The Korean journal of internal medicine

The Korean Association of Internal Medicine (대한내과학회)
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Hepatitis C virus infection in chronic kidney disease: paradigm shift in management

  • Kim, So Mi (Division of Nephrology, Department of Internal Medicine, Dankook University Hospital) ;
  • Song, Il Han (Division of Hepatology, Department of Internal Medicine, Dankook University Hospital)
  • Received : 2018.06.11
  • Accepted : 2018.06.17
  • Published : 2018.07.01
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Abstract

Hepatitis C virus (HCV) infection in chronic kidney disease (CKD) is associated with increased liver-related morbidity and mortality rates, accelerated progression to end-stage renal disease, and risk of cardiovascular events. CKD patients with HCV infection require antiviral therapy. Pegylated interferon (peg-IFN) plus ribavirin was the standard of care for HCV-infected CKD patients before the introduction of first-generation direct-acting antiviral (DAA) oral anti-HCV agents. Peg-IFN-based treatment has a low virologic response rate and poor compliance, resulting in a high dropout rate. Recently, several clinical trials of all-DAA combination regimens have reported excellent antiviral efficacy and few adverse drug reactions in HCV-infected patients with CKD. These positive results have revolutionized the treatment of chronic HCV infection in this population. In this review, we address the impact of chronic HCV infection in CKD patients, and discuss their management using next-generation DAAs.

Keywords

Acknowledgement

Supported by : Dankook University

References

  1. Thrift AP, El-Serag HB, Kanwal F. Global epidemiology and burden of HCV infection and HCV-related disease. Nat Rev Gastroenterol Hepatol 2017;14:122-132. https://doi.org/10.1038/nrgastro.2016.176
  2. Mohd Hanafiah K, Groeger J, Flaxman AD, Wiersma ST. Global epidemiology of hepatitis C virus infection: new estimates of age-specific antibody to HCV seroprevalence. Hepatology 2013;57:1333-1342. https://doi.org/10.1002/hep.26141
  3. Cacoub P, Poynard T, Ghillani P, et al. Extrahepatic manifestations of chronic hepatitis C. MULTIVIRC Group. Multidepartment virus C. Arthritis Rheum 1999;42:2204-2212. https://doi.org/10.1002/1529-0131(199910)42:10<2204::AID-ANR24>3.0.CO;2-D
  4. Cacoub P, Gragnani L, Comarmond C, Zignego AL. Extrahepatic manifestations of chronic hepatitis C virus infection. Dig Liver Dis 2014;46 Suppl 5:S165-S173. https://doi.org/10.1016/j.dld.2014.10.005
  5. Cacoub P, Comarmond C, Domont F, Savey L, Desbois AC, Saadoun D. Extrahepatic manifestations of chronic hepatitis C virus infection. Ther Adv Infect Dis 2016;3:3-14.
  6. Fabrizi F, Verdesca S, Messa P, Martin P. Hepatitis C virus infection increases the risk of developing chronic kidney disease: a systematic review and meta-analysis. Dig Dis Sci 2015;60:3801-3813. https://doi.org/10.1007/s10620-015-3801-y
  7. Park H, Adeyemi A, Henry L, Stepanova M, Younossi Z. A meta-analytic assessment of the risk of chronic kidney disease in patients with chronic hepatitis C virus infection. J Viral Hepat 2015;22:897-905. https://doi.org/10.1111/jvh.12413
  8. Park H, Chen C, Wang W, Henry L, Cook RL, Nelson DR. Chronic hepatitis C virus (HCV) increases the risk of chronic kidney disease (CKD) while effective HCV treatment decreases the incidence of CKD. Hepatology 2017 Sep 5 [Epub]. https://doi.org/10.1002/hep.29505.
  9. Bang BK, Choi BS, Kim HW, et al. Retrospective study on the impact of hepatitis B and hepatitis C virus infection on renal transplnat recipients over 15 years. Korean J Nephrol 2002;21:423-434.
  10. Fabrizi F, Martin P, Dixit V, Messa P. Meta-analysis of observational studies: hepatitis C and survival after renal transplant. J Viral Hepat 2014;21:314-324. https://doi.org/10.1111/jvh.12148
  11. Scott DR, Wong JK, Spicer TS, et al. Adverse impact of hepatitis C virus infection on renal replacement therapy and renal transplant patients in Australia and New Zealand. Transplantation 2010;90:1165-1171. https://doi.org/10.1097/TP.0b013e3181f92548
  12. Fried MW. Side effects of therapy of hepatitis C and their management. Hepatology 2002;36(5 Suppl 1):S237-S244.
  13. Rostaing L, Chatelut E, Payen JL, et al. Pharmacokinetics of alphaIFN-2b in chronic hepatitis C virus patients undergoing chronic hemodialysis or with normal renal function: clinical implications. J Am Soc Nephrol 1998;9:2344-2348.
  14. Lee JJ, Lin MY, Chang JS, et al. Hepatitis C virus infection increases risk of developing end-stage renal disease using competing risk analysis. PLoS One 2014;9:e100790. https://doi.org/10.1371/journal.pone.0100790
  15. Chen YC, Lin HY, Li CY, Lee MS, Su YC. A nationwide cohort study suggests that hepatitis C virus infection is associated with increased risk of chronic kidney disease. Kidney Int 2014;85:1200-1207. https://doi.org/10.1038/ki.2013.455
  16. Bose SK, Ray R. Hepatitis C virus infection and insulin resistance. World J Diabetes 2014;5:52-58. https://doi.org/10.4239/wjd.v5.i1.52
  17. Fabrizi F, Martin P, Dixit V, Bunnapradist S, Kanwal F, Dulai G. Post-transplant diabetes mellitus and HCV seropositive status after renal transplantation: meta-analysis of clinical studies. Am J Transplant 2005;5:2433-2440. https://doi.org/10.1111/j.1600-6143.2005.01040.x
  18. Villar LM, Caldas GC, Scalioni LP, et al. High prevalence of insulin resistance among Brazilian chronic hepatitis C patients. Arch Endocrinol Metab 2017;61:628-632. https://doi.org/10.1590/2359-3997000000315
  19. Kawaguchi T, Yoshida T, Harada M, et al. Hepatitis C virus down-regulates insulin receptor substrates 1 and 2 through up-regulation of suppressor of cytokine signaling 3. Am J Pathol 2004;165:1499-1508. https://doi.org/10.1016/S0002-9440(10)63408-6
  20. Bose SK, Shrivastava S, Meyer K, Ray RB, Ray R. Hepatitis C virus activates the mTOR/S6K1 signaling pathway in inhibiting IRS-1 function for insulin resistance. J Virol 2012;86:6315-6322. https://doi.org/10.1128/JVI.00050-12
  21. Horita S, Nakamura M, Suzuki M, et al. The role of renal proximal tubule transport in the regulation of blood pressure. Kidney Res Clin Pract 2017;36:12-21. https://doi.org/10.23876/j.krcp.2017.36.1.12
  22. Olson AL, Knight JB. Regulation of GLUT4 expression in vivo and in vitro. Front Biosci 2003;8:s401-s409. https://doi.org/10.2741/1072
  23. Sciacqua A, Perticone M, Tassone EJ, et al. Renal function is impaired in normotensive chronic HCV patients: role of insulin resistance. Intern Emerg Med 2016;11:553-559. https://doi.org/10.1007/s11739-015-1349-7
  24. Schamberg NJ, Lake-Bakaar GV. Hepatitis C virus-related mixed cryoglobulinemia: pathogenesis, clinica manifestations, and new therapies. Gastroenterol Hepatol (N Y) 2007;3:695-703.
  25. Curry MP, Golden-Mason L, Doherty DG, et al. Expansion of innate CD5pos B cells expressing high levels of CD81 in hepatitis C virus infected liver. J Hepatol 2003;38:642-650.
  26. Ozkok A, Yildiz A. Hepatitis C virus associated glomerulopathies. World J Gastroenterol 2014;20:7544-7554. https://doi.org/10.3748/wjg.v20.i24.7544
  27. Baid S, Pascual M, Williams WW Jr, et al. Renal thrombotic microangiopathy associated with anticardiolipin antibodies in hepatitis C-positive renal allograft recipients. J Am Soc Nephrol 1999;10:146-153.
  28. Markowitz GS, Cheng JT, Colvin RB, Trebbin WM, D'Agati VD. Hepatitis C viral infection is associated with fibrillary glomerulonephritis and immunotactoid glomerulopathy. J Am Soc Nephrol 1998;9:2244-2252.
  29. Roccatello D, Fornasieri A, Giachino O, et al. Multicenter study on hepatitis C virus-related cryoglobulinemic glomerulonephritis. Am J Kidney Dis 2007;49:69-82. https://doi.org/10.1053/j.ajkd.2006.09.015
  30. El-Serag HB, Hampel H, Yeh C, Rabeneck L. Extrahepatic manifestations of hepatitis C among United States male veterans. Hepatology 2002;36:1439-1445. https://doi.org/10.1002/hep.1840360621
  31. Liangpunsakul S, Chalasani N. Relationship between hepatitis C and microalbuminuria: results from the NHANES III. Kidney Int 2005;67:285-290. https://doi.org/10.1111/j.1523-1755.2005.00080.x
  32. Fissell RB, Bragg-Gresham JL, Woods JD, et al. Patterns of hepatitis C prevalence and seroconversion in hemodialysis units from three continents: the DOPPS. Kidney Int 2004;65:2335-2342. https://doi.org/10.1111/j.1523-1755.2004.00649.x
  33. Johnson DW, Dent H, Yao Q, et al. Frequencies of hepatitis B and C infections among haemodialysis and peritoneal dialysis patients in Asia-Pacific countries: analysis of registry data. Nephrol Dial Transplant 2009;24:1598-1603. https://doi.org/10.1093/ndt/gfn684
  34. Finelli L, Miller JT, Tokars JI, Alter MJ, Arduino MJ. National surveillance of dialysis-associated diseases in the United States, 2002. Semin Dial 2005;18:52-61. https://doi.org/10.1111/j.1525-139X.2005.18108.x
  35. Park HC, Lee YK, Yoo KD, et al. Korean clinical practice guidelines for preventing the transmission of infections in hemodialysis facilities. Kidney Res Clin Pract 2018;37:8-19. https://doi.org/10.23876/j.krcp.2018.37.1.8
  36. Karkar A. Infection control guidelines in hemodialysis facilities. Kidney Res Clin Pract 2018;37:1-3. https://doi.org/10.23876/j.krcp.2018.37.1.1
  37. Nakayama E, Akiba T, Marumo F, Sato C. Prognosis of anti-hepatitis C virus antibody-positive patients on regular hemodialysis therapy. J Am Soc Nephrol 2000;11:1896-1902.
  38. Kalantar-Zadeh K, Kilpatrick RD, McAllister CJ, et al. Hepatitis C virus and death risk in hemodialysis patients. J Am Soc Nephrol 2007;18:1584-1593. https://doi.org/10.1681/ASN.2006070736
  39. Goodkin DA, Bieber B, Jadoul M, Martin P, Kanda E, Pisoni RL. Mortality, hospitalization, and quality of life among patients with hepatitis C infection on hemodialysis. Clin J Am Soc Nephrol 2017;12:287-297. https://doi.org/10.2215/CJN.07940716
  40. Pereira BJ, Levey AS. Hepatitis C virus infection in dialysis and renal transplantation. Kidney Int 1997;51:981-999. https://doi.org/10.1038/ki.1997.139
  41. Kasiske BL, Snyder JJ, Gilbertson D, Matas AJ. Diabetes mellitus after kidney transplantation in the United States. Am J Transplant 2003;3:178-185. https://doi.org/10.1034/j.1600-6143.2003.00010.x
  42. Choi YK, Kim YJ, Choi NK, et al. Risk factors for new onset diabetes after transplantation among renal transplant recipients treated with tacrolimus. Korean J Nephrol 2010;29:761-767.
  43. Peev V, Reiser J, Alachkar N. Diabetes mellitus in the transplanted kidney. Front Endocrinol (Lausanne) 2014;5:141.
  44. Rodrigo E, Fernandez-Fresnedo G, Valero R, et al. Newonset diabetes after kidney transplantation: risk factors. J Am Soc Nephrol 2006;17(12 Suppl 3):S291-S295. https://doi.org/10.1681/ASN.2006080929
  45. Davidson J, Wilkinson A, Dantal J, et al. New-onset diabetes after transplantation: 2003 International consensus guidelines. Proceedings of an international expert panel meeting. Barcelona, Spain, 19 February 2003. Transplantation 2003;75(10 Suppl):SS3-SS24.
  46. Hammoud H, Haem J, Laurent B, et al. Glomerular disease during HCV infection in renal transplantation. Nephrol Dial Transplant 1996;11 Suppl 4:54-55.
  47. Cruzado JM, Gil-Vernet S, Ercilla G, et al. Hepatitis C virus-associated membranoproliferative glomerulonephritis in renal allografts. J Am Soc Nephrol 1996;7:2469-2475.
  48. Cosio FG, Cattran DC. Recent advances in our understanding of recurrent primary glomerulonephritis after kidney transplantation. Kidney Int 2017;91:304-314. https://doi.org/10.1016/j.kint.2016.08.030
  49. Rendina M, Schena A, Castellaneta NM, et al. The treatment of chronic hepatitis C with peginterferon alfa-2a (40 kDa) plus ribavirin in haemodialysed patients awaiting renal transplant. J Hepatol 2007;46:768-774. https://doi.org/10.1016/j.jhep.2006.12.016
  50. Liu CH, Huang CF, Liu CJ, et al. Pegylated interferon-${\alpha}2a$ with or without low-dose ribavirin for treatment-naive patients with hepatitis C virus genotype 1 receiving hemodialysis: a randomized trial. Ann Intern Med 2013;159:729-738. https://doi.org/10.7326/0003-4819-159-11-201312030-00005
  51. Liu CH, Liu CJ, Huang CF, et al. Peginterferon alfa-2a with or without low-dose ribavirin for treatment-naive patients with hepatitis C virus genotype 2 receiving haemodialysis: a randomised trial. Gut 2015;64:303-311. https://doi.org/10.1136/gutjnl-2014-307080
  52. Fabrizi F, Dixit V, Messa P, Martin P. Antiviral therapy (pegylated interferon and ribavirin) of hepatitis C in dialysis patients: meta-analysis of clinical studies. J Viral Hepat 2014;21:681-689. https://doi.org/10.1111/jvh.12276
  53. Mehawej M, Rostaing L, Alric L, Del Bello A, Izopet J, Kamar N. Boceprevir-based triple antiviral therapy for chronic hepatitis c virus infection in kidney-transplant candidates. J Transplant 2015;2015:159795.
  54. Kaya S, Aksoz S, Baysal B, Ay N, Danis R. Evaluation of telaprevir-containing triple therapy in the treatment of chronic hepatitis C in hemodialysed patients. Infect Dis (Lond) 2015;47:658-661. https://doi.org/10.3109/23744235.2015.1034769
  55. Dumortier J, Guillaud O, Gagnieu MC, et al. Anti-viral triple therapy with telaprevir in haemodialysed HCV patients: is it feasible? J Clin Virol 2013;56:146-149. https://doi.org/10.1016/j.jcv.2012.10.009
  56. Roth D, Nelson DR, Bruchfeld A, et al. Grazoprevir plus elbasvir in treatment-naive and treatment-experienced patients with hepatitis C virus genotype 1 infection and stage 4-5 chronic kidney disease (the C-SURFER study): a combination phase 3 study. Lancet 2015;386:1537-1545. https://doi.org/10.1016/S0140-6736(15)00349-9
  57. Saxena V, Koraishy FM, Sise ME, et al. Safety and efficacy of sofosbuvir-containing regimens in hepatitis C-infected patients with impaired renal function. Liver Int 2016;36:807-816. https://doi.org/10.1111/liv.13102
  58. Pockros PJ, Reddy KR, Mantry PS, et al. Efficacy of direct-acting antiviral combination for patients with hepatitis C virus genotype 1 infection and severe renal impairment or end-stage renal disease. Gastroenterology 2016;150:1590-1598. https://doi.org/10.1053/j.gastro.2016.02.078
  59. Gane E, Lawitz E, Pugatch D, et al. Glecaprevir and pibrentasvir in patients with HCV and severe renal impairment. N Engl J Med 2017;377:1448-1455. https://doi.org/10.1056/NEJMoa1704053
  60. Reau N, Kwo PY, Rhee S, et al. Glecaprevir/pibrentasvir treatment in liver or kidney transplant patients with hepatitis C virus infection. Hepatology 2018 Apr 19 [Epub]. https://doi.org/10.1002/hep.30046.

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