Perspectives in Clinical Nephrology

Kidney International (1994) 46, 1255–1263; doi:10.1038/ki.1994.393

Renal manifestations of hepatitis C virus infection

Richard J Johnson, Richard Willson, Hideaki Yamabe, William Couser, Charles E Alpers, Mark H Wener, Connie Davis and David R Gretch

Seattle, Washington, USA and Hirosaki, Japan

Correspondence: Richard Johnson MD, Division of Nephrology RM-11, University of Washington Medical Center, Seattle, Washington 98195, USA.

Received 4 March 1994; Revised 4 May 1994; Accepted 5 May 1994.

Top

Abstract

The existence of viral hepatitis has been known for centuries. In the 5th century B.C. Hippocrates noted epidemics of a jaundice-like illness. These were particularly common during various military campaigns, and likely represents one of the earliest reports of "infectious hepatitis" due to hepatitis A virus, an illness passed by fecal-oral route as a consequence of poor sanitation. The observation in the late 1800's that hepatitis could develop after smallpox vaccination with human lymph [1] and in the 1940's that hepatitis could be passed by transfusion to volunteers [2] led to the realization that there was a second type of hepatitis (that is, "serum" hepatitis) spread by contaminated blood products. Following the discovery of the "Australia" antigen (hepatitis B surface antigen, HBsAg) by Blumberg, Alter and Visnich in 1964 [3], it was recognized that many of the cases of "serum" hepatitis were due to infection with hepatitis B virus (HBV) [4], and that HBV was also an important cause of chronic active hepatitis and cirrhosis [reviewed in 5]. Unfortunately, by the late 1970s it was apparent that HBV was not the only cause of "serum" hepatitis, and that other "non-A-non-B" hepatitis viruses existed [6], which could be transmitted by blood products to humans and chimpanzees [7]. Using molecular biologic methods, Houghton and colleagues cloned and expressed portions of a RNA virus from the plasma of an infected chimpanzee in 1989 [8, 9]. This virus, designated hepatitis C virus (HCV), is now known to be a major cause of both transfusion-associated and sporadic non-A-non-B hepatitis [10, 11]. Infection with this virus is often persistent, and may result in chronic active hepatitis, cirrhosis or hepatocellular carcinoma [10–12, and reviewed in 13].

The persistent and indolent nature of HCV infection often results in prolonged viremia in spite of a strong humoral immune response [reviewed in 13, 14]. It is perhaps not surprising, then, that chronic immune complex diseases may occur in this setting. The relationship between immune complex disease of the kidney and hepatitis B infection, a long appreciated connection, has been recently reviewed [15]. In this paper, we will discuss some of the more recently recognized extrahepatic manifestations of HCV infection, with particular emphasis on its association with glomerular disease.

Top

References

  1. Lürman: An epidemic of icterus. (in German) Berlin Klin Wschr 22:20–223, 1885
  2. MacCallum FO, Bauer DJ: Homologous serum jaundice-Transmission experiments with human volunteers. Lancet i:622–627, 1944
  3. Blumberg BS, Alter HJ, Visnich S: A "new" antigen in leukemia sera. JAMA 191:101–106, 1965
  4. Prince AM, Hargrove RL, Szmuness W, Cherubin CE, Fontana VJ, Jeffries GH: Immunologic distinction between infectious and serum hepatitis. N Engl J Med 282:987–991, 1970
  5. Sherlock S: The natural history of hepatitis B. Postgrad Med J 63:7–11, 1987
  6. Feinstone SM, Kapikian AZ, Purcell RH, Alter HJ, Holland PV: Transfusion-associated hepatitis not due to viral hepatitis type A or B. N Engl J Med 292:767–770, 1975 | PubMed | ISI | ChemPort |
  7. Bradley DW, McCaustland KA, Cook EH, Schable CA, Ebert JW, Maynard JE: Posttransfusion Non-A, Non-B hepatitis in chimpanzees. Gastroenterology 88:773–779, 1985
  8. Choo Q-L, Kuo G, Weiner AJ, Overby LR, Bradley DW, Houghton M: Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244:359–361, 1989 | Article | PubMed | ISI | ChemPort |
  9. Kuo G, Choo Q-L, Alter HJ, Gitnick GL, Redeker AG, Purcell RH, Miyamura T, Dienstag JL, Alter MJ, Stevens CE, Tegtmeier GE, Bonino F, Colombo M, Lee W-S, Kuo C, Berger K, Shuster JR, Overby LR, Bradley DW, Houghton M: An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. Science 244:362–364, 1989 | Article | PubMed | ISI | ChemPort |
  10. Alter HJ, Purcell RH, Shih JW, Melpolder JC, Houghton M, Choo Q-L, Kuo G: Detection of antibody to hepatitis C virus in prospectively followed transfusion recipients with acute and chronic non-A, non-B hepatitis. N Engl J Med 321:1494–1500, 1989 | PubMed | ISI | ChemPort |
  11. Alter MJ, Margolis HS, Krawczynski K, Judson FN, Mares A, Alexander WJ, Hu PY, Miller JK, Gerber MA, Sampliner RE, Meeks EL, Beach MJ: The natural history of community-acquired hepatitis C in the United States. N Engl J Med 327:1899–1905, 1992 | ChemPort |
  12. Yuki N, Hayashi N, Kasahara A, Hagiwara H, Katayama K, Fusamoto H, Kamada T: Hepatitis B virus markers and antibodies to hepatitis C virus in Japanese patients with hepatocellular carcinoma. Digestive Dis Sci 37:65–72, 1992
  13. Esteban JI, Genesca J, Alter HJ: Hepatitis C: Molecular Biology, Pathogenesis, Epidemiology, Clinical Features, and Prevention, edited by Boyer JL, Ockner RK, New York, W.B. Saunders Co., 1992, pp 253–282 (Boyer JL, editor: Progress in Liver Disease, vol X, chapt 12)
  14. Houghton M, Weiner A, Han J, Kuo G, Choo Q-L: Molecular biology of the hepatitis C viruses: Implications for diagnosis, development and control of viral disease. Hepatology 14:381–388, 1991 | Article | PubMed | ChemPort |
  15. Johnson RJ, Couser WG: Hepatitis B infection and renal disease: Clinical, immunopathogenetic and therapeutic considerations. Kidney Int 37:663–676, 1990 | Article | PubMed | ISI | ChemPort |
  16. Weiner AJ, Brauer MJ, Rosenblatt J, Richman KH, Tung J, Crawford K, Bonino F, Saracco G, Choo Q-L, Houghton M, Han JH: Variable and hypervariable domains are found in the regions of HCV corresponding to the flavivirus envelope and NS1 proteins and the pestivirus envelope glycoproteins. Virology 180:842–848, 1991 | Article | PubMed | ISI | ChemPort |
  17. Simmonds P, Holmes EC, Cha T-A, Chan S-W, Mcomish F, Irvine B, Bealle E, Yap PL, Kolberg J, Urdea MS: Classification of hepatitis C virus into six major genotypes and a series of subtypes by phylogenetic analysis of the NS-5 region. J Gen Virol (in press)
  18. Weiner AJ, Kuo G, Bradley DW, Bonino F, Saracco G, Lee C, Rosenblatt J, Choo Q-L, Houghton M: Detection of hepatitis C viral sequences in non-A, non-B hepatitis. Lancet 335:1–3, 1990 | Article | PubMed | ISI | ChemPort |
  19. Nishiguchi S, Kuroki T, Ueda T, Fukuda K, Takeda T, Nakajima S, Shiomi S, Kobayashi K, Otani S, Hayashi N, Shikata T: Detection of hepatitis C virus antibody in the absence of viral RNA in patients with autoimmune hepatitis. Ann Int Med 116:21–25, 1992
  20. Clemens JM, Taskar S, Chau K, Vallari D, Shih J W-K, Alter HJ, Schleicher JB, Mimms LT: IgM antibody response in acute hepatitis C viral infection. Blood 79:169–172, 1992
  21. Lau J, Davis GL, Kniffen J, Qian K-P, Urdea MS, Chan CS, Mizokami M, Neuwald PD, Wilber JC: Significance of serum hepatitis C virus RNA levels in chronic hepatitis C. Lancet 341:1501–1504, 1993 | Article | PubMed | ISI | ChemPort |
  22. Bukh J, Purcell RH, Miller RH: Importance of primer selection for the detection of hepatitis C virus RNA with the polymerase chain reaction assay. Proc Natl Acad Sci USA 89:187–191, 1992
  23. Gretch D, Lee W, Corey L: Use of aminotransferase, hepatitis C antibody, and hepatitis C polymerase chain reaction RNA assays to establish the diagnosis of hepatitis C virus infection in a diagnostic virology laboratory. J Clin Microbiol 30:2145–2149, 1992
  24. Krauledat PB: Report of the proceedings, in First International Symposium of Hepatitis C Virus, Rome, Italy, 1989
  25. Tibbs CJ, Palmer SJ, Coker R, Clark SK, Parsons GM, Hojvat S, Peterson D, Banatvala JE: Prevalence of hepatitis C in tropical communities: The importance of confirmatory assays. J Med Virol 34:143–147, 1991
  26. Ellis LA, Brown JD, Conradie JD, Paterson R, Sher R, Millo J, Theodossiadou E, Dusheiko GM: Prevalence of hepatitis C in South Africa: Detection of anti-HCV in recent and stored serum. J Med Virol 32:249–251, 1990
  27. Hyams KC, Phillips IA, Moran AY, Tejada A, Wignall FS, Escamilla J: Seroprevalence of hepatitis C antibody in Peru. J Med Virol 37:127–131, 1992
  28. Alter HJ, Purcell RH, Holland PV, Alling DW, Koziol DE: Donor transaminase and recipient hepatitis. JAMA 246:630–634, 1981 | Article | PubMed | ISI | ChemPort |
  29. Koziol DE, Holland PV, Alling DW, Melpolder JC, Solomon RE, Purcell RH, Hudson LM, Shoup FJ, Krakauer H, Alter HJ: Antibody to hepatitis B core antigen as a paradoxical marker for non-A, non-B hepatitis agents in donated blood. Ann Int Med 104:488–495, 1986
  30. Esteban JI, González A, Hernández JM, Viladomiu L, Sánchez C, Lópex-Talavera JC, Lucea D, Martin-Vega C, Vidal X, Esteban R, Guardia J: Evaluation of antibodies to hepatitis C virus in a study of transfusion-associated hepatitis. N Engl J Med 323:1107–1112, 1990 | ChemPort |
  31. Pascual M, Perrin L, Giostra E, Schifferli JA: Hepatitis C virus in patients with cryoglobulinemia type II. J Infect Dis 162:569–570, 1990
  32. Ferri C, Greco F, Longombardo G, Palla P, Moretti A, Marzo E, Fosella PV, Pasero G, Bombardieri S: Antibodies against hepatitis C virus in mixed cryoglobulinemia patients. Infection 19:417–420, 1991
  33. Ferri C, Greco F, Longombardo G, Palla P, Marzo E, Moretti A, Mazzoni A, Pasero G, Bombardieri S: Association between hepatitis C virus and mixed cryoglobulinemia. Clin Exp Rheumatol 9:621–624, 1991
  34. Casato M, Taliani G, Pucillo LP, Goffredo F, Lagana B, Bonomo L: Cryoglobulinemia and hepatitis C virus. Lancet 337:1047–1048, 1991 | Article | PubMed | ISI | ChemPort |
  35. Disdier P, Harlé J-R, Weiller P-J: Cryoglobulinemia and hepatitis C infection. Lancet 338:1151–1152, 1991
  36. Dammacco F, Sansonno D: Antibodies to hepatitis C virus in essential mixed cryoglobulinemia. Clin Exp Immunol 87:352–356, 1992 | PubMed |
  37. Durand JM, Kaplanski G, Lefevre P, Richard MA, Andrac L, Trepo C, Soubeyrand J: Effect of interferon-alpha2b on cryoglobulinemia related to hepatitis C virus infection. J Infec Dis 165:778–779, 1992
  38. Galli M, Monti G, Monteverde A, Invernizzi F, Pietrogrande M, Girolamo MD, Mazzaro C, Migliaresi S, Mussini C, Ossi E, Renoldi P: Hepatitis C virus and mixed cryoglobulinemias. Lancet 339:989, 1992
  39. Ferri C, Greco F, Longombardo G, Palla P, Marzo E, Moretti A: Hepatitis C virus antibodies in mixed cryoglobulinemia. Clin Exp Rheumatol 9:95–96, 1991
  40. Pechère-Bertschi A, Perrin L, De Saussure P, Widmann JJ, Giostra E, Schifferli JA: Hepatitis C: A possible etiology for cryoglobulinaemia type II. Clin Exp Immunol 89:419–422, 1992 | PubMed |
  41. Agnello V, Chung RT, Kaplan LM: A role for hepatitis C virus infection in type II cryoglobulinemia. N Engl J Med 327:1490–1495, 1992 | PubMed | ISI | ChemPort |
  42. Marcellin P, Descamps V, Martinot-Peignoux M, Larzul D, Xu L, Boyer N, Pham B-N, Crickx B, Guillevin L, Belaich S, Erlinger S, Benhamou J-P: Cryoglobulinemia with vasculitis associated with hepatitis C virus infection. Gastroenterology 104:272–277, 1993 | PubMed |
  43. Levey JM, Bjornsson B, Banner B, Kuhns M, Malhotra R, Whitman N, Romain PL, Cropley T, Bonkovsky HL: Mixed cryoglobulinemia in chronic hepatitis C infection. Medicine 73:53–67, 1994
  44. Cacoub P, Fabiani FL, Musset L, Perrin M, Frangeul L, Leger JM, Huraux J-M, Piette J-C, Godeau P: Mixed cryoglobulinemia and hepatitis C virus. Am J Med 96:124–132, 1994 | Article | PubMed | ISI | ChemPort |
  45. Johnson RJ, Gretch DR, Yamabe H, Hart J, Bacchi CE, Hartwell P, Couser WG, Corey L, Wener MH, Alpers CE, Willson R: Membranoproliferative glomerulonephritis associated with hepatitis C virus infection. N Engl J Med 328:465–470, 1993 | Article | PubMed | ISI | ChemPort |
  46. Misiani R, Bellavita P, Fenili D, Borelli G, Marchesi D, Massazza M, Vendramin G, Comotti B, Tanzi E, Scudeller G, Zanetti A: Hepatitis C virus infection in patients with essential mixed cryoglobulinemia. Ann Int Med 117:573–577, 1992
  47. Horikoshi S, Okada T, Shirato I, Inokuchi S, Ohmuro H, Tomino Y, Koide H: Diffuse proliferative glomerulonephritis with hepatitis C virus-like particles in paramesangial dense deposits in a patient with chronic hepatitis C virus hepatitis. Nephron 64:462–464, 1993
  48. Harlé JR, Disdier P, Dussol B, Bolla G, Casanova P, Weiller PJ: Membranoproliferative glomerulonephritis and hepatitis C infection. Lancet 341:904, 1993
  49. Gonzalo A, Barcena R, Mampaso F, Zea A, Ortuño J: Membranopro-liferative glomerulonephritis and hepatitis C virus infection. Nephron 63:475–476, 1993
  50. Doutrelepont J-M, Adler M, Willems M, Durez P, Yap S-H: Hepatitis C infection and membranoproliferative glomerulonephritis. Lancet 341:317, 1993
  51. Yamabe H, Fukushi K, Ohsawa H, Miyata M, Inuma H, Sasaki T, Kaizuka M, Tamura N, Tsunoda S, Fujita Y, Onodera K: Hepatitis C virus (HCV) infection may be an important cause of membranoproliferative glomerulonephritis (MPGN) in Japan. (abstract) JASN 4:291, 1993
  52. Bursten DM, Rodby RA: Membranoproliferative glomerulonephritis associated with hepatitis C virus infection. J Am Soc Nephrol 4:1288–1293, 1993
  53. Pasquariello A, Ferri C, Moriconi L, LaCivita L, Longombardo G, Lombardini F, Greco F, Zignego AL: Cryoglobulinemic membranoproliferative glomerulonephritis and hepatitis C virus infection. Am J Nephrol 13:300–304, 1993 | PubMed | ISI | ChemPort |
  54. Sawada T, Hirohata S, Inoue T, Ito K: Development of rheumatoid arthritis after hepatitis C virus infection Arthr Rheum 34:1620–1621, 1991
  55. Haddad J, Deny P, Munz-Gotheil C, Ambrosini J-C, Trinchet J-C, Pateron D, Mal F, Callard P, Beaugrand M: Lymphocytic sialoadenitis of Sjögren's syndrome associated with chronic hepatitis C virus liver disease. Lancet 339:321–323, 1992
  56. Wilson SE, Lee WM, Murakami C, Weng J, Moninger GA: Mooren's corneal ulcers and hepatitis C virus infection. N Engl J Med 329:62, 1993 | Article | PubMed |
  57. Herrero C, Vicente A, Bruguera M, Ercilla MG, Barrera JM, Vidal J, Terés J, Mascaró JM, Rodés J: Is hepatitis C virus infection a trigger of porphyria cutanea tarda? Lancet 341:788–789, 1993
  58. Pawlotsky J-M, Yahia MB, Andre C, Voisin M-C, Intrator L, Roudot-Thoraval F, Deforges L, Duvoux C, Zafrani E-S, Duval J, Dhumeaux D: Immunological disorders in C virus chronic active hepatitis: A prospective case-control study. Hepatol 19:841–848, 1994
  59. Pateron D, Hartmann DJ, Duclos-Vallee JC, Jouanolle H, Beaugrand M: Latent autoimmune thyroid disease in patients with chronic HCV hepatitis. J Hepatol 16:244–245, 1992
  60. Cacoub P, Lunel-Fabian F, Huong Du LT: Polyarteritis nodosa and hepatitis C virus infection. Ann Int Med 116:605–606, 1992
  61. Quint L, Deny P, Guillevin L, Granger B, Jarrousse B, Lhote F, Scavizzi M: Hepatitis C virus in patients with polyarteritis nodosa. Prevalence in 38 patients. Clin Exp Rheumatol 9:253–257, 1991
  62. Florin-Christensen A, Roux MEB, Arana RM: Cryoglobulins in acute and chronic liver diseases. Clin Exp Immunol 16:599–605, 1974
  63. Popp JW, Dienstag JL, Wands JR, Bloch KJ: Essential mixed cryoglobulinemia without evidence for hepatitis B virus infection. Ann Int Med 92:379–383, 1980
  64. Levo Y, Gorevic PD, Kassab HJ, Zucker-Franklin D, Franklin EC: Association between hepatitis B virus and essential mixed cryoglobulinemia. N Engl J Med 296:1501–1504, 1977 | PubMed | ChemPort |
  65. Levo Y, Gorevic PD, Kassab H, Zucker-Franklin D, Gigli I, Franklin EC: Mixed cryoglobulinemia—An immune complex disease often associated with hepatitis B virus infection. Trans Assoc Am Phys 90:167–173, 1977
  66. Gorevic PD, Kassab HJ, Levo Y, Kohn R, Meltzer M, Prose P, Franklin EC: Mixed cryoglobulinemia: Clinical aspects and long-term follow-up of 40 patients. Am J Med 69:287–308, 1980 | Article | PubMed | ISI | ChemPort |
  67. D'Amico G, Colasanti G, Ferrario F, Sinico RA: Renal involvement in essential mixed cryoglobulinemia. Kidney Int 35:1004–1014, 1989
  68. Cordonnier DJ, Renversez JC, Vialtel P, Dechelette E: The kidney in mixed cryoglobulinemias. Springer Semin Immunopathol 9:395–415, 1987
  69. Tarantino A, De Vecchi A, Montagnino G, Imbasciati E, Mihatsch MJ, Zollinger HU, Di Belgiojoso GB, Busnach G, Ponticelli C: Renal disease in essential mixed cryoglobulinemia. Quart J Med 1–30, 1981
  70. Perez GO, Pardo V, Fletcher MA: Renal involvement in essential mixed cryoglobulinemia. Am J Kidney Dis 10:276–280, 1987
  71. Druet P, Letonturier P, Contet A, Mandet C: Cryoglobulinaemia in human renal diseases. Clin Exp Immunol 15:483–496, 1973
  72. Mazzucco G, Monga G, Casanova S, Cagnoli L: Cell interposition in glomerular capillary walls in cryoglobulinemic glomerulonephritis (CRYGN) ultrastructural investigation of 23 cases. Ultrastruc Pathol 10:355–361, 1986
  73. Fiorini G, Bernasconi P, Sinico RA, Chianese R, Pozzi F, D'Amico G: Increased frequency of antibodies to ubiquitous viruses in essential mixed cryoglobulinemia. Clin Exp Immunol 64:65–70, 1986 | PubMed |
  74. Fisher ER, Hellstrom HR: The membranous and proliferative glomerulonephritis of hepatic cirrhosis. Am J Clin Pathol 32:48–55, 1959
  75. Bloodworth JMB Jr, Sommers SC: "Cirrhotic glomerulosclerosis", a renal lesion associated with hepatic cirrhosis. Lab Invest 8:962–978, 1959
  76. Feizi T, Gitlin N: Immune-complex disease of the kidney associated with chronic hepatitis and cryoglobulinemia. Lancet ii:873–876, 1969
  77. Hague RV: Acute glomerulonephritis complicating Australia antigen-negative viral hepatitis. Scand J Infect Dis 7:277–279, 1975
  78. Nochy D, Callard P, Bellon B, Bariety J, Druet P: Association of overt glomerulonephritis and liver disease: A study of 34 patients. Clin Nephrol 6:422–427, 1976
  79. Berger J, Yaneva H, Nabarra B: Glomerular changes in patients with cirrhosis of the liver. Adv Nephrol 7:3–14, 1978
  80. Newell GC: Cirrhotic glomerulonephritis. Incidence, morphology, clinical features and pathogenesis. Am J Kidney Dis 9:183–190, 1987 | PubMed | ISI | ChemPort |
  81. Crawford DHG, Endre ZH, Axelsen RA, Lynch SV, Balderson GA, Strong RW, Kerlin P, Powell LW, Fleming SJ: Universal occurrence of glomerular abnormalities in patients receiving liver transplants. Am J Kidney Dis 19:339–344, 1992 | PubMed |
  82. Nakamoto Y, Iida H, Kobayashi K, Dohi K, Kida H, Hattori N, Takeuchi J: Hepatic glomerulonephritis. Vichows Arch 392:45–54, 1981
  83. Noble-Jamieson G, Thiru S, Johnston P, Friend P, Barnes ND: Glomerulonephritis with end-stage liver disease in childhood. Lancet 339:706–707, 1992
  84. Habib R, Broyer M: Clinical significance of allograft glomerulopathy. Kidney Int 44:S95–S98, 1993 | ISI |
  85. Krawczynski K, Beach MJ, Bradley DW, Kuo G, Di Bisceglie AM, Houghton M, Reyes GR, Kim JP, Choo Q-L, Alter MJ: Hepatitis C virus antigen in hepatocytes: Immunomorphologic detection and identification. Gastroenterology 103:622–629, 1992 | PubMed | ISI | ChemPort |
  86. Hiramatsu N, Hayashi N, Haruna Y, Kasahara A, Fusamoto H, Mori C, Fuke I, Okayama H, Kamada T: Immunohistochemical detection of hepatitis C virus-infected hepatocytes in chronic liver disease with monoclonal antibodies to core, envelope and NS3 regions of the hepatitis C virus genome. Hepatology 16:306–311, 1992
  87. Negro F, Pacchioni D, Shimizu Y, Miller RH, Bussolati G, Purcell RH, Bonino F: Detection of intrahepatic replication of hepatitis C virus RNA by in situ hybridization and comparison with histopathology. Proc Natl Acad Sci USA 89:2247–2251, 1992 | PubMed | ChemPort |
  88. Blight K, Trowbridge R, Rowland R, Gowans E: Detection of hepatitis C virus RNA by in situ hybridization. Liver 12:286–289, 1992
  89. Tiebosch ATMG, Wolters J, Frederik PFM, Van Der Wiel TWM, Zeppenfeldt E, Van Breda Vriesman PJC: Epidemiology of idiopathic glomerular disease: A prospective study. Kidney Int 32:112–116, 1987 | PubMed | ISI | ChemPort |
  90. Simon P, Ramee MP, Ang KS, Cam G: Variations of primary glomerulonephritis incidence in a rural area of 400,000 inhabitants in the last decade. Nephron 45:171, 1987
  91. Di Belgiojoso GB, Baroni M, Pagliari B, Lavagni MG, Porri MT, Banfi G, Colasanti G, Confalonieri R: Is membranoproliferative glomerulonephritis really decreasing? Nephron 40:380–381, 1985
  92. Habte B, Zewdic D, Porter KA, Mowbray JF: Pattern of glomerular disease in adult Ethiopians. International Society of Nephrology, Jerusalem, Israel, June 1993, (abstract) p 601
  93. Rollino C, Roccatello D, Giachino O, Basolo B, Piccoli G: Hepatitis C virus infection and membranous glomerulonephritis. Nephron 59:319–320, 1991
  94. Davda R, Peterson J, Weiner R, Croker B, Lau JY: Membranous glomerulonephritis in association with hepatitis C virus infection. Am J Kidney Dis 22:452–455, 1993
  95. Kato N, Ootsuyama Y, Ohkoshi S, Nakazawa T, Sekiya H, Hijikata M, Shimotohno K: Characterization of hypervariable regions in the putative envelope protein of hepatitis C virus. Biochem Biophys Res Commun 189:119–127, 1992
  96. Geltner D: Therapeutic approaches in mixed cryoglobulinemia. Springer Semin Immunopathol 10:103–113, 1988
  97. Gorevic PD, Frangione B: Mixed cryoglobulinemia cross-reactive idiotypes: Implications for the relationship of MC to rheumatic and lymphoproliferative diseases. Sem Hematol 28:79–94, 1991
  98. Kunkel HG, Agnello V, Joslin FG, Winchester RJ, Capra JD: Cross-idiotypic specificity among monoclonal IgM proteins with anti-gamma-globulin activity. J Exp Med 137:331–342, 1973 | Article | PubMed | ChemPort |
  99. Geltner D, Franklin EC, Frangione B: Anti-idiotypic activity in the IgM fractions of mixed cryglobulins. J Immunol 125:1530–1535, 1980 | PubMed | ChemPort |
  100. Alpers CE, Hudkins KL, Pritzl P, Johnson RJ: Mechanisms of clearance of immune complexes from peritubular capillaries in the rat. Am J Pathol 139:855–867, 1991 | PubMed | ISI | ChemPort |
  101. Fries JWU, Mendrick DL, Rennke HG: Determinants of immune complex-mediated glomerulonephritis. Kidney Int 34:333–345, 1988 | PubMed |
  102. Braverman IM, Yen A: Demonstration of immune complexes in spontaneous and histamine-induced lesions and in normal skin of patients with leukocytoclastic angiitis. J Invest Derm 64:105–112, 1975
  103. Mishiro S, Hoshi Y, Takeda K, Yoshikawa A, Gotanda T, Takahashi K, Akahane Y, Yoshizawa H, Okamoto H, Tsuda F, Peterson DA, Muchmore E: Non-A, non-B hepatitis specific antibodies directed at host-derived epitope: Implication for an autoimmune process. Lancet 336:1400–1403, 1990
  104. Michel G, Ritter A, Gerken G, Meyer Zum Büschenfelde K-H, Decker R, Manns MP: Anti-GOR and hepatitis C virus in autoimmune liver diseases. Lancet 339:267–269, 1992
  105. Warny M, Brenard R, Cornu C, Tomasi J-P, Geubel A-P: Anti-neutrophil antibodies in chronic hepatitis and the effect of alpha-interferon therapy. J Hepatol 17:294–300, 1993
  106. Davis GL, Balart LA, Schiff ER, Lindsay K, Bodenheimer HC, Perrillo RP, Carey W, Jacobson IM, Payne J, Dienstag JL, Van Thiel DH, Tamburro C, Lefkowitch J, Albrecht J, Meschievitz C, Ortego TJ, Gibas A: Treatment of chronic hepatitis C with recombinant interferon alfa. N Engl J Med 321:1501–1506, 1989 | PubMed | ISI | ChemPort |
  107. Di Bisceglie AM, Martin P, Kassianides C, Lisker-Melman M, Murray L, Waggoner J, Goodman Z, Banks SM, Hoofnagle JH: Recombinant interferon alfa therapy for chronic hepatitis C. N Engl J Med 321:1506–1510, 1989 | PubMed | ChemPort |
  108. Bonomo L, Casato M, Afeltra A, Caccavo D: Treatment of idiopathic mixed cryoglobulinemia with alpha interferon. Am J Med 83:726–730, 1987
  109. Knox TA, Hillyer CD, Kaplan MM, Berkman EM: Mixed cryoglobulinemia responsive to interferon-alpha. Am J Med 91:554–555, 1991
  110. Ferri C, Marzo E, Longombardo G, Lombardini F, Greco F, Bombardieri S: Alpha interferon in the treatment of mixed cryoglobulinemia patients. Eur J Cancer 27:S81–S82, 1991
  111. Casato M, Laganá B, Antonelli G, Dianzani F, Bonomo L: Long-term results of therapy with interferon-alpha for type II essential mixed cryoglobulinemia. Blood 78:3142–3147, 1991
  112. Taillan B, Ferrari E, Garnier G, Pesce A, Fuzibet J-G, Dujardin P: Low-dose interferon-alpha for mixed cryoglobulinemia associated with hepatitis C virus. (letter) Am J Med 93:476, 1992
  113. Ferri C, Marzo E, Longombardo G, Lombardini F, Civita LL, Vanacore R, Liberati AM, Gerli R, Greco F, Moretti A, Monti M, Gentilini P, Bombardieri S, Zignego AL; Interferon-alpha in mixed cryoglobulinemia patients. A randomized, crossover-controlled trial. Blood 81:1132–1136, 1993 | PubMed |
  114. Misiani R, Bellavita P, Fenili D, Vicari O, Marchesi D, Sironi PL, Zilio P, Vernocchi A, Massazza M, Vendramin G, Tanzi E, Zanetti: Interferon alpha-2a therapy in cryoglobulinemia associated with hepatitis virus. N Engl J Med 330:751–756, 1994 | Article | PubMed | ISI | ChemPort |
  115. Peters M: Mechanisms of action of interferons. Semin Liver Dis 9:235–239, 1989
  116. Selby P, Kohn J, Raymond J, Judson I, McElwain T: Nephrotic syndrome during treatment with interferon. Brit Med J 290:1180, 1985
  117. Averbuch S, Austin H, Sherwin S, Antonovynch T, Bunn P, Longo D: Acute interstitial nephritis with the nephrotic syndrome following recombinant leukocyte interferon therapy for mycosis fungoides. N Engl J Med 310:32–35, 1984 | PubMed | ISI | ChemPort |
  118. De Vecchi A, Montagnino G, Pozzi C, Tarantino A, Locatelli F, Ponticelli C: Intravenous methylprednisolone pulse therapy in essential mixed cryoglobulinemia nephropathy. Clin Nephrol 19:221–227, 1983
  119. Bradley JD, Brandt KD, Katz BP: Infectious complications of cyclophosphamide treatment for vasculitis. Arthr Rheum 32:45–53, 1989
  120. Erickson AL, Houghton M, Choo QL, Weiner AJ, Ralston R, Muchmore E, Walker CM: Hepatitis C virus-specific CTL responses in the liver of chimpanzees with acute and chronic hepatitis C. J Immunol 151:4189–4199, 1993 | ChemPort |
  121. Koziel MJ, Dudley D, Afdhal N, Choo Q-L, Houghton M, Ralston R, Walker BD: Hepatitis C virus (HCV)-specific cytotoxic T lymphocytes recognize epitopes in the core and envelope proteins of HCV. J Virol 67:7522–7532, 1993 | PubMed | ChemPort |
  122. Botarelli P, Brunetto MR, Minutello MA, Calvo P, Unutmaz D, Weiner AJ, Choo Q-L, Shuster JR, Kuo G, Bonino F, Houghton M, Abrignani: T-lymphocyte response to hepatitis C virus in different clinical courses of infection. Gastroenterology 104:580–587, 1993 | ChemPort |
  123. Gretch D, Han J, Wilson J, Dela Rosa C, Willson R, Carithers R, Busch M, Hart J, Sayers M, Corey L: Assessment of hepatitis C virus RNA levels by quantitative competitive RNA polymerase chain reaction: High titer viremia correlates with advanced state of disease. J Infect Dis (in press)
  124. Hagiwara H, Hayashi N, Mita E, Naito M, Kasahara A, Fusamoto H, Kamada T: Quantitation of hepatitis C virus RNA in serum of asymptomatic blood donors and patients with type C chronic liver disease. Hepatology 17:545–550, 1993
  125. Wright TL, Donegan E, Hsu H, Ferrell L, Lake JR, Kim M, Combs C, Fennessy S, Roberts JP, Ascher NL, Greenberg HB: Recurrent and acquired hepatitis C viral infection in liver transplant recipients. Gastroenterology 103:317–322, 1992
  126. Ferrell LD, Wright TL, Roberts J, Ascher N, Lake J: Hepatitis C viral infection in liver transplant recipients. Hepathology 16:865–876, 1992
  127. Morales JM, Munoz MA, Castellano G, Colina F, Fuertes A, Andres A, Campo C, Blasco A, Hernandez E, Rodicio JL: Impact of hepatitis C in long-functioning renal transplants: A clinicopathological follow-up. Transplant Proc 25:1450–1453, 1993
  128. Pereira BJG, Milford EL, Kirkman RL, Quan S, Sayre KR, Johnson PJ, Wilber JC, Levey AS: Prevalence of hepatitis C virus RNA in organ donors positive for hepatitis C antibody and in the recipients of their organs. N Engl J Med 327:910–915, 1992
  129. Aeder MI, Shield CF, Tegtmeier GE, Bayer W, Luger AM, Nelson PW, Pierce GE, Polito A, Wilber JC, Johnson P, Ross G, Bryan CF: Incidence and clinical impact of hepatitis C virus-positive donors in cadaveric transplantation. Transplant Proc 25:1469–1471, 1993
  130. Roth D, Zucker K, Cirocco R, Demattos A, Burke GW, Nery J, Esquenazi V, Babischkin S, Miller J: The impact of hepatitis C virus infection on renal allograft recipients. Kidney Int 45:238–244, 1994 | PubMed |
  131. Pol S, Legendre C, Saltiel C, Carnot F, Bréchot C, Berthelot P, Mattlinger B, Kreis H: Hepatitis C virus in kidney recipients. Epidemiology and impact on renal transplantation. J Hepatol 15:202–206, 1992
  132. Rao KV, Anderson WR, Kasiske BL, Dahl DC: Value of liver biopsy in the evaluation and management of chronic liver disease in renal transplant recipients. Am J Med 94:241–250, 1993 | PubMed |
  133. Gretch DR, Gaur L, Lesniewski R, Nelson K, Strong M, Johnson R, Corey L, Perkins J, Lesniewski R, Nelson K, Strong M, Johnson R, Corey L, Perkins J, Carithers R: Donor-recipient match at the HLA-DQbeta locus is associated with recrudescence of chronic hepatitis following liver transplantation for end stage hepatitis C. Am Assoc Liver Dis Chicago, November, 1993 (abstract)

Extra navigation

.
ADVERTISEMENT