Natural history of hepatitis C virus infection in HIV-infected individuals and the impact of HIV in the era of highly active antiretroviral therapy: A meta-analysis

AIDS

Volumn 22, Issue 15, 2008, Pages 1979-1991

  Thein, Hla Hla ^a,b,f   Yi, Qilong ^c   Dore, Gregory J ^d   Krahn, Murray D ^a,b,e  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c National Epidemiology and Surveillance   (Canada)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

^e UNIVERSITY OF TORONTO   (Canada)

^f TORONTO GENERAL HOSPITAL   (Canada)

Author keywords

Cirrhosis; Fibrosis; Hepatitis C virus; HIV hepatitis C virus coinfection; Meta regression; Risk factors; Systematic review

Indexed keywords

ANTIRETROVIRUS AGENT; PROTEINASE INHIBITOR; RNA DIRECTED DNA POLYMERASE INHIBITOR;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; CD4 LYMPHOCYTE COUNT; CONFIDENCE INTERVAL; COVARIANCE; DISEASE COURSE; DISEASE DURATION; EMBASE; HEPATITIS C; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFORMATION RETRIEVAL; LIVER CIRRHOSIS; LIVER FIBROSIS; MEDLINE; MIXED INFECTION; OUTCOME ASSESSMENT; PREVALENCE; PRIORITY JOURNAL; PROBABILITY; RISK ASSESSMENT; SYSTEMATIC REVIEW;

ADULT; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; DISEASE PROGRESSION; HEPATITIS C, CHRONIC; HIV INFECTIONS; HUMANS; LIVER CIRRHOSIS; PROGNOSIS; RISK ASSESSMENT;

EID: 53549115066     PISSN: 02699370     EISSN: None     Source Type: Journal    
DOI: 10.1097/QAD.0b013e32830e6d51     Document Type: Article

References (84)

1. Kuo G, Choo QL, Alter HJ, Gitnick GL, Redeker AG, Purcell RH, et al. An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis. Science 1989; 244:362-364.
2. Centers for Disease Control and Prevention. Recommendations for prevention and control of hepatitis C virus (HCV) infection and HCV-related chronic disease. MMWR 1998; 47:1-39.
3. Rockstroh JK, Mocroft A, Soriano V, Tural C, Losso MH, Horban A, et al. Influence of hepatitis C virus infection on HIV-1 disease progression and response to highly active antiretroviral therapy. J Infect Dis 2005; 192:992-1002.
4. Rodger AJ, Roberts S, Lanigan A, Bowden S, Brown T, Crofts N. Assessment of long-term outcomes of community-acquired hepatitis C infection in a cohort with sera stored from 1971 to 1975. Hepatology 2000; 32:582-587.
5. Rodger AJ, Thomson JA, Thompson SC, Jolley D, Mijch AM, Lanigan A, et al. Assessment of long-term outcomes of hepatitis C virus infection in a cohort of patients with acute hepatitis in 1971-1975: results of a pilot study. J Gastroenterol Hepatol 1999; 14:269-273.
6. Thomas DL, Astemborski J, Rai RM, Anania FA, Schaeffer M, Galai N, et al. The natural history of hepatitis C virus infection: host, viral, and environmental factors. JAMA 2000; 284:450-456.
7. Pol S, Fontaine H, Carnot F, Zylberberg H, Berthelot P, Brechot C, et al. Predictive factors for development of cirrhosis in parenterally acquired chronic hepatitis C: a comparison between immunocompetent and immunocompromised patients. J Hepatol 1998; 29:12-19.
8. Pol S, Lamorthe B, Thi NT, Thiers V, Carnot F, Zylberberg H, et al. Retrospective analysis of the impact of HIV infection and alcohol use on chronic hepatitis C in a large cohort of drug users. J Hepatol 1998; 28:945-950.
9. Makris M, Preston FE, Rosendaal FR, Underwood JC, Rice KM, Triger DR. The natural history of chronic hepatitis C in haemophiliacs. Br J Haematol 1996; 94:746-752.
10. Eyster ME, Diamondstone LS, Lien JM, Ehmann WC, Quan S, Goedert JJ. Natural history of hepatitis C virus infection in multitransfused hemophiliacs: effect of coinfection with human immunodeficiency virus. The Multicenter Hemophilia Cohort Study. J Acquir Immune Defic Syndr 1993; 6:602-610.
11. Telfer P, Sabin C, Devereux H, Scott F, Dusheiko G, Lee C. The progression of HCV-associated liver disease in a cohort of haemophilic patients. Br J Haematol 1994; 87:555-561.
12. Mohsen AH, Easterbrook PJ, Taylor C, Portmann B, Kulasegaram R, Murad S, et al. Impact of human immunodeficiency virus (HIV) infection on the progression of liver fibrosis in hepatitis C virus infected patients. Cut 2003; 52:1035-1040.
13. Benhamou Y, Bochet M, Di Martino V, Charlotte F, Azria F, Coutellier A, et al. Liver fibrosis progression in human immunodeficiency virus and hepatitis C virus coinfected patients. The Multivirc Group. Hepatology 1999; 30:1054-1058.
14. Benhamou Y, Di Martino V, Bochet M, Colombet G, Thibault V, Liou A, et al. Factors affecting liver fibrosis in human immunodeficiency virus-and hepatitis C virus-coinfected patients: impact of protease inhibitor therapy. Hepatology 2001; 34:283-287.
15. Di Martino V, Rufat P, Boyer N, Renard P, Degos F, Martinot-Peignoux M, et al. The influence of human immunodeficiency virus coinfection on chronic hepatitis C in injection drug users: a long-term retrospective cohort study. Hepatology 2001; 34:1193-1199.
16. Martinez-Sierra C, Arizcorreta A, Diaz F, Roldan R, Martin-Herrera L, Perez-Guzman E, et al. Progression of chronic hepatitis C to liver fibrosis and cirrhosis in patients coinfected with hepatitis C virus and human immunodeficiency virus. Clin Infect Dis 2003; 36:491-498.
17. Sanchez-Quijano A, Andreu J, Gavilan F, Luque F, Abad MA, Soto B, et al. Influence of human immunodeficiency virus type 1 infection on the natural course of chronic parenterally acquired hepatitis C. Eur J Clin Microbiol Infect Dis 1995; 14:949-953.
18. Ragni MV, Belle SH. Impact of human immunodeficiency virus infection on progression to end-stage liver disease in individuals with hemophilia and hepatitis C virus infection. J Infect Dis 2001; 183:1112-1115.
19. Vallet-Pichard A, Pol S. Natural history and predictors of severity of chronic hepatitis C virus (HCV) and human immunodeficiency virus (HIV) co-infection. J Hepatol 2006; 44:S28-S34.
20. Bierhoff E, Fischer HP, Willsch E, Rockstroh J, Spengler U, Brackmann HH, et al. Liver histopathology in patients with concurrent chronic hepatitis C and HIV infection. Virchows Archiv 1997; 430:271-277.
21. Soto B, Sanchez-Quijano A, Rodrigo L, del Olmo JA, Garcia-Bengoechea M, Hernandez-Quero J, et al. Human immunodeficiency virus infection modifies the natural history of chronic parenterally-acquired hepatitis C with an unusually rapid progression to cirrhosis. J Hepatol 1997; 26:1-5.
22. Martin-Carbonero L, Benhamou Y, Puoti M, Berenguer J, Mallolas J, Quereda C, et al. Incidence and predictors ofsevere liver fibrosis in human immunodeficiency virus-infected patients with chronic hepatitis C: a European collaborative study. Clin Infect Dis 2004; 38:128-133.
23. Giordano TP, Kramer JR, SouchekJ, Richardson P, El-Serag HB. Cirrhosis and hepatocellular carcinoma in HIV-infected veterans with and without the hepatitis C virus: a cohort study, 1992-2001. Arch Intern Med 2004; 164:2349-2354.
24. Bica I, McGovern B, Dhar R, Stone D, McGowan K, Scheib R, et al. Increasing mortality due to end-stage liver disease in patients with human immunodeficiency virus infection. Clin Infect Dis 2001; 32:492-497.
25. Mocroft A, Soriano V, Rockstroh J, Reiss P, Kirk O, de Wit S, et al. Is there evidence for an increase in the death rate from liver-related disease in patients with HIV? AIDS 2005; 19:2117-2125.
26. Palella FJ Jr, Delaney KM, Moorman AC, Loveless MO, Fuhrer J, Satten GA, et al. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. N Engl J Med 1998; 338:853-860.
27. Pineda JA, Garcia-Garcia JA, Aguilar-Guisado M, Rios-Villegas MJ, Ruiz-Morales J, Rivero A, et al. Clinical progression of hepatitis C virus-related chronic liver disease in human immunodeficiency virus-infected patients undergoing highly active antiretroviral therapy. Hepatology 2007; 46:622-630.
28. Garcia-Samaniego J, Rodriguez M, Berenguer J, Rodriguez-Rosado R, Carbo J, Asensi V, et al. Hepatocellular carcinoma in HIV-infected patients with chronic hepatitis C. Am J Gastroenterol 2001; 96:179-183.
29. Macias J, Japon MA, Saez C, Palacios RB, Mira JA, Garcia-Garcia JA, et al. Increased hepatocyte fas expression and apoptosis in HIV and hepatitis C virus coinfection. J Infect Dis 2005; 192:1566-1576.
30. Macias J, Mira JA, Lopez-Cortes LF, Santos I, Giron-Gonzalez JA, Gonzalez-Serrano M, et al. Antiretroviral therapy based on protease inhibitors as a protective factor against liver fibrosis progression in patients with chronic hepatitis C. Antivir Ther 2006; 11:839-846.
31. Marine-Barjoan E, Saint-Paul MC, Pradier C, Chaillou S, Anty R, Michiels JF, et al. Impact of antiretroviral treatment on progression of hepatic fibrosis in HIV/hepatitis C virus co-infected patients. AIDS 2004; 18:2163-2170.
32. Merchante N, Macias J, Palacios RB, Mira JA, Garcia-Garcia JA, Lozano F, et al. Prevalence of nonsignificant liver fibrosis and rate of fibrosis progression in HIV/hepatitis C virus- co-infected patients: still a role for liver biopsy? AIDS 2004; 18:1746-1748.
33. Graham CS, Baden LR, Yu E, Mrus JM, Carnie J, Heeren T, et al. Influence of human immunodeficiency virus infection on the course of hepatitis C virus infection: a meta-analysis. aClin Infect Dis 2001; 33:562-569.
34. Bonacini M, Louie S, Bzowej N, Wohl AR. Survival in patients with HIV infection and viral hepatitis B or C: a cohort study. AIDS 2004; 18:2039-2045.
35. Qurishi N, Kreuzberg C, Luchters G, Effenberger W, Kupfer B, Sauerbruch T, et al. Effect of antiretroviral therapy on liver-related mortality in patients with HIV and hepatitis C virus coinfection. Lancet 2003; 362:1708-1713.
36. Verma S, Wang CH, Govindarajan S, Kanel G, Squires K, Bonacini M. Do type and duration of antiretroviral therapy attenuate liver fibrosis in HIV-hepatitis C virus-coinfected patients? Clin Infect Dis 2006; 42:262-270.
37. Brau N, Salvatore M, Rios-Bedoya CF, Fernandez-Carbia A, Paronetto F, Rodriguez-Orengo JF, et al. Slower fibrosis progression in HIV/HCV-coinfected patients with successful HIV suppression using antiretroviral therapy. J Hepatol 2006; 44:47-55.
38. Tural C, Fuster D, Tor J, Ojanguren I, Sirera G, Ballesteros A, et al. Time on antiretroviral therapy is a protective factor for liver fibrosis in HIV and hepatitis C virus (HCV) co-infected patients. J Viral Hepat 2003; 10:118-125.
39. Macias J, Castellano V, Merchante N, Palacios RB, Mira JA, Saez C, et al. Effect of antiretroviral drugs on liver fibrosis in HIV-infected patients with chronic hepatitis C: harmful impact of nevirapine. AIDS 2004; 18:767-774.
40. Mehta SH, Thomas DL, Torbenson M, Brinkley S, Mirel L, Chaisson RE, et al. The effect of antiretroviral therapy on liver disease among adults with HIV and hepatitis C coinfection. Hepatology 2005; 41:123-131.
41. Centers for Disease Control and Prevention. 1993 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults. MMWR 1992; 41:1-19.
42. Bedossa P, Poynard T. An algorithm for the grading of activity in chronic hepatitis C. The METAVIR Cooperative Study Group. Hepatology 1996; 24:289-293.
43. Desmet VJ, Gerber M, Hoofnagle JH, Manns M, Scheuer PJ. Classification of chronic hepatitis: diagnosis, grading and staging. Hepatology 1994; 19:1513-1520.
44. Ishak K, Baptista A, Bianchi L, Callea F, De Groote J, Gudat F, et al. Histological grading and staging of chronic hepatitis. J Hepatol 1995; 22:696-699.
45. Scheuer PJ. Classification of chronic viral hepatitis: a need for reassessment. J Hepatol 1991; 13:372-374.
46. Knodell RG, Ishak KG, Black WC, Chen TS, Craig R, Kaplowitz N, et al. Formulation and application of a numerical scoring system for assessing histological activity in asymptomatic chronic active hepatitis. Hepatology 1981; 1:431-435.
47. Bonacini M, Hadi G, Govindarajan S, Lindsay KL. Utility of a discriminant score for diagnosing advanced fibrosis or cirrhosis in patients with chronic hepatitis C virus infection. Am J Gastroenterol 1997; 92:1302-1304.
48. Gaiani S, Gramantieri L, Venturoli N, Piscaglia F, Siringo S, D'Errico A, et al. What is the criterion for differentiating chronic hepatitis from compensated cirrhosis? A prospective study comparing ultrasonography and percutaneous liver biopsy. J Hepatol 1997; 27:979-985.
49. Yi Q, Wang PP, Krahn M. Improving the accuracy of long-term prognostic estimates in hepatitis C virus infection. J Viral Hepat 2004; 11:166-174.
50. Poynard T, Bedossa P, Opolon P. Natural history of liver fibrosis progression in patients with chronic hepatitis C. The OBSVIRC, METAVIR, CLINIVIR, and DOSVIRC groups. Lancet 1997; 349:825-832.
51. Greenland S. Meta-analysis. In: Rothman KJ, Greenland S, editors. Modern epidemiology, 2nd ed. Philadelphia: Lippin-cott-Raven; 1998. pp. 643-673.
52. Egger M, Davey Smith G, Schneider M, Minder C. Bias in metaanalysis detected by a simple, graphical test. BMJ 1997; 313:629-634.
53. van Buuren S, Boshuizen HC, Knook DL. Multiple imputation of missing blood pressure covariates in survival analysis. Stat Med 1999; 18:681-694.
54. Thompson SG, Higgins JP. How should meta-regression analyses be undertaken and interpreted?Stat Med 2002; 21:1559-1573.
55. Lesens O, Deschenes M, Steben M, Belanger G, Tsoukas CM. Hepatitis C virus is related to progressive liver disease in human immunodeficiency virus-positive hemophiliacs and should be treated as an opportunistic infection. J Infect Dis 1999; 179:1254-1258.
56. Grabczewska E, Pawlowska M. Morphological liver changes of chronic hepatitis C in antiretroviral-naive HIV-infected patients. Przegl Epidemiol 2005; 59:423-430.
57. van Houwelingen HC, Arends LR, Stijnen T. Advanced methods in meta-analysis: multivariate approach and meta-regression. Stat Med 2002; 21:589-624.
58. AIlory Y, Charlotte F, Benhamou Y, Opolon P, Le Charpentier Y, Poynard T. Impact of human immunodeficiency virus infection on the histological features of chronic hepatitis C: a case-control study. The MULTIVIRC group. Hum Pathol 2000; 31:69-74.
59. Myers RP, Benhamou Y, Imbert-Bismut F, Thibault V, Bochet M, Charlotte F, et al. Serum biochemical markers accurately predict liver fibrosis in HIV and hepatitis C virus co-infected patients. AIDS 2003; 17:721-725.
60. Gaslightwala I, Bini EJ. Impact of human immunodeficiency virus infection on the prevalence and severity of steatosis in patients with chronic hepatitis C virus infection. J Hepatol 2006;44:1026-1032.
61. Gonzalez SA, Liu RC, Edlin BR, Jacobson IM, Talal AH. HIV/ hepatitis C virus-coinfected patients with normal alanine aminotransferase levels. J Acquir Immune Defic Syndr 2006; 41:582-589.
62. Macias J, Gíron-Gonzalez JA, Gonzalez-Serrano M, Merino D, Cano P, Mira JA, et al. Prediction of liver fibrosis in human immunodeficiency virus/hepatitis C virus coinfected patients by simple noninvasive indexes. Cut 2006; 55:409-414.
63. Merchante N, Macias J, Ramayo E, Vergara S, Garcia-Garcia JA, Mira JA, et al. Insulin resistance is not associated with liver fibrosis progression in HIV/hepatitis C virus-coinfected patients. J Viral Hepat 2006; 13:449-456.
64. Mira JA, Macias J, Giron-Gonzalez JA, Merino D, Gonzalez-Serrano M, Jimenez-Mejias ME, et al. Incidence of and risk factors for severe hepatotoxicity of nelfinavir-containing regimens among HIV-infected patients with chronic hepatitis C. J Antimicrob Chemother 2006; 58:140-146.
65. Monto A, Dove LM, Bostrom A, Kakar S, Tien PC, Wright TL. Hepatic steatosis in HIV/hepatitis C coinfection: prevalence and significance compared with hepatitis C monoinfection. Hepatology 2005; 42:310-316.
66. Quereda C, Moreno S, Moreno L, Moreno A, Garca-Sanmiguel L, Perez-Elas MJ, et al. The role of liver biopsy in the management of chronic hepatitis C in patients infected with the human immunodeficiency virus. Hum Pathol 2004; 35:1083-1087.
67. Rey D, Carrieri MP, Spire B, Loubiere S, Dellamonica P, Gallais H, et al. Factors associated with liver biopsy performance in HCV-HIV coinfected injecting drug users with HCV viremia: results from a five-year longitudinal assessment. J Urban Health 2004; 81:48-57.
68. Sanchez-Conde M, Berenguer J, Mirai les P, Alvarez F, Carlos Lopez J, Cosin J, et al. Liver biopsy findings for HIV-infected patients with chronic hepatitis C and persistently normal levels of alanine aminotransferase. Clin Infect Dis 2006; 43:640-644.
69. Trimoulet P, Neau D, Le Bail B, Rullier A, Winnock M, Galperine T, et al. Intrahepatic HCV RNA loads in 37 HIV-HCV co-infected patients with controlled HIV infection. J Med Virol 2002; 67:143-151.
70. Uberti-Foppa C, De Bona A, Galli L, Sitia G, Gallotta G, Sagnelli C, et al. Liver fibrosis in HIV-positive patients with hepatitis C virus: role of persistently normal alanine aminotransferase levels. J Acquir Immune Defic Syndr 2006; 41:63-67.
71. Vergara S, Macias J, Mira JA, Garcia-Garcia JA, Merchante N, del Valle J, et al. Low-level liver enzyme elevations during HAART are not associated with liver fibrosis progression among HIV/HCV-coinfected patients. J Antimicrob Chemother 2007;59:87-91.
72. Vincent T, Portales P, Baillat V, de Boever CM, Le Moing V, Vidal M, et al. T-cell surface CCR5 density is not correlated with hepatitis severity in hepatitis C virus/HIV-coinfected individuals: implications for the therapeutic use of CCR5 antagonists. J Acquir Immune Defic Syndr 2005; 38:305-309.
73. Rodriguez-Torres M, Rios-Bedoya CF, Rodriguez-Orengo J, Fernandez-Carbia A, Marxuach-Cuetara AM, Lopez-Torres A, et al. Progression to cirrhosis in Latinos with chronic hepatitis C: differences in Puerto Ricans with and without human immunodeficiency virus coinfection and along gender. J Clin Gastroenterol 2006; 40:358-366.
74. Romeo R, Rumi MG, Donato MF, Cargnel MA, Vigano P, Mondelli M, et al. Hepatitis C is more severe in drug users with human immunodeficiency virus infection. J Viral Hepat 2000; 7:297-301.
75. Sarmento-Castro R, Horta A, Vasconcelos O, Coelho H, Mendez J, Tavares AP, et al. Impact of peginterferon alpha-2b and ribavirin treatment on liver tissue in patients with HCV or HCV-HIV co-infection. J Infect 2007; 54:609-616.
76. Serfaty L, Costagliola D, Wendum D, Picard O, Meyohas MC, Girard PM, et al. Impact of early-untreated HIV infection on chronic hepatitis C in intravenous drug users: a case-control study. AIDS 2001; 15:2011-2016.
77. Valle Tovo C, Alves de Mattos A, Ribeiro de Souza A, Ferrari de Oliveira Rigo J, Lerias de Almeida PR, Galperim B, et al. Impact of human immunodeficiency virus infection in patients infected with the hepatitis C virus. Liver Int 2007; 27:40-46.
78. Freeman AJ, Dore GJ, Law MG, Thorpe M, Von Overbeck J, Lloyd AR, et al. Estimating progression to cirrhosis in chronic hepatitis C virus infection. Hepatology 2001; 34:809-816.
79. Canchis PW, Yee HT, Fiel MI, Dieterich DT, Liu R-C, Chiriboga L, et al. Intrahepatic CD4+ cell depletion in hepatitis C virus/ HlV-coinfected patients. J Acquir Immune Defic Syndr 2004; 37:1125-1131.
80. Schmid CH, Stark PC, Berlin JA, Landais P, Lau J. Meta-regression detected associations between heterogeneous treatment effects and study-level, but not patient-level, factors. J Clin Epidemiol 2004; 57:683-697.
81. Sulkowski MS, Mast EE, Seeff LB, Thomas DL. Hepatitis C virus infection as an opportunistic disease in persons infected with human immunodeficiency virus. Clin Infect Dis 2000; 30 (Suppl 1):S77-S84.
82. Thomas DL. Hepatitis C and human immunodeficiency virus infection. Hepatology 2002; 36:S201-S209.
83. Sulkowski MS, Thomas DL, Mehta SH, Chaisson RE, Moore RD. Hepatotoxicity associated with nevirapine or efavirenz-containing antiretroviral therapy: role of hepatitis C and B infections. Hepatology 2002; 35:182-189.
84. Koopman L, van der Heijden GJ, Grobbee DE, Rovers MM. Comparison of methods of handling missing data in individual patient data meta-analyses: an empirical example on antibiotics in children with acute otitis media. Am J Epidemiol 2008; 167:540-545.