [PMID: 11434620]
54. Ryder SD, Irving WL, Jones DA, Neal KR, Underwood JC. Progression of hepatic fibrosis in patients with hepatitis C: a prospective repeat liver biopsy study. Gut 2004; 53: 451-455 [PMID: 14960533]
55. van der Meer AJ, Wedemeyer H, Feld JJ, Hansen BE, Manns MP, Zeuzem S, Janssen HL. Is there sufficient evidence to recommend antiviral therapy in hepatitis C? J Hepatol 2014; 60: 191-196 [PMID: 23973931 DOI: 10.1016/j.jhep.2013.07.043]
56. Kowdley KV, Lawitz E, Poordad F, Cohen DE, Nelson DR, Zeuzem S, Everson GT, Kwo P, Foster GR, Sulkowski MS, Xie W, Pilot-Matias T, Liossis G, Larsen L, Khatri A, Podsadecki T, Bernstein B. Phase 2b trial of interferon-free therapy for hepatitis C virus genotype 1. N Engl J Med 2014; 370: 222-232 [PMID: 24428468 DOI: 10.1056/NEJMoa1306227]
57. Sulkowski MS, Gardiner DF, Rodriguez-Torres M, Reddy KR, Hassanein T, Jacobson I, Lawitz E, Lok AS, Hinestrosa F, Thuluvath PJ, Schwartz H, Nelson DR, Everson GT, Eley T, Wind-Rotolo M, Huang SP, Gao M, Hernandez D, McPhee F, Sherman D, Hindes R, Symonds W, Pasquinelli C, Grasela DM. Daclatasvir plus sofosbuvir for previously treated or untreated chronic HCV infection. N Engl J Med 2014; 370: 211-221 [PMID: 24428467 DOI: 10.1056/NEJMoa1306218]
58. Melmed S, Kenneth S, Polonsky KS, Larsen PR, Henry M. Kronenberg HM. Williams textbook of endocrinology. In: Eisenbarth GS, Buse JB. Type 1 Diabetes. 12th ed. Philadelphia: Elsevier Inc, 2011: 1436-1459