Ribavirin-induced anemia in hepatitis C virus patients undergoing combination therapy

PLoS Computational Biology

Volumn 7, Issue 2, 2011, Pages

  Krishnan, Sheeja M ^a   Dixit, Narendra M ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDES; ANTIBIOTICS; BLOOD; ESTIMATION; GLYCOPROTEINS; PATIENT MONITORING; PATIENT TREATMENT; VIRUSES;

% REDUCTIONS; 'CURRENT; COMBINATION THERAPY; HEPATITIS C VIRUS; LIFESPANS; MODEL PREDICTION; RIBAVIRIN; STANDARD OF CARES; TREATMENT RESPONSE; VIRUS INFECTION;

INTERFERONS;

ERYTHROPOIETIN; HEMOGLOBIN; RIBAVIRIN; ALPHA2A INTERFERON; ALPHA2B INTERFERON; ANTIVIRUS AGENT; MACROGOL DERIVATIVE; PEGINTERFERON ALPHA2A; PEGINTERFERON ALPHA2B;

ADVERSE DRUG REACTION; ANEMIA; ARTICLE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DISEASE SEVERITY; DOSE RESPONSE; DRUG ACCUMULATION; DRUG DOSE REDUCTION; DRUG RESPONSE; ERYTHROCYTE KINETICS; ERYTHROCYTE LIFESPAN; ERYTHROPOIESIS; HEPATITIS C; HUMAN; MATHEMATICAL MODEL; POPULATION DYNAMICS; PREDICTION; PROGNOSIS; QUANTITATIVE ANALYSIS; BIOLOGICAL MODEL; BIOLOGY; BLOOD; CHEMICALLY INDUCED DISORDER; DRUG COMBINATION; DRUG EFFECT; HEMOLYTIC ANEMIA; MATHEMATICAL PHENOMENA;

HEPATITIS C VIRUS;

ANEMIA, HEMOLYTIC; ANTIVIRAL AGENTS; COMPUTATIONAL BIOLOGY; DRUG THERAPY, COMBINATION; ERYTHROCYTE AGING; HEPATITIS C; HUMANS; INTERFERON ALFA-2A; INTERFERON ALFA-2B; MATHEMATICAL CONCEPTS; MODELS, BIOLOGICAL; POLYETHYLENE GLYCOLS; RIBAVIRIN;

EID: 79952460602     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1001072     Document Type: Article

References (67)

1. Lavanchy D, (2009) The global burden of hepatitis C. Liver Int 29: 74-81.
2. Ghany MG, Strader DB, Thomas DL, Seeff LB, (2009) Diagnosis, management, and treatment of hepatitis C: An update. Hepatology 49: 1335-1374.
3. Dusheiko G, Main J, Thomas H, Reichard O, Lee C, et al. (1996) Ribavirin treatment for patients with chronic hepatitis C: results of a placebo-controlled study. J Hepatol 25: 591-598.
4. Bodenheimer HC, Lindsay KL, Davis GL, Lewis JH, Thung SN, et al. (1997) Tolerance and efficacy of oral ribavirin treatment of chronic hepatitis C: A multicenter trial. Hepatology 26: 473-477.
5. Zoulim F, Haem J, Ahmed SS, Chossegros P, Habersetzer F, et al. (1998) Ribavirin monotherapy in patients with chronic hepatitis C: a retrospective study of 95 patients. J Viral Hepat 5: 193-198.
6. Pawlotsky JM, Dahari H, Neumann AU, Hezode C, Germanidis G, et al. (2004) Antiviral action of ribavirin in chronic hepatitis C. Gastroenterology 126: 703-714.
7. Manns MP, McHutchison JG, Gordon SC, Rustgi VK, Shiffman M, et al. (2001) Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet 358: 958-965.
8. Fried MW, Shiffman ML, Reddy KR, Smith C, Marinos G, et al. (2002) Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med 347: 975-982.
9. McHutchison JG, Gordon SC, Schiff ER, Shiffman ML, Lee WM, et al. (1998) Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. N Engl J Med 339: 1485-1492.
10. Reichard O, Norkrans G, Fryden A, Braconier JH, Sonnerborg A, et al. (1998) Randomized, double-blind, placebo-controlled trial of interferon alpha-2b with and without ribavirin for chronic hepatitis C. Lancet 351: 83-87.
11. Poynard T, Marcellin P, Lee SS, Niederau C, Minuk GS, et al. (1998) Randomized trial of interferon alpha2b plus ribavirin for 48 weeks or for 24 weeks versus interferon alpha2b plus placebo for 48 weeks for treatment of chronic infection with hepatitis C virus. Lancet 352: 1426-1432.
12. Franceschi LD, Fattovich G, Turrini F, Brugnara C, Manzato F, et al. (2000) Hemolytic anemia induced by ribavirin therapy in patients with chronic hepatitis C virus infection: Role of membrane oxidative damage. Hepatology 31: 997-1004.
13. Sulkowski MS, (2003) Anemia in the treatment of hepatitis C virus Infection. Clin Infect Dis 37: s315-322.
14. Reddy KR, Shiffman ML, Morgan TR, Zeuzem S, Hadziyannis S, et al. (2007) Impact of ribavirin dose reductions in hepatitis C virus genotype 1 patients completing peginterferon alfa-2a/ribavirin treatment. Clin Gastroenterol Hepatol 5: 124-129.
15. Sulkowski MS, Wasserman R, Brooks L, Ball L, Gish R, (2004) Changes in haemoglobin during interferon alpha-2b plus ribavirin combination therapy for chronic hepatitis C virus infection. J Viral Hepat 11: 243-250.
16. Reddy KR, Nelson DR, Zeuzem S, (2009) Ribavirin: Current role in the optimal clinical management of chronic hepatitis C. J Hepatol 50: 402-411.
17. Hazode C, Forestier N, Dusheiko G, Ferenci P, Pol S, et al. (2009) Telaprevir and peginterferon with or without ribavirin for chronic HCV infection. N Engl J Med 360: 1839-1850.
18. Lemon SM, McKeating JA, Pietschmann T, Frick DN, Glenn JS, et al. (2010) Development of novel therapies for hepatitis C. Antivir Res 86: 79-92.
19. Zeuzem S, (2008) Interferon-based therapy for chronic hepatitis C: current and future perspectives. Nat Clin Pract Gastroenterol Hepatol 5: 610-622.
20. Jain MK, Zoellner C, (2010) Role of ribavirin in HCV treatment response: now and in the future. Expert Opin Pharmaco 11: 673-683.
21. Landaverde C, Saab S, (2009) Optimizing peginterferon and ribavirin administration in difficult-to-treat patient populations. Curr Hepatitis Rep 8: 43-51.
22. Morello J, Rodriguez-Novoa S, Jimenez-Nacher I, Soriano V, (2008) Usefulness of monitoring ribavirin plasma concentrations to improve treatment response in patients with chronic hepatitis C. J Antimicrob Chemother 62: 1174-1180.
23. Schmid M, Kreil A, Jessner W, Homoncik M, Datz C, et al. (2005) Suppression of haematopoiesis during therapy of chronic hepatitis C with different interferon alpha mono and combination therapy regimens. Gut 54: 1014-1020.
24. Tod M, Farcy-Afif M, Stocco J, Boyer N, Bouton VR, et al. (2005) Pharmacokinetic/pharmacodynamic and time-to-event models of ribavirin-induced anaemia in chronic hepatitis C. Clin Pharmacokinet 44: 417-428.
25. DebRoy S, Kribs-Zaleta C, Mubayi A, Cardona-Meléndez GM, Medina-Rios L, et al. (2010) Evaluating treatment of hepatitis C for hemolytic anemia management. Math Biosci 225: 141-155.
26. Dieterich DT, Wasserman R, Brau N, Hassanein TI, Bini EJ, et al. (2003) Once-weekly epoetin alfa improves anemia and facilitates maintenance of ribavirin dosing in hepatitis C virus-infected patients receiving ribavirin plus interferon alfa. Am J Gastroenterol 98: 2491-2499.
27. Afdhal NH, Dieterich DT, Pockros PJ, Schiff ER, Shiffman ML, et al. (2004) Epoetin alfa maintains ribavirin dose in HCV-infected patients: a prospective, double-blind, randomized controlled study. Gastroenterology 126: 1302-1311.
28. Rio RAD, Post AB, Singer ME, (2006) Cost-effectiveness of hematologic growth factors for anemia occurring during hepatitis C combination therapy. Hepatology 44: 1598-1606.
29. Homoncik M, Sieghart W, Formann E, Schmid M, Ferenci P, et al. (2006) Erythropoietin treatment is associated with more severe thrombocytopenia in patients with chronic hepatitis C undergoing antiviral therapy. Amer J Gastroenterol 101: 2275-2282.
30. Shiffman ML, Salvatore J, Hubbard S, Price A, Sterling RK, et al. (2007) Treatment of chronic hepatitis C virus genotype 1 with peginterferon, ribavirin, and epoetin alpha. Hepatology 46: 371-379.
31. Falasca F, Ucciferri C, Mancino P, Gorgoretti V, Pizzigallo E, et al. (2010) Use of epoetin beta during combination therapy of infection with hepatitis c virus with ribavirin improves a sustained viral response. J Med Virol 82: 49-56.
32. Feld JJ, Hoofnagle JH, (2005) Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436: 967-972.
33. Parker WB, (2005) Metabolism and antiviral activity of ribavirin. Virus Res 107: 165-171.
34. Dixit NM, Perelson AS, (2006) The metabolism, pharmacokinetics and mechanisms of antiviral activity of ribavirin against hepatitis C virus. Cell Mol Life Sci 63: 832-842.
35. Neumann AU, Lam NP, Dahari H, Gretch DR, Wiley TE, et al. (1998) Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-alpha therapy. Science 282: 103-107.
36. Herrmann E, Lee JH, Marinos G, Modi M, Zeuzem S, (2003) Effect of ribavirin on hepatitis C viral kinetics in patients treated with pegylated interferon. Hepatology 37: 1351-1358.
37. Colombatto P, Civitano L, Oliveri F, Coco B, Ciccorossi P, et al. (2003) Sustained response to interferon-ribavirin combination therapy predicted by a model of hepatitis C virus dynamics using both HCV RNA and alanine aminotransferase. Antivir Ther 8: 519-530.
38. Dixit NM, Layden-Almer JE, Layden TJ, Perelson AS, (2004) Modelling how ribavirin improves interferon response rates in hepatitis C virus infection. Nature 432: 922-924.
39. Dahari H, Ribeiro RM, Perelson AS, (2007) Triphasic decline of hepatitis C virus RNA during antiviral therapy. Hepatology 46: 16-21.
40. Dixit NM, (2008) Advances in the mathematical modelling of hepatitis C virus dynamics. J Indian I Sci 88: 37-43.
41. Rong L, Dahari H, Ribeiro RM, Perelson AS, (2010) Rapid emergence of protease inhibitor resistance in hepatitis C virus. Sci Transl Med 2: 30ra32.
42. Rong L, Perelson AS, (2010) Treatment of hepatitis C virus infection with interferon and small molecule direct antivirals: viral kinetics and modeling. Crit Rev Immunol 30: 131-148.
43. Vlierberghe HV, Delanghe JR, Vos MD, Leroux-Roel G, (2001) Factors influencing ribavirin-induced hemolysis. J Hepatol 34: 911-916.
44. Takaki S, Tsubota A, Hosaka T, Akuta N, Someya T, et al. (2004) Factors contributing to ribavirin dose reduction due to anemia during interferon alfa2b and ribavirin combination therapy for chronic hepatitis C. J Gastroenterol 39: 668-673.
45. Balan V, Schwartz D, Wu GY, Muir AJ, Ghalib R, et al. (2005) Erythropoietic response to anemia in chronic hepatitis C patients receiving combination pegylated interferon/ribavirin. Am J Gastroenterol 100: 299-307.
46. Donnerer J, Grahovic M, Stelzl E, Kessler HH, Bankuti C, et al. (2006) Ribavirin levels and haemoglobin decline in early virological responders and non-responders to hepatitis C virus combination therapy. Pharmacology 76: 136-140.
47. Inoue Y, Hommaa M, Matsuzaki Y, Shibata M, Matsumura T, et al. (2006) Erythrocyte ribavirin concentration for assessing hemoglobin reduction in interferon and ribavirin combination therapy. Hepatol Res 34: 23-27.
48. Glue P, (1999) The clinical pharmacology of ribavirin. Semin Liv Dis 19: 17-24.
49. Krishnan SM, Dixit NM, (2009) Estimation of red blood cell lifespan from alveolar carbon monoxide measurements. Transl Res 154: 15-17.
50. Virtue MA, Furne JK, Ho SB, Levitt MD, (2004) Use of alveolar carbon monoxide to measure the effect of ribavirin on red blood cell survival. Am J Hematol 76: 107-113.
51. Fellay J, Thompson AJ, Ge D, Gumbs CE, Urban TJ, et al. (2010) ITPA gene variants protect against anaemia in patients treated for chronic hepatitis C. Nature 464: 405-408.
52. Preston SL, Drusano GL, Glue P, Nash J, Gupta SK, et al. (1999) Pharmacokinetics and absolute bioavailability of ribavirin in healthy volunteers as determined by stable-isotope methodology. Antimicrob Agents Chemother 43: 2451-2456.
53. Endres CJ, Moss AM, Ke B, Govindarajan R, Choi DS, et al. (2009) The role of the equilibrative nucleoside transporter 1 (ENT1) in transport and metabolism of ribavirin by human and wild-type or Ent1-/- mouse erythrocytes. J Pharmacol Exp Ther 329: 387-398.
54. McHutchison JG, Manns MP, Brown RS, Reddy KR, Shiffman ML, et al. (2007) Strategies for managing anemia in hepatitis C patients undergoing antiviral therapy. Am J Gastroenterol 102: 880-889.
55. Mangoni ED, Marrone A, Saviano D, Del Vecchio C, Utili R, et al. (2003) Normal erythropoietin response in chronic hepatitis C patients with ribavirin-induced anemia. Antivir Ther 8: 57-63.
56. Glue P, Rouzier-Panis R, Raffanel C, Sabo R, Gupta SK, et al. (2000) A dose-ranging study of pegylated interferon alfa-2b and ribavirin in chronic hepatitis C. Hepatology 32: 647-653.
57. Jarvis SM, Thorn JA, Glue P, (1998) Ribavirin uptake by human erythrocytes and the involvement of nitrobenzylthioinosine-sensitive (es)-nucleoside transporters. Br J Pharmacol 123: 1587-1592.
58. Spivak JL, (2000) The blood in systemic disorders. Lancet 355: 1707-1712.
59. Mahaffy JM, Belair J, Mackey MC, (1998) Hematopoietic model with moving boundary condition and state dependent delay: applications in erythropoiesis. J Theor Biol 190: 135-146.
60. Veng-Pederson P, Chapel S, Schmidt PRL, Al-Huniti NH, Cook RT, et al. (2002) An integrated pharmacodynamic analysis of erythropoietin, reticulocyte, and hemoglobin responses in acute anemia. Pharm Res 19: 1630-1635.
61. Colijn C, Mackey MC, (2005) A mathematical model of hematopoiesis-I. Periodic chronic myelogenous leukemia. J Theor Biol 237: 117-132.
62. Roeder I, (2006) Quantitative stem cell biology: computational studies in the hematopoietic system. Curr Opin Hematol 13: 222-228.
63. Crauste F, Pujo-Menjouet L, Génieys S, Molina C, Gandrillon O, (2008) Adding self-renewal in committed erythroid progenitors improves the biological relevance of a mathematical model of erythropoiesis. J Theor Biol 250: 322-338.
64. Krzyzanski W, Perez-Ruixo J, Vermeulen A, (2008) Basic pharmacodynamic models for agents that alter the lifespan distribution of natural cells. J Pharmacokinet Phar 35: 349-377.
65. Savill NJ, Chadwick W, Reece SE, (2009) Quantitative analysis of mechanisms that govern red blood cell age structure and dynamics during anaemia. PLoS Comput Biol 5: e1000416.
66. Berk PD, Berlin NI, Blaschke TF, Bloomer JR, Howe RB, (1972) Bilirubin production as a measure of red-cell life-span. J Lab Clin Med 79: 364-378.
67. Beck WS, (1991) Hematology. MIT Press, Cambridge, Massachusetts.