Extrahepatic manifestations of HCV infection: Facts and controversies

Journal of Hepatology

Volumn 31, Issue 2, 1999, Pages 369-376

  Zignego, Anna Linda ^a   Bréchot, Christian ^b  

^a UNIVERSITY OF FLORENCE   (Italy)

^b HÔPITAL NECKER ENFANTS MALADES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT ALPHA INTERFERON; VIRUS RNA;

CHRONIC HEPATITIS; CRYOGLOBULINEMIA; HASHIMOTO DISEASE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; LICHEN PLANUS; LUNG FIBROSIS; LYMPHOPROLIFERATIVE DISEASE; NONHODGKIN LYMPHOMA; PRIORITY JOURNAL; REVIEW; SJOEGREN SYNDROME; VIRUS HEPATITIS;

EID: 0345593806     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-8278(99)80239-6     Document Type: Review

References (99)

1. Lunel F, Musset L. Hepatitis C virus infection and cryoglobulinemia. J Hepatol. 29:1998;848-855.
2. Ferri C, Greco F, Longombardo G, Palla P, Moretti A, Marzo E, et al. Antibodies against hepatitis C virus in mixed cryoglobulinemia patients. Infection. 19:1991;417-420.
3. Agnello V, Chung RT, Kaplan LM. A role for hepatitis C virus infection in type II cryoglobulinemia. N Engl J Med. 327:1992;1490-1495.
4. Misiani R, Bellavita P, Fenili D, Borelli G, Marchesi D, Massazza M, et al. Hepatitis C virus infection in patients with essential mixed cryoglobulinemia. Ann Intern Med. 117:1992;573-577.
5. Ferri C, Marzo E, Longombardo G, Lombardini F, La Civita L, Vanacore R, et al. Interferon-alpha in mixed cryoglobulinemia patients: a randomized, crossover-controlled trial. Blood. 81:1993;1132-1136.
6. Marcellin P, Descamps V, Martinot-Peignoux M, Larzul D, Xu L, Boyer N, et al. Cryoglobulinemia with vasculitis associated with hepatitis C virus infection. Gastroenterology. 104:1993;272-277.
7. Cacoub P, Fabiani FL, Musset L, Perrin M, Frangeul L, Leger JM, et al. Mixed cryoglobulinemia and hepatitis C virus. Am J Med. 96:1994;124-132.
8. Zignego AL, Ferri C, Giannini C, La Civita L, Careccia G, Longombardo G, et al. Analysis of HCV infection in mixed cryoglobulinemia and B-cell non-Hodgkin's lymphoma: evidence for a pathogenetic role. Arch Virol. 142:1997;545-555.
9. Ferri C, Monti M, La Civita L, Longombardo G, Greco F, Pasero G, et al. Infection of peripheral blood mononuclear cells by hepatitis C virus in mixed cryoglobulinemia. Blood. 82:1993;3701-3704.
10. Pawlotsky JM, Roudot-Thoraval F, Simmonds P, Mellor J, Ben Yahia MB, Andre C, et al. Extrahepatic immunologic manifestations in chronic hepatitis C and hepatitis C virus serotypes. Ann Intern Med. 122:1995;169-173.
11. Zignego AL, Ferri C, Giannini C, Monti M, La Civita L, Careccia G, et al. Hepatitis C virus genotype analysis in patients with type II mixed cryoglobulinemia. Ann Intern Med. 124:1996;31-34.
12. Gournay J, Ferrell LD, Roberts JP, Ascher NL, Wright TL, Lake JR. Cryoglobulinemia presenting after liver transplantation. Gastroenterology. 110:1996;265-270.
13. Pozzato G, Mazzaro C, Crovatto M, Modolo ML, Ceselli S, Mazzi G, et al. Low-grade malignant lymphoma, hepatitis C virus infection, and mixed cryoglobulinemia. Blood. 84:1994;3047-3053.
14. Monteverde A, Ballare M, Pileri S. Hepatic lymphoid aggregates in chronic hepatitis C and mixed cryoglobulinemia. Springer Semin Immunopathol. 19:1997;99-110.
15. Zehender G, De Maddalena C, Monti G, Ballare M, Saccardo F, Piconi S, et al. HCV genotypes in bone marrow and peripheral blood mononuclear cells of patients with mixed cryoglobulinemia. Clin Exp Rheumatol. 13S:1995;S87-S90.
16. Cerino A, Silini E, Brambilla S, Asti M, Bellati G, Lisa A, et al. Serological response to HCV hypervariable region 1 are mainly cross-reactive and genotype-dependent. J Hepatol. 26S1:1997;62.
17. Missale G, Cariani E, Lamonaca V, Ravaggi A, Rossini A, Bertoni R, et al. Effects of interferon treatment on the antiviral T-cell response in hepatitis C virus genotype 1b- and genotype 2c-infected patients. Hepatology. 26:1997;792-797.
18. Silvestri F, Barillari G, Fanin R, Pipan C, Falasca E, Salmaso F, et al. The genotype of the hepatitis C virus in patients with HCV-related B cell non-Hodgkin's lymphoma. Leukemia. 11:1997;2157-2161.
19. Andreone P, Zignego AL, Cursaro C, Gramenzi A, Gherlinzoni F, Fiorino S, et al. Prevalence of monoclonal gammopathies in patients with hepatitis C virus infection. Ann Intern Med. 129:1998;294-298.
20. Misiani R, Bellavita P, Fenili D, Vicari O, Marchesi D, Sironi PL, et al. Interferon alfa-2a therapy in cryoglobulinemia associated with hepatitis C virus. N Engl J Med. 330:1994;751-756.
21. Ferri C, Monti M, La Civita L, Careccia G, Mazzaro C, Longombardo G, et al. Hepatitis C virus infection in non-Hodgkin's B-cell lymphoma complicating mixed cryoglobulinaemia. Eur J Clin Invest. 24:1994;781-784.
22. La Civita L, Zignego AL, Monti M, Longombardo G, Pasero G, Ferri C. Mixed cryoglobulinemia as a possible preneoplastic disorder. Arthritis Rheum. 38:1995;1859-1860.
23. Franzin F, Efremov DG, Pozzato G, Tulissi P, Batista F, Burrone OR. Clonal B-cell expansions in peripheral blood of HCV-infected patients. Br J Haematol. 90:1995;548-552.
24. Zignego AL, Ferri C, Giannini C, La Civita L, Careccia G, Longombardo G, et al. Hepatitis C virus infection in mixed cryoglobulinemia and B-cell non-Hodgkin's lymphoma: evidence for a pathogenetic role. Arch Virol. 142:1997;545-555.
25. Izumi T, Sasaki R, Tsunoda S, Akutsu M, Okamoto H, Miura Y. B cell malignancy and hepatitis C virus infection. Leukemia. S3:1997;516-518.
26. Satoh T, Yamada T, Nakano S, Tokunaga O, Kuramochi S, Kanai T, et al. The relationship between primary splenic malignant lymphoma and chronic liver disease associated with hepatitis C virus infection. Cancer. 80:1997;1981-1988.
27. Sikuler E, Shnaider A, Zilberman D, Hilzenrat N, Shemer-Avni Y, Neumann L, et al. Hepatitis C virus infection and extrahepatic malignancies. J Clin Gastroenterol. 24:1997;87-89.
28. Zuckerman E, Zuckerman T, Levine AM, Douer D, Gutekunst K, Mizokami M, et al. Hepatitis C virus infection in patients with B-cell non-Hodgkin lymphoma. Ann Intern Med. 127:1997;423-428.
29. Ferri C, La Civita L, Monti M, Longombardo G, Pasero G, Zignego AL. Can type C hepatitis infection be complicated by malignant lymphoma? Lancet. 346:1995;1426-1427.
30. Ferri C, Caracciolo F, Zignego AL, La Civita L, Monti M, Longombardo G, et al. Hepatitis C virus infection in patients with non-Hodgkin's lymphoma. Br J Haematol. 88:1994;392-394.
31. Ferri C, Caracciolo F, La Civita L, Monti M, Longombardo G, Zignego AL. Hepatitis C virus infection and B-cell lymphomas. Eur J Cancer. 30A:1994;1591-1592.
32. Zignego AL, Ferri C, Innocenti F, Giannini C, Monti M, Bellesi G, et al. Lack of preferential localization of tumoral mass in B-cell non-Hodgkin's lymphoma associated with hepatitis C virus infection. Blood. 89:1997;3066-3068.
33. Luppi M, Grazia Ferrari M, Bonaccorsi G, Longo G, Narni F, Barozzi P, et al. Hepatitis C virus infection in subsets of neoplastic lymphoproliferations not associated with cryoglobulinemia. Leukemia. 10:1996;351-355.
34. Silvestri F, Pipan C, Barillari G, Zaja F, Fanin R, Infanti L, et al. Prevalence of hepatitis C virus infection in patients with lymphoproliferative disorders. Blood. 87:1996;4296-4301.
35. De Vita S, Sacco C, Sansonno D, Gloghini A, Dammacco F, Crovatto M, et al. Characterization of overt B-cell lymphomas in patients with hepatitis C virus infection. Blood. 90:1997;776-782.
36. Ferri C, La Civita L, Caracciolo F, Bellesi G, Zignego AL. Hepatitis C virus and lymphoproliferative disorders. Blood. 88:1997;4730.
37. De Rosa G, Gobbo ML, De Renzo A, Notaro R, Garofalo S, Grimaldi M, et al. High prevalence of hepatitis C virus infection in patients with B-cell lymphoproliferative disorders in Italy. Am J Hematol. 55:1997;77-82.
38. Brind AM, Watson JP, Burt A, Kestevan P, Wallis J, Proctor SJ, et al. Non-Hodgkin's lymphoma and hepatitis C virus infection. Leuk Lymphoma. 21:1996;127-130.
39. McColl MD, Singer IO, Tait RC, McNeil IR, Cumming RL, Hogg RB. The role of hepatitis C virus in the aetiology of non-Hodgkins lymphoma - a regional association? Leuk Lymphoma. 26:1997;127-130.
40. La Civita L, Zignego AL, Monti M, Longombardo G, Greco F, Pasero G, et al. Type C hepatitis and chronic lymphocytic leukaemia. Type C hepatitis and chronic lymphocytic leukaemia. Eur J Cancer. 32A:1996;1819-1820.
41. Moazami G, Auran JD, Florakis GJ, Wilson SE, Srinivasan DB. Interferon treatment of Mooren's ulcers associated with hepatitis C. Am J Ophthalmol. 119:1995;365-366.
42. Wong S, Mehta AE, Faiman C, Berard L, Ibbott T, Minuk GY. Absence of serologic evidence for hepatitis C virus infection in patients with Hashimoto's thyroiditis. Hepatogastroenterology. 43:1996;420-421.
43. Boadas J, Rodriguez-Espinosa J, Enríquez J, Miralles F, Martinez-Cerezo FJ, González P, et al. Prevalence of thyroid autoantibodies is not increased in blood donors with hepatitis C virus infection. J Hepatol. 22:1995;611-615.
44. Roti E, Minelli R, Giuberti T, Marchelli S, Schianchi C, Gardini E, et al. Multiple changes in thyroid function in patients with chronic active HCV hepatitis treated with recombinant interferon-alpha. Am J Med. 101:1996;482-487.
45. Aceti A, Taliani G, Sorice M, Amendolea MA. HCV and Sjögren's syndrome. Lancet. 339:1992;1425-1426.
46. Haddad J, Deny P, Munz-Gotheil C, Ambrosini JC, Trinchet JC, Pateron D, et al. Lymphocytic sialadenitis of Sjögren's syndrome associated with chronic hepatitis C virus liver disease. Lancet. 339:1992;321-323.
47. Pirisi M, Scott C, Fabris C, Ferraccioli G, Soardo G, Ricci R, et al. Mild sialoadenitis: a common finding in patients with hepatitis C virus infection. Scand J Gastroenterol. 29:1994;940-942.
48. Coll J, Gambus G, Corominas J, Tomas S, Esteban JI, Guardia J. Immunohistochemistry of minor salivary gland biopsy specimens from patients with Sjögren's syndrome with and without hepatitis C virus infection. Ann Rheum Dis. 56:1997;390-392.
49. Scott CA, Avellini C, Desinan L, Pirisi M, Ferraccioli GF, Bardus P, et al. Chronic lymphocytic sialoadenitis in HCV-related chronic liver disease: comparison of Sjögren's syndrome. Histopathology. 30:1997;41-48.
50. Koike K, Moriya K, Ishibashi K, Yotsuyanagi H, Shintani Y, Fujie H, et al. Sialadenitis histologically resembling Sjögren syndrome in mice transgenic for hepatitis C virus envelope genes. Proc Natl Acad Sci USA. 94:1997;233-236.
51. Tzioufas AG, Manoussakis MN, Costello R, Silis M, Papadopoulos NM, Moutsopoulos HM. Cryoglobulinemia in autoimmune rheumatic diseases. Evidence of circulating monoclonal cryoglobulins in patients with primary Sjögren's syndrome. Arthritis Rheum. 29:1986;1098-1104.
52. Luppi M, Grazia Ferrari M, Bonaccorsi G, Longo G, Narni F, Barozzi P, et al. Hepatitis C virus infection in subsets of neoplastic lymphoproliferations not associated with cryoglobulinemia. Leukemia. 10:1996;351-355.
53. Ueda N, Shah SV. Apoptosis. J Lab Clin Med. 124:1994;169-177.
54. Ohta K, Ueda T, Nagai S, Yamada K, Yamaguchi M, Nakano J, et al. Pathogenesis of idiopathic pulmonary fibrosis: is hepatitis C virus involved? Nippon Kyobu Shikkan Gakkai Zasshi. 31S:1993;32-35.
55. Yamaguchi S, Kubo K, Fujimoto K, Honda T, Sekiguchi M, Sodeyama T. Analysis of bronchoalveolar lavage fluid in patients with chronic hepatitis C before and after treatment with interferon alpha. Thorax. 52:1997;33-37.
56. Irving WL, Day S, Johnston ID. Idiopathic pulmonary fibrosis and hepatitis C virus infection. Am Rev Respir Dis. 148:1993;1683-1684.
57. Ferri C, La Civita L, Fazzi P, Solfanelli S, Lombardini F, Begliomini E, et al. Interstitial lung fibrosis and rheumatic disorders in patients with hepatitis C virus infection. Br J Rheumatol. 36:1997;360-365.
58. Piperno A, D'Alba R, Roffi L, Pozzi M, Farina A, Vecchi L, et al. Hepatitis C virus infection in patients with idiopathic hemochromatosis (IH) and porphyria cutanea tarda (PCT). Arch Virol Suppl. 4:1992;215-216.
59. Fargion S, Piperno A, Cappellini MD, Sampietro M, Fracanzani AL, Romano R, et al. Hepatitis C virus and porphyria cutanea tarda: evidence of a strong association. Hepatology. 16:1992;1322-1326.
60. Ferri C, Baicchi U, la Civita L, Greco F, Longombardo G, Mazzoni A, et al. Hepatitis C virus-related autoimmunity in patients with porphyria cutanea tarda. Eur J Clin Invest. 23:1993;851-855.
61. Navas S, Bosch O, Castillo I, Marriott E, Carreno V. Porphyria cutanea tarda and hepatitis C and B viruses infection: a retrospective study. Hepatology. 21:1995;279-284.
62. Hussain I, Hepburn NC, Jones A, O'Rourke K, Hayes PC. The association of hepatitis C viral infection with porphyria cutanea tarda in the Lothian region of Scotland. Clin Exp Dermatol. 21:1996;283-285.
63. O'Reilly FM, Darby C, Fogarty J, O'Moore R, Courtney MG, O'Connor J, et al. Porphyrin metabolism in hepatitis C infection. Photodermatol Photoimmunol Photomed. 12:1996;31-33.
64. Ferri C, Baicchi U, la Civita L, Greco F, Longombardo G, Mazzoni A, et al. Hepatitis C virus-related autoimmunity in patients with porphyria cutanea tarda. Eur J Clin Invest. 23:1993;851-855.
65. Nagao Y, Sata M, Tanikawa K, Itoh K, Kameyama T. Lichen planus and hepatitis C virus in the northern Kyushu region of Japan. Eur J Clin Invest. 25:1995;910-914.
66. Tanei R, Watanabe K, Nishiyama S. Clinical and histopathologic analysis of the relationship between lichen planus and chronic hepatitis C. J Dermatol. 22:1995;316-323.
67. Carrozzo M, Gandolfo S, Carbone M, Colombatto P, Broccoletti R, Garzino-Demo P, et al. Hepatitis C virus infection in Italian patients with oral lichen planus: a prospective case-control study. J Oral Pathol Med. 25:1996;527-533.
68. Nagao Y, Sata M, Ide T, Suzuki H, Tanikawa K, Itoh K, et al. Development and exacerbation of oral lichen planus during and after interferon therapy for hepatitis C. Eur J Clin Invest. 26:1996;1171-1174.
69. De Vita S, Sansonno D, Dolcetti R, Ferraccioli G, Carbone A, Cornacchiulo V, et al. Hepatitis C virus within a malignant lymphoma lesion in the course of type II mixed cryoglobulinemia. Blood. 86:1995;1887-1892.
70. Zignego AL, Macchia D, Monti M, Thiers V, Mazzetti M, Foschi M, et al. Infection of peripheral mononuclear blood cells by hepatitis C virus. J Hepatol. 15:1992;382-386.
71. Muller HM, Pfaff E, Goeser T, Kallinowski B, Solbach C, Theilmann L. Peripheral blood leukocytes serve as a possible extrahepatic site for hepatitis C virus replication. J Gen Virol. 74:1993;669-676.
72. Willems M, Sheng L, Roskams T, Ramdani B, Doutrelepont JM, Nevens F, et al. Hepatitis C virus and its genotypes in patients suffering from chronic hepatitis C with or without a cryoglobulinemia-related syndrome. J Med Virol. 44:1994;266-271.
73. Zignego AL, De Carli M, Monti M, Careccia G, La Villa G, Giannini C, et al. Hepatitis C virus infection of mononuclear cells from peripheral blood and liver infiltrates in chronically infected patients. J Med Virol. 47:1995;58-64.
74. Moldvay J, Deny P, Pol S, Brechot C, Lamas E. Detection of hepatitis C virus RNA in peripheral blood mononuclear cells of infected patients by in situ hybridization. Blood. 83:1994;269-273.
75. Cribier B, Schmitt C, Bingen A, Kirn A, Keller F. In vitro infection of peripheral blood mononuclear cells by hepatitis C virus. J Gen Virol. 76:1995;2485-2491.
76. Bronowicki JP, Loriot MA, Thiers V, Grignon Y, Zignego AL, Brechot C. Hepatitis C virus persistence in human hematopoietic cells injected into SCID mice. Hepatology. 28:1998;211-218.
77. Lerat H, Rumin S, Habersetzer F, Berby F, Trabaud MA, Trepo C, et al. In vivo tropism of hepatitis C virus genomic sequences in hematopoietic cells: influence of viral load, viral genotype, and cell phenotype. Blood. 91:1998;3841-3849.
78. Shimizu YK, Igarashi H, Kanematu T, Fujiwara K, Wong DC, Purcell RH, et al. Sequence analysis of the hepatitis C virus genome recovered from serum, liver, and peripheral blood mononuclear cells of infected chimpanzees. J Virol. 71:1997;5769-5773.
79. Kato N, Ikeda M, Sugiyama K, Mizutani T, Tanaka T, Shimotohno K. Hepatitis C virus population dynamics in human lymphocytes and hepatocytes infected in vitro. J Gen Virol. 79:1998;1859-1869.
80. Fujii K, Hino K, Okazaki M, Okuda M, Kondoh S, Okita K. Differences in hypervariable region 1 quasispecies of hepatitis C virus between human serum and peripheral blood mononuclear cells. Biochem Biophys Res Commun. 225:1996;771-776.
81. Saito H, Tsuchimoto K, Miyaguchi S, Tada S, Sawaguchi K, Komatsu K, et al. Multicenter trial in high-dose interferon-alpha 2b treatment for chronic hepatitis C. Keio Interferon-alpha 2b Study Group. J Med. 45:1996;161-167.
82. Maggi F, Fornai C, Vatteroni ML, Giorgi M, Morrica A, Pistello M, et al. Differences in hepatitis C virus quasispecies composition between liver, peripheral blood mononuclear cells and plasma. J Gen Virol. 78:1997;1521-1525.
83. Zignego AL, Ferri C, Monti M, LaCivita L, Giannini C, Careccia G, et al. Hepatitis C virus as a lymphotropic agent: evidence and pathogenetic implications. Clin Exp Rheumatol. 13S:1995;33-37.
84. Lenzi M, Frisoni M, Mantovani V, Ricci P, Muratori L, Francesconi R, et al. Haplotype HLA-B8-DR3 confers susceptibility to hepatitis C virus-related mixed cryoglobulinemia. Blood. 91:1998;2062-2066.
85. Mecchia M, Casato M, Tafi R, Filocamo G, Bonomo L, Fiorilli M, et al. Nonrheumatoid IgM in human hepatitis C virus-associated type II cryoglobulinemia recognize mimotopes of the CD4-like LAG-3 protein. J Immunol. 157:1996;3727-3736.
86. Lohr HF, Goergen B, Meyer zum Büschenfelde KH, Gerken G. HCV replication in mononuclear cells stimulates anti-HCV-secreting B cells and reflects nonresponsiveness to interferon-alpha. J Med Virol. 46:1995;314-320.
87. Ferri C, Lo Jacono L, Monti M, Caracciolo F, La Civita L, Barsanti LA, et al. Lymphotropic virus infection of peripheral blood mononuclear cells in B-cell non-Hodgkin's lymphoma. Acta Haematol. 98:1997;89-94.
88. Zignego AL, Giannini C, Bellesi G, Gentilini P, Hadzyiannis S, Ferri C. May HGV infection be implicated in lymphomagenesis? Br J Haematol. 98:1997;778-779.
89. Ellis M, Rathaus M, Amiel A, Manor Y, Klein A, Lishner M. Monoclonal lymphocyte proliferation and bcl-2 rearrangement in essential mixed cryoglobulinaemia. Eur J Clin Invest. 25:1995;833-837.
90. Jaeger U, Karth GD, Knapp S, Friedl J, Laczika K, Kusec R. Molecular mechanism of the t(14; 18) - a model for lymphoidspecific chromosomal translocations. Leuk Lymphoma. 14:1994;197-202.
91. Ueda N. Shah SV Apoptosis. J Lab Clin Med. 124:1994;169-177.
92. Poetsch M, Weber-Matthiesen K, Plendl HJ, Grote W, Schlegelberger B. Detection of the t(14;18) chromosomal translocation by interphase cytogenetics with yeast-artificial-chromosome probes in follicular lymphoma and nonneoplastic lymphoproliferation. J Clin Oncol. 14:1996;963-969.
93. Zignego AL, Giannelli F, Marrocchi ME, Giannini C, Gentilini P, Ferri C. Frequency of bcl-2 rearrangement in patients with mixed cryoglobulinemia and HCV-positive liver diseases. Clin Exp Rheumatol. 15:1997;711-712.
94. McDonnell TJ, Korsmeyer SJ. Progression from lymphoid hyperplasia to high-grade malignant lymphoma in mice transgenic for the t(14; 18). Nature. 349:1991;254-256.
95. Ray RB, Lagging LM, Meyer K, Steele R, Ray R. Transcriptional regulation of cellular and viral promoters by the hepatitis C virus core protein. Virus Res. 37:1995;209-220.
96. Ray RB, Meyer K, Ray R. Suppression of apoptotic cells death by hepatitis C virus core protein. Virology. 226:1996;176-182.
97. Fanidi A, Harrington EA, Evan GI. Cooperative interaction between c-myc and bcl-2 proto-oncogenes. Nature. 359:1992;554-556.
98. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F, Petracca R, Weiner AJ, Houghton M, Rosa D, Grandi G, Abrignani S. Binding of hepatitis C virus to CD81. Science. 282:1998;938-941.
99. Agnello V. The etiology and pathophysiology of mixed cryoglobulinemia secondary to hepatitis C virus infection. Springer Semin Immunopathol. 19:1997;111-129.