Hepatitis C virus: Models of immunopathogenesis and prophylaxis

Transfusion

Volumn 36, Issue 9, 1996, Pages 836-844

  Eckels, D D ^a   Flomenberg, P ^b,c   Gill, J C ^b  

^a BLOOD RESEARCH INSTITUTE   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; HEPATITIS VACCINE; VIRUS RNA;

BLOOD TRANSFUSION; CRYOGLOBULINEMIA; DISEASE ASSOCIATION; DISEASE SEVERITY; DISEASE TRANSMISSION; FLAVIVIRUS; HEALTH CARE SYSTEM; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNOPATHOLOGY; INCIDENCE; LIVER CELL; LIVER CELL CARCINOMA; LIVER FAILURE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; VACCINATION;

EID: 0029794026     PISSN: 00411132     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1537-2995.1996.36996420765.x     Document Type: Review

References (123)

1. Alter HJ. The hepatitis C virus and its relationship to the clinical spectrum of NANB hepatitis. J Gastroenterol Hepatol 1990;5(Suppl 1):78-94.
2. Esteban JI, Gonzalez A, Hernandez JM, et al. Evaluation of antibodies to hepatitis C virus in a study of transfusion-associated hepatitis. N Engl J Med 1990;323:1107-12.
3. Dodd RY. The risk of transfusion-transmitted infection (editorial). N Engl J Med 1992;327:419-21.
4. Kleinman S, Alter H, Busch M, et al. Increased detection of hepatitis C virus (HCV)-infected blood donors by a multiple-antigen HCV enzyme immunoassay. Transfusion 1992;32:805-13.
5. Alter MJ, Hadler SC, Judson FN, et al. Risk factors for acute non-A, non-B hepatitis in the United States and association with hepatitis C virus infection. JAMA 1990;264:2231-5.
6. Kuo G, Choo QL, Alter HJ, et al. An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. Science 1989;244:362-4.
7. Novati R, Thiers V, Monforte AD, et al. Mother-to-child transmission of hepatitis C virus detected by nested polymerase chain reaction. J Infect Dis 1992;165:720-3.
8. Plagemann PG. Hepatitis C virus. Arch Virol 1991;120:165-80.
9. Resnick RH, Koff R. Hepatitis C-related hepatocellular carcinoma. Prevalence and significance. Arch Intern Med 1993;153:1672-7.
10. Misiani R, Bellavita P, Fenili D, et al. Interferon alfa-2a therapy in cryoglobulinemia associated with hepatitis C virus. N Engl J Med 1994;330:751-6.
11. Thiele DL. Implications of anti-hepatitis C reactivity in 'autoimmune' chronic active hepatitis. Gastroenterology 1990;99:1531-3.
12. McFarlane BM, Bridger C, Tibbs CJ, et al. Virus-induced autoimmunity in hepatitis C virus infections: a rare event. J Med Virol 1994;42:66-72.
13. Dienstag JL, Alter HJ. Non-A, non-B hepatitis: evolving epidemiologic and clinical perspective. Semin Liver Dis 1986;6:67-81.
14. Koretz RL, Stone O, Mousa M, Gitnick GL. Non-A, non-B post-transfusion hepatitis - a decade later. Gastroenterology 1985;88:1251-4.
15. Alter MJ, Margolis HS, Krawczynski K, et al. The natural history of community-acquired hepatitis C in the United States. N Engl J Med 1992;327:1899-905.
16. Alter MJ. Non-A, Non-B hepatitis: sorting through a diagnosis of exclusion. Ann Intern Med 1989;110:583-5.
17. Tong MJ, el-Farra NS, Reikes AR, Co RL. Clinical outcomes after transfusion-associated hepatitis C. N Engl J Med 1995;332:1463-6.
18. Bernstein BM, Gill JC. Natural history and therapy of hepatitis B and C in patients with HIV disease. AIDS Clin Rev 1993-94:129-43.
19. Choo QL, Kuo G, Weiner AJ, et al. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 1989;244:359-62.
20. Takahashi K, Kishimoto S, Yoshizawa H, et al. p26 protein and 33-nm particle associated with nucleocapsid of hepatitis C virus recovered from the circulation of infected hosts. Virology 1992;191:431-4.
21. Alter HJ, Shih JW. Probable visualization of the elusive hepatitis C virus. Hepatology 1993;17:1164-6.
22. Waxman I, Baker B, Feinstone SM, Di Bisceglie AM. Detection of hepatitis C viral RNA in serum of a patient with acute non A, non B hepatitis. Am J Gastroenterol 1991;86:1240-2.
23. 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 U S A 1992;89:187-91.
24. Cuypers HT, Bresters D, Winkel IN, et al. Storage conditions of blood samples and primer selection affect the yield of cDNA polymerase chain reaction products of hepatitis C virus. J Clin Microbiol 1992;30:3220-4.
25. Chambers TJ, Hahn CS, Galler R, Rice CM. Flavivirus genome organization, expression, and replication. Annu Rev Microbiol 1990;44:649-88.
26. Choo QL, Richman KH, Han JH, et al. Genetic organization and diversity of the hepatitis C virus. Proc Natl Acad Sci U S A 1991;88:2451-5.
27. Grakoui A, Wychowski C, Lin C, et al. Expression and identification of hepatitis C virus polyprotein cleavage products. J Virol 1993;67:1385-95.
28. Hijikata M, Kato N, Ootsuyama Y, et al. Gene mapping of the putative structural region of the hepatitis C virus genome by in vitro processing analysis. Proc Natl Acad Sci U S A 1991;88:5547-51.
29. Houghton M, Weiner A, Han J, et al. Molecular biology of the hepatitis C viruses: implications for diagnosis, development and control of viral disease. Hepatology 1991;14:381-8.
30. Takamizawa A, Mori C, Fuke I, et al. Structure and organization of the hepatitis C virus genome isolated from human carriers. J Virol 1991;65:1105-13.
31. Cha TA, Kolberg J, Irvine B, et al. Use of a signature nucleotide sequence of hepatitis C virus for detection of viral RNA in human serum and plasma. J Clin Microbiol 1991;29:2528-34.
32. Han JH, Shyamala V, Richman KH, et al. Characterization of the terminal regions of hepatitis C viral RNA: identification of conserved sequences in the 5′ untranslated region and poly(A) tails at the 3′ end. Proc Natl Acad Sci U S A 1991;88:1711-5.
33. Takeuchi K, Kubo Y, Boonmar S, et al. The putative nucleocapsid and envelope protein genes of hepatitis C virus determined by comparison of the nucleotide sequences of two isolates derived from an experimentally infected chimpanzee and healthy human carriers. J Gen Virol 1990;71:3027-33.
34. Weiner AJ, Brauer MJ, Rosenblatt J, et al. 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 1991;180:842-8.
35. Han JH, Houghton M. Group specific sequences and conserved secondary structures at the 3′ end of HCV genome and its implication for viral replication. Nucleic Acids Res 1992;20:3520.
36. Koziel MJ. Immunology of viral hepatitis. Am J Med 1996;100:98-109.
37. Murakawa K, Esumi M, Kato T, et al. Heterogeneity within the nonstructural protein 5-encoding region of hepatitis C viruses from a single patient. Gene 1992;117:229-32.
38. Ulrich PP, Romeo JM, Lane PK, et al. Detection, semiquantitation, and genetic variation in hepatitis C virus sequences amplified from the plasma of blood donors with elevated alanine aminotransferase. J Clin Invest 1990;86:1609-14.
39. Okamoto H, Kojima M, Okada S, et al. Genetic drift of hepatitis C virus during an 8.2-year infection in a chimpanzee: variability and stability. Virology 1992;190:894-9.
40. Weiner AJ, Geysen HM, Christopherson C, et al. Evidence for immune selection of hepatitis C virus (HCV) putative envelope glycoprotein variants: potential role in chronic HCV infections. Proc Natl Acad Sci U S A 1992;89:3468-72.
41. Sodeyama T, Kiyosawa K, Urushihara A, et al. Detection of hepatitis C virus markers and hepatitis C virus genomic-RNA after needlestick accidents. Arch Intern Med 1993;153:1565-72.
42. Tedder RS, Briggs M, Ring C, et al. Hepatitis C antibody profile and viraemia prevalence in adults with severe haemophilia. Br J Haematol 1991;79:512-5.
43. Chien DY, Choo QL, Tabrizi A, et al. Diagnosis of hepatitis C virus (HCV) infection using an immunodominant chimeric polyprotein to capture circulating antibodies: reevaluation of the role of HCV in liver disease. Proc Natl Acad Sci U S A 1992;89:10011-5.
44. Nasoff MS, Zebedee SL, Inchauspe G, Prince AM. Identification of an immunodominant epitope within the capsid protein of hepatitis C virus. Proc Natl Acad Sci U S A 1991;88:5462-6.
45. Farci P, Alter HJ, Govindarajan S, et al. Lack of protective immunity against reinfection with hepatitis C virus. Science 1992;258:135-40.
46. Choo QL, Kuo G, Ralston R, et al. Vaccination of chimpanzees against infection by the hepatitis C virus. Proc Natl Acad Sci U S A 1994;91:1294-8.
47. Alberti A, Morsica G, Chemello L, et al. Hepatitis C viraemia and liver disease in symptom-free individuals with anti-HCV. Lancet 1992;340:697-8.
48. Hino K, Sainokami S, Shimoda K, et al. Genotypes and titers of hepatitis C virus for predicting response to interferon in patients with chronic hepatitis C. J Med Virol 1994;42:299-305.
49. 2b for 60 weeks. Hepatology 1994;19:280-5.
50. Enomoto N, Sakuma I, Asahina Y, et al. Comparison of full-length sequences of interferon-sensitive and resistant hepatitis C virus 1b. Sensitivity to interferon is conferred by amino acid substitutions in the NS5A region. J Clin Invest 1995;96:224-30.
51. Poynard T, Bedossa P, Chevallier M, et al. A comparison of three interferon alfa-2b regimens for the long-term treatment of chronic non-A, non-B hepatitis. Multicenter Study Group. N Engl J Med 1995;332:1457-62.
52. Kobayashi Y, Watanabe S, Konishi M, et al. Detection of hepatitis C virus RNA by nested polymerase chain reaction in sera of patients with chronic non-A, non-B hepatitis treated with interferon. J Hepatol 1992;16:138-44.
53. Bresters D, Mauser-Bunschoten EP, Cuypers HT, et al. Disappearance of hepatitis C virus RNA in plasma during interferon alpha-2B treatment in hemophilia patients. Scand J Gastroenterol 1992;27:166-8.
54. Chayama K, Saitoh S, Arase Y, et al. Effect of interferon administration on serum hepatitis C virus RNA in patients with chronic hepatitis C. Hepatology 1991;13:1040-3.
55. Hagiwara H, Hayashi N, Mita E, et al. Detection of hepatitis C virus RNA in serum of patients with chronic hepatitis C treated with interferon-alpha. Hepatology 1992;15:37-41.
56. Okada S, Akahane Y, Suzuki H, et al. The degree of variability in the amino terminal region of the E2/NS1 protein of hepatitis C virus correlates with responsiveness to interferon therapy in viremic patients. Hepatology 1992;16:619-24.
57. Shindo M, Di Bisceglie AM, Cheung L, et al. Decrease in serum hepatitis C viral RNA during alpha-interferon therapy for chronic hepatitis C. Ann Intern Med 1991;115:700-4.
58. Yoshioka K, Kakumu S, Wakita T, et al. Detection of hepatitis C virus by polymerase chain reaction and response to interferon-alpha therapy: relationship to genotypes of hepatitis C virus. Hepatology 1992;16:293-9.
59. Farci P, Alter HJ, Wong D, et al. A long-term study of hepatitis C virus replication in non-A, non-B hepatitis. N Engl J Med 1991;325:98-104.
60. Miyamoto H, Okamoto H, Sato K, et al. Extraordinarily low density of hepatitis C virus estimated by sucrose density gradient centrifugation and the polymerase chain reaction. J Gen Virol 1992;73:715-8.
61. Bukh J, Purcell RH, Miller RH. Sequence analysis of the 5′ noncoding region of hepatitis C virus. Proc Natl Acad Sci U S A 1992;89:4942-6.
62. Ballardini G, Groff P, Pontisso P, et al. Hepatitis C virus (HCV) genotype, tissue HCV antigens, hepatocellular expression of HLA-A,B,C, and intercellular adhesion-1 molecules. Clues to pathogenesis of hepatocellular damage and response to interferon treatment in patients with chronic hepatitis C. J Clin Invest 1995;95:2067-75.
63. Shimizu YK, Iwamoto A, Hijikata M, et al. Evidence for in vitro replication of hepatitis C virus genome in a human T-cell line. Proc Natl Acad Sci U S A 1992;89:5477-81.
64. Zignego AL, Macchia D, Mont: M, et al. Infection of peripheral mononuclear blood cells by hepatitis C virus. J Hepatol 1992;15:382-6.
65. Ferri C, Monti M, La Civita L, et al. Infection of peripheral blood mononuclear cells by hepatitis C virus in mixed cryoglobulinemia. Blood 1993;82:3701-4.
66. Moldvay J, Deny P, Pol S, et al. Detection of hepatitis C virus RNA in peripheral blood mononuclear cells of infected patients by in situ hybridization. Blood 1994;83:269-73.
67. Willems M, Peerlinck K, Moshage H, et al. Hepatitis C virus-RNAs in plasma and in peripheral blood mononuclear cells of hemophiliacs with chronic hepatitis C: evidence for viral replication in peripheral blood mononuclear cells. J Med Virol 1994;42:272-8.
68. Martell M, Esteban JI, Quer J, et al. Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: quasispecies nature of HCV genome distribution. J Virol 1992;66:3225-9.
69. Bouffard P, Hayashi PH, Acevedo R, et al. Hepatitis C virus is detected in a monocyte/macrophage subpopulation of peripheral blood mononuclear cells of infected patients. J Infect Dis 1992;166:1276-80.
70. Lamas E, Baccarini P, Housset C, et al. Detection of hepatitis C virus (HCV) RNA sequences in liver tissue by in situ hybridization. J Hepatol 1992;16:219-23.
71. Takehara T, Hayashi N, Mita E, et al. Detection of the minus strand of hepatitis C virus RNA by reverse transcription and polymerase chain reaction: implications for hepatitis C virus replication in infected tissue. Hepatology 1992;15:387-90.
72. Adorini L, Harvey MA, Miller A, Sercarz EE. Fine specificity of regulatory T cells. II. Suppressor and helper T cells are induced by different regions of hen egg-white lysozyme in a genetically nonresponder mouse strain. J Exp Med 1979;150:293-306.
73. Eckels DD, Sell TW, Bronson SR, et al. Human helper T-cell clones that recognize different influenza hemagglutinin determinants are restricted by different HLA-D region epitopes. Immunogenetics 1984;19:409-23.
74. Klenerman P, Rowland-Jones S, McAdam S, et al. Cytotoxic T-cell activity antagonized by naturally occurring HIV-1 Gag variants. Nature 1994;369:403-7.
75. Bertoletti A, Sette A, Chisari FV, et al. Natural variants of cytotoxic epitopes are T-cell receptor antagonists for antiviral cytotoxic T cells. Nature 1994;369:407-10.
76. Cerny A, McHutchison JG, Pasquinelli C, et al. Cytotoxic T lymphocyte response to hepatitis C virus-derived peptides containing the HLA A2.1 binding motif. J Clin Invest 1995;95:521-30.
77. Shirai M, Arichi T, Nishioka M, et al. CTL responses of HLA-A2.1-transgenic mice specific for hepatitis C viral peptides predict epitopes for CTL of humans carrying HLA-A2.1. J Immunol 1995;154:2733-42.
78. Botarelli P, Brunetto MR, Minutello MA, et al. T-lymphocyte response to hepatitis C virus in different clinical courses of infection. Gastroenterology 1993;104:580-7.
79. Minutello MA, Pileri P, Unutmaz D, et al. Compartmentalization of T lymphocytes to the site of disease: intrahepatic CD4+ T cells specific for the protein NS4 of hepatitis C virus in patients with chronic hepatitis C. J Exp Med 1993;178:17-25.
80. Engelhard VH. Structure of peptides associated with class I and class II MHC molecules. Annu Rev Immunol 1994;12:181-207.
81. Jane way CA Jr. The T cell receptor as a multicomponent signalling machine: CD4/CD8 coreceptors and CD45 in T cell activation. Annu Rev Immunol 1992;10:645-74.
82. Linsley PS, Ledbetter JA. The role of the CD28 receptor during T cell responses to antigen. Annu Rev Immunol 1993;11:191-212.
83. Romagnani S. Lymphokine production by human T cells in disease states. Annu Rev Immunol 1994;12:227-57.
84. Allen PM. Peptides in positive and negative selection: a delicate balance. Cell 1994;76:593-6.
85. Evavold BD, Allen PM. Separation of IL-4 production from Th cell proliferation by an altered T cell receptor ligand. Science 1991;252:1308-10.
86. Carding SR, West J, Woods A, Bottomly K. Differential activation of cytokine genes in normal CD4-bearing T cells is stimulus dependent. Eur J Immunol 1989;19:231-8.
87. Murray JS, Madri J, Pasqualini T, Bottomly K. Functional CD4 T cell subset interplay in an intact immune system. J Immunol 1993;150:4270-6.
88. Pfeiffer C, Murray J, Madri J, Bottomly K. Selective activation of Th1- and Th2-like cells in vivo - response to human collagen IV. Immunol Rev 1991;123:65-84.
89. Stout RD, Bottomly K. Antigen-specific activation of effector macrophages by IFN-γproducing (TH1) T cell clones. Failure of IL-4-producing (TH2) T cell clones to activate effector function in macrophages. J Immunol 1989;142:760-5.
90. Killar LM, Hatfield CA, Carding SR, et al. In vivo administration of interleukin 1 elicits increased Ia antigen expression on B cells through the induction of interleukin 4. Eur J Immunol 1989;19:2205-10.
91. Paul WE, Ohara J. B-cell stimulatory factor-1/interleukin 4. Annu Rev Immunol 1987;5:429-59.
92. Ding L, Linsley PS, Huang LY, et al. IL-10 inhibits macrophage costimulatory activity by selectively inhibiting the up-regulation of B7 expression. J Immunol 1993;151:1224-34.
93. Schwartz RH. Costimulation of T lymphocytes: the role of CD28, CTLA-4, and B7/BB1 in interleukin-2 production and immunotherapy. Cell 1992;71:1065-8.
94. Moore KW, O'Garra A, de Waal Malefyt R, et al. Interleukin-10. Annu Rev Immunol 1993;11:165-90.
95. Gooding LR. Virus proteins that counteract host immune defenses. Cell 1992;71:5-7.
96. Saukkonen JJ, Kornfeld H, Berman JS. Expansion of a CD8+CD28- cell population in the blood and lung of HIV-positive patients. J Acquir Immune Defic Syndr 1993;6:1194-204.
97. Markmann J, Lo D, Naji A, et al. Antigen presenting function of class II MHC expressing pancreatic beta cells. Nature 1988;336:476-9.
98. Schall TJ, O'Hehir RE, Goeddel DV, Lamb JR. Uncoupling of cytokine mRNA expression and protein secretion during the induction phase of T cell anergy. J Immunol 1992;148:381-7.
99. Koziel MJ, Dudley D, Wong JT, et al. Intrahepatic cytotoxic T lymphocytes specific for hepatitis C virus in persons with chronic hepatitis. J Immunol 1992;149:3339-44.
100. Mondelli M, Alberti A, Tremolada F, et al. In-vitro cell-mediated cytotoxicity for autologous liver cells in chronic non-A, non-B hepatitis. Clin Exp Immunol 1986;63:147-55.
101. Mondelli MU, Alberti A, Realdi G, Rondanelli EG. In vitro effect of lymphoblastoid alpha-interferon on subpopulations of effector cells mediating cytotoxicity for autologous hepatocytes in hepatitis B and non-A, non-B. Int J Immunopharmacol 1986;8:887-91.
102. Poralla T, Hutteroth TH, Meyerzum Buschenfelde KH. Cellular cytotoxicity against autologous hepatocytes in acute and chronic non-A, non-B hepatitis. Gut 1984;25:114-20.
103. Shirai M, Akatsuka T, Pendleton CD, et al. Induction of cytotoxic T cells to a cross-reactive epitope in the hepatitis C virus nonstructural RNA polymerase-like protein. J Virol 1992;66:4098-106.
104. Shirai M, Okada H, Nishioka M, et al. An epitope in hepatitis C virus core region recognized by cytotoxic T cells in mice and humans. J Virol 1994;68:3334-42.
105. Ferrari C, Valli A, Galati L, et al. T-cell response to structural and nonstructural hepatitis C virus antigens in persistent and self-limited hepatitis C virus infections. Hepatology 1994;19:286-95.
106. Eckels DD, Lamb JR, Lake P, et al. Antigen-specific human T-lymphocyte clones. Genetic restriction of influenza virus-specific responses to HLA-D region genes. Hum Immunol 1982;4:313-24.
107. Lamb JR, Green N. Analysis of the antigen specificity of influenza haemagglutinin-immune human T lymphocyte clones: identification of an immunodominant region for T cells. Immunology 1983;50:659-66.
108. Lamb JR, Eckels DD, Phelan M, et al. Antigen-specific human T lymphocyte clones: viral antigen specificity of influenza virus-immune clones. J Immunol 1982;128:1428-32.
109. Lamb JR, Eckels DD, Lake P, et al. Antigen-specific human T lymphocyte clones: induction, antigen specificity, and MHC restriction of influenza virus-immune clones. J Immunol 1982;128:233-8.
110. Allan W, Tabi Z, Cleary A, Doherty PC. Cellular events in the lymph node and lung of mice with influenza. Consequences of depleting CD4+ T cells. J Immunol 1990;144:3980-6.
111. Eichelberger M, Allan W, Zijlstra M, et al. Clearance of influenza virus respiratory infection in mice lacking class I major histocompatibility complex-restricted CD8+ T cells. J Exp Med 1991;174:875-80.
112. Eichelberger MC, Wang ML, Allan W, et al. Influenza virus RNA in the lung and lymphoid tissue of immunologically intact and CD4-depleted mice. J Gen Virol 1991;72:1695-8.
113. Hou S, Doherty PC, Zijlstra M, et al. Delayed clearance of Sendai virus in mice lacking class I MHC-restricted CD8+ T cells. J Immunol 1992;149:1319-25.
114. Doherty PC, Allan W. Eichelberger M, Carding SR. Roles of alpha beta and gamma delta T cell subsets in viral immunity. Annu Rev Immunol 1992;10:123-51.
115. Lamb JR, Eckels DD, Lake P, et al. Human T-cell clones recognize chemically synthesized peptides of influenza haemagglutinin. Nature 1982;300:66-9.
116. Unanue ER, Allen PM. Biochemistry and biology of antigen presentation by macrophages. Cell Immunol 1986;99:3-6.
117. Rosenthal AS, Shevach EM. Function of macrophages in antigen recognition by guinea pig T lymphocytes. I. Requirement for histocompatible macrophages and lymphocytes. J Exp Med 1973;138:1194-212.
118. Shevach EM, Rosenthal AS. Function of macrophages in antigen recognition by guinea pig T lymphocytes. II. Role of the macrophage in the regulation of genetic control of the immune response. J Exp Med 1973;138:1213-29.
119. Zinkernagel RM, Doherty PC. MHC-restricted cytotoxic T cells: studies on the biological role of polymorphic major transplantation antigens determining T-cell restriction-specificity, function, and responsiveness. Adv Immunol 1979;27:51-177.
120. Brodsky FM, Guagliardi LE. The cell biology of antigen processing and presentation. Annu Rev Immunol 1991;9:707-44.
121. Eyster ME, Diamondstone LS, Lien JM, et al. Natural history of hepatitis C virus infection in multitransfused hemophiliacs: effect of coinfection with human immunodeficiency virus. J Acquir Immune Defic Syndr 1993;6:602-10.
122. Flomenberg P, Balliet K, Bernstein B, et al. High specificity of hepatitis C second-generation enzyme immunoassay in HIV-infected patients (letter). J Acquir Immune Defic Syndr Hum Retrovirol 1995;9:97-8.
123. Linnen J, Wages J Jr, Zhang-Keck ZY, et al. Molecular cloning and disease association of hepatitis G virus: a transfusion-transmissible agent. Science 1996;271:505-8.