Liver retransplantation in the modern concept of treatment of its terminal pathology (literature review)

The work is devoted to the analysis of modern literature data and approaches in performing repeated liver transplantation. The most frequent causes of liver graft loss are PNFT, HAT, recurrent initial disease and chronic rejection. The leading indication for retransplantation in children is HAT. The one-year survival rate after retransplantation is approximately 75%. Reducing the cost of organ retransplantation and the cost-effectiveness of the procedure are controversial issues. Mathematical modeling has identified several significant recipient and donor factors affecting the outcomes of retransplantation. Despite ethical and economic considerations, retransplantation is the only option for transplant patients whose grafts have failed to engraft. The decision to retransplant should be made with some caution, with full multi-type approach in large multidisciplinary transplant centers.

1. 1 SRTR Annual Report 2009. Available at: http://www.srtr.org/annual_Reports/default.aspx. Accessed October 22, 2014.

2. 2 Azoulay D, Linhares M, Huguet E, et al. Decision for retransplantation of the liver: an experience- and cost-based analysis. Ann Surg. 2002;236:713-721.

3. 3 Busuttil RW, Farmer DG, Yersiz H, et al. Analysis of long-term outcomes of 3200 liver transplantations over two decades. A single center experience. Ann Surg. 2005 June;241(6):905-918.

4. 4 Organ Procurement and Transplantation Network. http://optn. transplant.hrsa.gov/latestData/rptData.asp. Accessed July 13, 2012.

5. 5 Kashyap R, Jain A, Reyes J, et al. Causes of retransplantation after primary liver transplantation in 4000 consecutive patients: 2 to 19 years follow-up. Transplant Proc. 2001;33:1486-1487.

6. 6 Marudanayagam R, Shanmugam V, Sandhu B, et al. Liver retransplantation in adults: a single centre, 25-year experience. HPB. 2010;12(3):217-224.

7. 7 Markmann J, Markowitz J, Yersiz H, et al. Long-term survival after retransplantation of the liver. Ann Surg. 1997;226:408-420.

8. 8 Strasberg SM, Howard TK, Molmenti EP, Hertl M. Selecting the donor liver: risk factors for poor function after orthotopic liver transplantation. Hepatology. 1994 Oct;20(4 Pt 1):829-838.

9. 9 Ploeg RJ, D'Alessandro AM, Knechtle SJ, et al. Risk factors for primary dysfunction after liver transplantation – a multivariate anal- ysis. Transplantation. 1993 Apr;55(4):807-813.

10. 10 Tector AJ, Mangus RS, Chestovich P, et al. Use of extended crite- ria livers decreases wait time for liver transplantation without Adversely Impacting Posttransplant Survival. Ann Surg. 2006 September;244(3):439-450.

11. 11 Silberhumer GR, Pokorny H, Hetz H, et al. Combination of extended donor criteria and changes in the model for end stage liver disease score predit patient survival and primary dysfunction in liver transplantation: a retrospective analysis. Transplantation. 2007;83(5):588-592.

12. 12 Amin MG, Wolf MP, TenBrook JA, et al. Expanded criteria donor grafts for deceased donor liver transplantation under the MELD system: a decision analysis. Liver Transpl. 2004;10(12):1468-1475.

13. 13 Biggins S, Beldecos A, Rabkin J, Rosen H. Retransplantation for hepatic allograft failure: prognostic modeling and ethical considerations. Liver Transpl. 2002;8:313-322.

14. 14 Bekker J, Ploem S, De Jong KP. Early hepatic artery thrombosis after liver transplantation: a systematic review of the incidence, outcome and risk factors. Am J Transplant. 2009;9(4):746-757.

15. 15 Freise CE, Gillespie BW, Koffron AJ, et al. Recipient morbidity after living and deceased donor liver transplantation: findings from the A2ALL Retrospective Cohort Study. Am J Transplant. 2008 Dec;8(12):2569-2579.

16. 16 Duffy JP, Hong JC, Farmer DG, et al. Vascular complications of orthotopic liver transplantation: experience in more than 4,200 patients. J Am Coll Surg. 2009 May;208(5):896-903.

17. 17 Feng S, Goodrich NP, Bragg-Gresham JL, et al. Characteristics associated with liver graft failure: the concept of a donor risk index. Am J Transplant. 2006 Apr;6(4):783-790.

18. 18 Olthoff KM, Merion RM, Ghobrial RM, et al. Outcomes of 385 adult-to-adult living donor liver transplant recipients: a report from the A2ALL Consortium. Ann Surg. 2005 Sep;242(3):314-323.

19. 19 Stevens LH, Emond JC, Piper JB, et al. Hepatic artery thrombosis in infants. A comparison of whole livers, reduced-size grafts, and grafts from living-related donors. Transplantation. 1992 Feb;53(2):396-399.

20. 20 Shakleton C, Goss J, Swenson K, et al. The impact of micro- surgical hepatic arterial reconstruction on the outcome of liver transplantation for congenital biliary atresia. Am J Surg. 1997;173:431-435.

21. 21 Stange B, Glanemann M, Nuessler N, et al. Hepatic artery throm- bosis after adult liver transplantation. Liver Transpl. 2003;9:612-620.

22. 22 Ackermann O, Branchereau S, Franchi-Abella S, et al. The long- term outcome of hepatic artery thrombosis after liver transplanta- tion in children: role of urgent revascularization. Am J Transplant. 2012;12(6):1496-1503.

23. 23 Grodzicki M, Anysz-Grodzicka A, Remiszewski P, et al. Treat- ment of early hepatic artery thrombosis after liver transplantation. Transplant Proc. 2011 Oct;43(8):3039-3042.

24. 24 Reference deleted during page review.

25. 25 Verna EC, Brown Jr RS. Hepatitis C and liver transplantation: enhancing outcomes and should patients be retransplanted. Clin Liver Dis. 2008 Aug;12(3):637-659.

26. 26 Rosen H. Retransplantation for hepatitis C: implications of different policies. Liver Transpl. 2000;6:S41-S46.

27. 27 Ghobrial R. Retransplantation for recurrent hepatitis C. Liver Transpl. 2002;8:S38-S43.

28. 28 Berenguer M, Prieto M, Palau A, et al. Severe recurrent hepatitis C after liver retransplantation for hepatitis C virus–related graft cirrhosis. Liver Transpl. 2003;9:228-235.

29. 29 Ghobrial R, Farmer D, Baquerizo A, et al. Orthotopic liver trans- plantation for hepatitis C: outcome, effect of immuno suppression, and causes of retransplantation during an 8-year single-center experience. Ann Surg. 1999;229:824-833.

30. 30 Ghobrial R, Colquhoun S, Rosen H, et al. Retransplantation for recurrent hepatitis C following tacrolimus or cyclosporine immu- nosuppression. Transplant Proc. 1998;30:1740-1741.

31. 31 Rosen H, Martin P. Hepatitis C infection in patients undergoing liver retransplantation. Transplantation. 1998;66:1612-1616.

32. 32 Jacobson IM, McHutchison JG, Dusheiko G, et al. Telaprevir for previously untreated chronic hepatitis C virus infection. N Engl J Med. 2011;364:2405-2416.

33. 33 Fontana RJ, Hughes EA, Appelman H, et al. A case report of suc- cessful peginterferon, ribavirin, and daclatasvir therapy for recurrent cholestatic hepatitis C following liver retransplantation. Liver Transpl. 2012;18(9):1053-1059.

34. 34 Schiano TD, Charlton M, Younossi Z, et al. Monoclonal antibody HCV-AbXTL68 in patients undergoing liver transplantation for HCV: Results of a phase 2 randomized study. Liver Transpl. 2006;12(9):1381-1389.

35. 35 Eason JD, Freeman Jr RB, Rohrer RJ, et al. Should liver transplantation be performed for patients with hepatitis B? Transplantation. 1994 Jun 15;57(11):1588-1593.

36. 36 Crespo G, Mariño Z, Navasa M, Forns X. Viral hepatitis in liver transplantation. Gastroenterology. 2012 May;142(6):1373-1383.

37. 37 Viral Hepatitis Surveillance – United States, 2010. Centers for Disease Control and Prevention. http://www.cdc.gov/hepatitis/Statistics/2010Surveillance/Commentary.htm

38. 38 Brock GN, Mostajabi F, Ferguson N, et al. Prophylaxis against de novo hepatitis B for liver transplantation utilizing hep B core (+) donors: does hepatitis B immunoglobulin provide a survival advantage? Transpl Int. 2011 Jun;24(6):570-581.

39. 39 Lucey MR. Liver transplantation in patients with alcoholic liver disease. Liver Transpl. 2011 Jul;17(7):751-759.

40. 40 Bravata D, Olkin I, Barnato A, et al. Employment and alcohol use after liver transplantation for alcoholic and nonalcoholic liver disease: A systematic review. Liver Transpl. 2001;7:191-203.

41. 41 Burra P, Mioni D, Cecchetto A, et al. Histological features after liver transplantation in alcoholic cirrhotics. J Hepatol. 2001;34(5): 716-722.

42. 42 Pageaux G, Michel J, Coste V, et al. Alcoholic cirrhosis is a good indication for liver transplantation, even for cases of recidivism. Gut. 1999;45:421-426.

43. 43 Burra P, Senzolo M, Adam R, et al. Liver transplantation for alco- holic liver disease in Europe: A study from the ELTR (European Liver Transplant Registry). Am J Transplant. 2010;10(1):138-148.

44. 44 Montano-Loza AJ, Mason AL, Ma M, et al. Risk factors for recurrence of autoimmune hepatitis after liver transplantation. Liver Transpl. 2009;15(10):1254-1261.

45. 45 Molmenti EP, Netto GJ, Murray NG, et al. Incidence and recurrence of autoimmune/alloimmune hepatitis in liver transplant recipients. Liver Transpl. 2002 Jun;8(6):519-526.

46. 46 Reich D, Fiel I, Guarrera J, et al. Liver transplantation for auto immune hepatitis. Hepatology. 2000;32:693-700.

47. 47 Trouillot TE, Shrestha R, Kam I, et al. Successful withdrawal of prednisone after adult liver transplantation for autoimmune hepatitis. Liver Transpl Surg. 1999;5:375-380.

48. 48 Shaw BW, Gordon RD, Iwatsuki S, et al. Hepatic retransplantation. Transplant Proc. 1985 Feb;17(1):264-271.

49. 49 Maguire D, Hart R, Heaton N, Rela M. A complication of infrarenal arterial conduit following orthotopic liver transplant. HPB (Oxford). 2001;3(4):275-277.

50. 50 Reese PP, Yeh H, Thomasson AM, et al. Transplant center volume and outcomes after liver retransplantation. Am J Transplant. 2009;9(2):309-317.

51. 51 Thuluvath PJ, Guidinger MK, Fung JJ, et al. Liver transplantation in the United States, 1999-2008. Am J Transpl. 2010;10(Part 2): 1003-1019.

52. 52 Akpinar E, Selvaggi G, Levi D, et al. Liver retransplantation of more than two grafts for recurrent failure. Transplantation. 2009; 88(7):884-890.

53. 53 Ghabril M, Dickson R, Wiesner R. Improving outcomes of liver retransplantation: an analysis of trends and the impact of hepatitis C infection. Am J Transpl. 2008;8:404-411.

54. 54 Hong JC, Kaldas FM, Kositamongkol P, et al. Predictive index for long-term survival after retransplantation of the liver in adult recipients. Ann Surg. 2011;254(3):444-449.

55. 55 Marudanayagam R, Shanmugam V, Gunson BK, et al. Liver retransplantation in adults: a single-centre, 25-year experience. HPB. 2010;12:217-224.

56. 56 Yao FY, Saab S, Bass NM, et al. Prediction of survival after liver retransplantation for late graft failure based on preoperative prog- nostic scores. Hepatology. 2004;39(1):230-238.

57. 57 Lerut J, Laterre P, Roggen F, et al. Adult hepatic retransplanta- tion. UCLA experience. Acta Gastroenterol Belg. 1999;62:261-266.

58. 58 Kumar N, Wall W, Grant D, et al. Liver retransplantation. Transplant Proc. 1999;31:541-542.

59. 59 Meneu Diaz J, Vicente E, Moreno Gonzalez E, et al. Indications for liver retransplantation: 1087 orthotopic liver transplantations between 1986 and 1997. Transplant Proc. 2002;34:306.

60. 60 Doyle H, Morelli F, McMichael J, et al. Hepatic retransplantation – an analysis of risk factors associated with outcome. Transplantation. 1996;61:1499-1505.

61. 61 Shaw B, Gordon R, Iwatsuki S. Hepatic retransplantation. Transplant Proc. 1985;17:264.

62. 62 Busuttil RW, Farmer DG, Yersiz H, et al. Analysis of long-term outcomes of 3200 liver transplantations over two decades. A singlecenter experience. Ann Surg. 2005 June;241(6):905-918.

63. 63 Powelson J, Cosimi A, Lewis W, et al. Hepatic retransplantation in New England – a regional experience and survival model. Transplantation. 1993;55:802-806.

64. 64 Linhares MM, Azoulay D, Matos D, et al. Liver retransplantation: a model for determining long-term survival. Transplantation. 2006;81(7):1016-1021.

65. 65 De Carlis L, Slim A, Giacomoni A, et al. Liver retransplantation: indications and results over a 15-year experience. Transplant Proc. 2001;33:1411-1413.

66. 66 Facciuto M, Heidt D, Guarrera J, et al. Retransplantation for late liver graft failure: Predictors of mortality. Liver Transpl. 2000;6:174-179.

67. 67 Watt KDS, Lyden ER. McCashland. Poor survival after liver retransplantation: Is hepatitis C to blame? Liver Transpl. 2003; 9(10):1019-1024.

68. 68 Andes A, Gerstel E, Combescure C, et al. A score predicting survival after liver retransplantation for hepatitis C virus cirrhosis. Transplantation. 2012;93(7):717-722.

69. 69 Pelletier SJ, Schaubel DE, Punch JD, et al. Hepatitis C is a risk factor for death after liver retransplantation. Liver Transpl. 2005; 11(4):434-440.

70. 70 Yoo HY, Maheshwar A, Thuluvath PJ. Retransplantation of liver: primary graft nonfunction and hepatitis C virus are associated with worse outcome. Liver Transpl. 2003;9(9):897-904.

71. 71 Perry DK, Willingham DL, Sibulesky L, et al. Should donation after cardiac death liver grafts be used for retransplantation. Ann Hepatol. 2011;10(4):482-485.

72. 72 Markmann J, Gornbein J, Markowitz J, et al. A simple model to estimate survival after retransplantation of the liver. Transplantation. 1999;67:422-430.

73. 73 Wong T, Devlin J, Rolando N, et al. Clinical characteristics affecting the outcome of liver retransplantation. Transplantation. 1997; 61:878-881.

74. 74 Granov D.A., Borovik V.V., Zherebtsov F.K., Polysalov V.N., Maistrenko D.N., Rutkin I.O. et al. Liver retransplantation: the experience of the Russian Scientific Center of Radiology and Surgical Technologies (RSCRT). Bulletin of Transplantology and Artificial Organs. 2014;13(4):43-47. (In Russ).

75. 75 Khubutia M.Sh., Zhuravel S.V., Kuznetsova N.K., & Vereshchagin A.S. Liver failure after liver surgery. Annals of Surgical Hepatology. 2014;19(3):27-32. (In Russ).

76. 76 Shcherba A.E., Dziadzko A.M., Aminov A.F., Katin M.L., Korotkov S.V., Efimov D.Yu. et al. Retransplantation in patients with ischemic liver transplant cholangiopathy. Bulletin of Transplantology and Artificial Organs. 2019;21(S):84-84. (In Russ).