Environmental triggers of thyroiditis: Hepatitis C and interferon-α

Journal of Endocrinological Investigation

Volumn 34, Issue 1, 2011, Pages 78-84

  Menconi, F ^a   Hasham, A ^a   Tomer, Y ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Autoimmunity; Hepatitis C; Infection; Interferon; Thyroiditis

Indexed keywords

ALPHA INTERFERON; IODINE;

CLINICAL FEATURE; ENVIRONMENTAL FACTOR; GENETIC PREDISPOSITION; GRAVES DISEASE; HASHIMOTO DISEASE; HEPATITIS C; HUMAN; INFECTION; PATHOGENESIS; REVIEW; THYROID FUNCTION; THYROIDITIS;

EID: 79955459180     PISSN: 03914097     EISSN: 17208386     Source Type: Journal    
DOI: 10.1007/bf03346699     Document Type: Review

References (79)

1. Huber A, Menconi F, Corathers S, Jacobson EM, Tomer Y. Joint genetic susceptibility to type 1 diabetes and autoimmune thyroiditis: from epidemiology to mechanisms. Endocr Rev 2008, 29: 697-725.
2. Brix TH, Kyvik KO, Christensen K, Hegedus L. Evidence for a major role of heredity in Graves' disease: a population- based study of two Danish twin cohorts. J Clin Endocrinol Metab 2001, 86: 930-4. (Pubitemid 32207518)
3. Rose NR, Bonita R, Burek CL. Iodine: an environmental trigger of thyroiditis. Autoimmun Rev 2002, 1: 97-103.
4. Li HS, Jiang HY, Carayanniotis G. Modifying effects of iodine on the immunogenicity of thyroglobulin peptides. J Autoimmun 2007, 28: 171-6. (Pubitemid 46754763)
5. Oppenheim Y, Ban Y, Tomer Y. Interferon induced Autoimmune Thyroid Disease (AITD): a model for human autoimmunity. Autoimmun Rev 2004, 3: 388-93. (Pubitemid 38993361)
6. Tomer Y, Davies TF. Infections and autoimmune endocrine disease. Baillieres Clin Endocrinol Metab 1995, 9: 47-70.
7. Tomer Y, Huber A. The etiology of autoimmune thyroid disease: a story of genes and environment. J Autoimmun 2009, 32: 231-9.
8. Tomer Y, Blackard JT, Akeno N. Interferon alpha treatment and thyroid dysfunction. Endocrinol Metab Clin North Am 2007, 36: 1051-66. (Pubitemid 350026253)
9. Burek CL, Talor MV. Environmental triggers of autoimmune thyroiditis. J Autoimmun 2009, 33: 183-9.
10. Bahn AK, Mills JL, Snyder PJ, et al. Hypothyroidism in workers exposed to polybrominated biphenyls. N Engl J Med 1980, 302: 31-3. (Pubitemid 10212233)
11. Desailloud R, Hober D. Viruses and thyroiditis: an update. Virol J 2009, 6: 5.
12. Deutsch M, Dourakis S, Manesis EK, et al. Thyroid abnormalities in chronic viral hepatitis and their relationship to interferon alfa therapy. Hepatology 1997, 26: 206-10. (Pubitemid 27280326)
13. Tomer Y, Davies TF. Searching for the autoimmune thyroid disease susceptibility genes: From gene mapping to gene function. Endocr Rev 2003, 24: 694-717. (Pubitemid 37330587)
14. Mandac JC, Chaudhry S, Sherman KE, Tomer Y. The clinical and physiological spectrum of interferon-alpha induced thyroiditis: toward a new classification. Hepatology 2006, 43: 661-672.
15. Dalgard O, Bjoro K, Hellum K, et al. Thyroid dysfunction during treatment of chronic hepatitis C with interferon alpha: no association with either interferon dosage or efficacy of therapy. J Intern Med 2002, 251: 400-6. (Pubitemid 34534115)
16. Prummel MF, Laurberg P. Interferon-alpha and autoimmune thyroid disease. Thyroid 2003, 13: 547-51. (Pubitemid 36842660)
17. Grossman CJ, Roselle GA, Mendenhall CL. Sex steroid regulation of autoimmunity. J Steroid Biochem Mol Biol 1991, 40: 649-59.
18. Tomer Y, Menconi F, Davies TF, et al. Dissecting genetic heterogeneity in autoimmune thyroid diseases by subset analysis. J Autoimmun 2007, 29: 69-77. (Pubitemid 47385112)
19. Ban Y, Tozaki T, Tobe T, et al. The regulatory T cell gene FOXP3 and genetic susceptibility to thyroid autoimmunity: An association analysis in Caucasian and Japanese cohorts. J Autoimmun 2007, 28: 201-7. (Pubitemid 46805032)
20. Ban Y, Greenberg DA, Davies TF, Jacobson E, Concepcion E, Tomer Y. Linkage analysis of thyroid antibody production: evidence for shared susceptibility to clinical autoimmune thyroid disease. J Clin Endocrinol Metab 2008, 93: 3589-96.
21. Vanderpump MP, Tunbridge WM, French JM, et al. The incidence of thyroid disorders in the community: a twenty-year follow-up of the Whickham Survey. Clin Endocrinol (Oxf) 1995. 43: 55-68.
22. Roti E, Minelli R, Giuberti T, et al. Multiple changes in thyroid function in patients with chronic active HCV hepatitis treated with recombinant interferon-alpha. Am J Med 1996, 101: 482-7. (Pubitemid 126335968)
23. Oppenheim Y, Kim G, Ban Y, et al. The effects of alpha interferon on the development of autoimmune thyroiditis in the NOD H2h4 mouse. Clin Dev Immunol 2003, 10: 161-5. (Pubitemid 38089407)
24. Jacobson EM, Huber A, Tomer Y. The HLA gene complex in thyroid autoimmunity: From epidemiology to etiology. J Autoimmun 2008, 30: 58-62.
25. Jacobson EM, Tomer Y. The CD40, CTLA-4, thyroglobulin, TSH receptor, and PTPN22 gene quintet and its contribution to thyroid autoimmunity: Back to the future. J Autoimmun 2007, 28: 85-98. (Pubitemid 46670687)
26. Kakizaki S, Takagi H, Murakami M, Takayama H, Mori M. HLA antigens in patients with interferon-alpha-induced autoimmune thyroid disorders in chronic hepatitis C. J Hepatol 1999, 30: 794-800. (Pubitemid 29248978)
27. Kryczka W, Brojer E, Kowalska A, Zarebska-Michaluk D. Thyroid gland dysfunctions during antiviral therapy of chronic hepatitis C. Med Sci Monit 2001, 7 (Suppl 1): 221-5.
28. Jacobson EM, Chaudhry S, Mandac JC, Concepcion E, Tomer Y. Immune-regulatory gene involvement in the etiology of interferon induced thyroiditis (IIT). Thyroid 2006, 16: 926 (Meeting Abstract).
29. Tomer Y, Villanueva R. Hepatitis C and thyroid autoimmunity: is there a link? Am J Med 2004, 117: 60-1.
30. Antonelli A, Ferri C, Pampana A, et al. Thyroid disorders in chronic hepatitis C. Am J Med 2004, 117: 10-3.
31. Huang MJ, Tsai SL, Huang BY, Sheen IS, Yeh CT, Liaw YF. Prevalence and significance of thyroid autoantibodies in patients with chronic hepatitis C virus infection: a prospective controlled study. Clin Endocrinol (Oxf) 1999, 50: 503-9.
32. Floreani A, Betterle C, Carderi I, Presotto F, Pedini B, Moscon A et al. Is hepatitis C virus a risk factor for thyroid autoimmunity? J Viral Hepat 2006, 13: 272-7.
33. Ganne-Carrie N, Medini A, Coderc E, et al. Latent autoimmune thyroiditis in untreated patients with HCV chronic hepatitis: a case-control study. J Autoimmun 2000, 14: 189-93. (Pubitemid 30662578)
34. Andrade LJ, Atta AM, D'Almeida Junior A, Paraná R. Thyroid dysfunction in hepatitis C individuals treated with interferon-alpha and ribavirin - a review. Braz J Infect Dis 2008, 12: 144-8.
35. Ward DL, Bing-You RG. Autoimmune thyroid dysfunction induced by interferon-alpha treatment for chronic hepatitis C: screening and monitoring recommendations. Endocr Pract 2001, 7: 52-8. (Pubitemid 32834247)
36. Antonelli A, Ferri C, Fallahi P, et al. Thyroid disorders in chronic hepatitis C virus infection. Thyroid 2006, 16: 563-72. (Pubitemid 44066263)
37. Hsieh MC, Yu ML, Chuang WL, et al. Virologic factors related to interferon-alpha-induced thyroid dysfunction in patients with chronic hepatitis C. Eur J Endocrinol 2000, 142: 431-7.
38. Bartolome J, Rodriguez-Inigo E, Quadras P, et al. Detection of hepatitis C virus in thyroid tissue from patients with chronic HCV infection. J Med Virol 2008, 80: 1588-94.
39. Akeno N, Blackard JT, Tomer Y. HCV E2 protein binds directly to thyroid cells and induces IL-8 production: a new mechanism for HCV induced thyroid autoimmunity. J Autoimmun 2008, 31: 339-44.
40. Tomer Y, Menconi F. Interferon induced thyroiditis. Best Pract Res Clin Endocrinol Metab 2009, 23: 703-12.
41. Pfeffer LM, Dinarello CA, Herberman RB, et al. Biological properties of recombinant alpha-interferons: 40th anniversary of the discovery of interferons. Cancer Res 1998, 58: 2489-99. (Pubitemid 28275413)
42. Fried MW, Shiffman ML, Reddy KR, et al. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 2002, 347: 975-82.
43. Russo MW, Fried MW. Side effects of therapy for chronic hepatitis C. Gastroenterology 2003, 124: 1711-9. (Pubitemid 36617688)
44. Negro F. Adverse effects of drugs in the treatment of viral hepatitis. Best Pract Res Clin Gastroenterol 2010, 24: 183-92.
45. Caraccio N, Giannini R, Cuccato S, Faviana P, Berti P, Galleri D et al. Type I interferons modulate the expression of thyroid peroxidase, sodium/iodide symporter, and thyroglobulin genes in primary human thyrocyte cultures. J Clin Endocrinol Metab 2005, 90: 1156-62. (Pubitemid 40279248)
46. Caraccio N, Cuccato S, Pratesi F, Dardano A, Ursino S, Chimenti D et al. Effect of type I interferon(s) on cell viability and apoptosis in primary human thyrocyte cultures. Thyroid 2009, 19: 149-55.
47. Chung RT, Gale M Jr, Polyak SJ, Lemon SM, Liang TJ, Hoofnagle JH. Mechanisms of action of interferon and ribavirin in chronic hepatitis C: Summary of a workshop. Hepatology 2008, 47: 306-20. (Pubitemid 351171068)
48. Feld JJ, Hoofnagle JH. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 2005, 436: 967-72. (Pubitemid 41191673)
49. Corssmit EP, de Metz J, Sauerwein HP, Romijn JA. Biologic responses to IFN-alpha administration in humans. J Interferon Cytokine Res 2000, 20: 1039-47. (Pubitemid 32015242)
50. You X, Teng W, Shan Z. Expression of ICAM-1, B7.1 and TPO on human thyrocytes induced by IFN-alpha. Chin Med J (Engl) 1999, 112: 61-6.
51. Ajjan RA, Watson PF, McIntosh RS, Weetman AP. Intrathyroidal cytokine gene expression in Hashimoto's thyroiditis. Clin Exp Immunol 1996, 105: 523-8. (Pubitemid 26297900)
52. Todd I, Pujol-Borrell R, Hammond LJ, Bottazzo GF, Feldmann M. Interferon-gamma induces HLA-DR expression by thyroid epithelium. Clin Exp Immunol 1985, 61: 265-73. (Pubitemid 15247751)
53. Farrar JD, Murphy KM. Type I interferons and T helper development. Immunol Today 2000, 21: 484-9.
54. Cerella C, Amato G, Biondi B, et al. Longitudinal study of antibodies against thyroid in patients undergoing interferon-alpha therapy for HCV chronic hepatitis. Horm Res 1995, 44: 110-4.
55. Land KJ, Moll JS, Kaplan MH, Seetharamaiah GS. Signal transducer and activator of transcription (Stat)-6-dependent, but not Stat4-dependent, immunity is required for the development of autoimmunity in Graves' hyperthyroidism. Endocrinology 2004, 145: 3724-30. (Pubitemid 39037558)
56. Mazziotti G, Sorvillo F, Piscopo M, et al. Innate and acquired immune system in patients developing interferon-alpha-related autoimmune thyroiditis: a prospective study. J Clin Endocrinol Metab 2005, 90: 4138-44. (Pubitemid 41058188)
57. Nagayama Y, Mizuguchi H, Hayakawa T, Niwa M, McLachlan SM, Rapoport B. Prevention of autoantibody-mediated Graves'-like hyperthyroidism in mice with IL-4, a Th2 cytokine. J Immunol 2003, 170: 3522-7. (Pubitemid 36359218)
58. Corssmit EP, Heijligenberg R, Hack CE, Endert E, Sauerwein HP, Romijn JA. Effects of interferon-alpha (IFN-alpha) administration on leucocytes in healthy humans. Clin Exp Immunol 1997, 107: 359-63. (Pubitemid 27049265)
59. Krause I, Valesini G, Scrivo R, Shoenfeld Y. Autoimmune aspects of cytokine and anticytokine therapies. Am J Med 2003, 115: 390-7. (Pubitemid 37311257)
60. Lindahl P, Leary P, Gresser I. Enhancement by interferon of the expression of surface antigens on murine leukemia L 1210 cells. Proc Natl Acad Sci U S A 1973, 70: 2785-8.
61. th Meeting of the Endocrine Society, Toronto, Canada, June 2007.
62. Fentiman IS, Thomas BS, Balkwill FR, Rubens RD, Hayward JL. Primary hypothyroidism associated with interferon therapy of breast cancer. Lancet 1985, 1: 1166. (Pubitemid 15080733)
63. Hollowell JG, Staehling NW, Flanders WD, et al. Serum TSH, T(4), and thyroid antibodies in the United States population (1988 to 1994): National Health and Nutrition Examination Survey (NHANES III). J Clin Endocrinol Metab 2002, 87: 489-99.
64. Imagawa A, Itoh N, Hanafusa T, et al. Autoimmune endocrine disease induced by recombinant interferon-alpha therapy for chronic active type C hepatitis. J Clin Endocrinol Metab 1995, 80: 922-6.
65. Watanabe U, Hashimoto E, Hisamitsu T, Obata H, Hayashi N. The risk factor for development of thyroid disease during interferon-alpha therapy for chronic hepatitis C. Am J Gastroenterol 1994, 89: 399-403. (Pubitemid 24074402)
66. Preziati D, La Rosa L, Covini G, et al. Autoimmunity and thyroid function in patients with chronic active hepatitis treated with recombinant interferon alpha-2a. Eur J Endocrinol 1995, 132: 587-93.
67. Cerella C, Amato G, Biondi B et al. Longitudinal study of antibodies against thyroid in patients undergoing interferon-alpha therapy for HCV chronic hepatitis. Horm Res 1995, 44: 110-4.
68. Marazuela M, Garcia-Buey L, Gonzalez-Fernandez B, et al. Thyroid autoimmune disorders in patients with chronic hepatitis C before and during interferon-alpha therapy. Clin Endocrinol (Oxf) 1996, 44: 635-42. (Pubitemid 26225178)
69. Carella C, Mazziotti G, Morisco F, et al. Long-term outcome of interferon-alpha-induced thyroid autoimmunity and prognostic influence of thyroid autoantibody pattern at the end of treatment. J Clin Endocrinol Metab 2001, 86: 1925-9. (Pubitemid 32472899)
70. Martocchia A, Labbadia G, Paoletti V, et al. Hashimoto's disease during interferon-alpha therapy in a patient with pre-treatment negative anti-thyroid autoantibodies and with the specific genetic susceptibility to the thyroid disease. Neuro Endocrinol Lett 2001, 22: 49-52. (Pubitemid 32186251)
71. Baudin E, Marcellin P, Pouteau M, et al. Reversibility of thyroid dysfunction induced by recombinant alpha interferon in chronic hepatitis C. Clin Endocrinol (Oxf) 1993, 39: 657-61. (Pubitemid 24010954)
72. Koh LK, Greenspan FS, Yeo PP. Interferon-alpha induced thyroid dysfunction: three clinical presentations and a review of the literature. Thyroid 1997, 7: 891-6.
73. Wong V, Fu AX, George J, Cheung NW. Thyrotoxicosis induced by alpha-interferon therapy in chronic viral hepatitis. Clin Endocrinol (Oxf) 2002, 56: 793-8. (Pubitemid 34785912)
74. Lisker-Melman M, Di Bisceglie AM, Usala SJ, Weintraub B, Murray LM, Hoofnagle JH. Development of thyroid disease during therapy of chronic viral hepatitis with interferon alfa. Gastroenterology 1992, 102: 2155-60.
75. Carella C, Mazziotti G, Amato G, Braverman LE, Roti E. Clinical review 169: Interferon-alpha-related thyroid disease: pathophysiological, epidemiological, and clinical aspects. J Clin Endocrinol Metab 2004, 89: 3656-61.
76. Tran HA. The swinging thyroid in hepatitis C infection and interferon therapy QJM 2010, 103: 187-91.
77. Bohbot NL, Young J, Orgiazzi J, et al. Interferon-alpha-induced hyperthyroidism: a three-stage evolution from silent thyroiditis towards Graves' disease. Eur J Endocrinol 2006, 154: 367-72.
78. Antonelli A, Ferri C, Fallahi P. Hepatitis C: thyroid dysfunction in patients with hepatitis C on IFN-alpha therapy. Nat Rev Gastroenterol Hepatol 2009, 6: 633-5.
79. Cadwell K, Patel KK, Maloney NS, et al. Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 2010, 141: 1135-45.