New insights in antibody-mediated rejection

Current Opinion in Nephrology and Hypertension

Volumn 23, Issue 6, 2014, Pages 597-604

  Gosset, Clément ^a,c   Lefaucheur, Carmen ^a,b,c   Glotz, Denis ^a,b,c  

^a SAINT LOUIS HOSPITAL   (France)

^b INSERM   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Antibody mediated rejection; Antibody mediated rejection treatment; C1q fixing donor specific antibodies; C4d negative antibody mediated rejection

Indexed keywords

COMPLEMENT COMPONENT C4D; ALLOANTIBODY; COMPLEMENT;

ANTIBODY MEDIATED REJECTION; ANTIBODY SPECIFICITY; COMPLEMENT FIXATION; CONTINUOUS PROCESS; DISEASE MARKER; GRAFT FAILURE; HISTOLOGY; HUMAN; OUTCOME ASSESSMENT; PATHOGENICITY; PREDICTION; PRIORITY JOURNAL; PROGNOSIS; REVIEW; RISK FACTOR; ADVERSE EFFECTS; ANIMAL; BIOPSY; GRAFT REJECTION; GRAFT SURVIVAL; IMMUNOLOGY; KIDNEY; KIDNEY TRANSPLANTATION; PATHOLOGY; PREDICTIVE VALUE; RISK ASSESSMENT; SURGERY; TREATMENT OUTCOME;

ANIMALS; BIOPSY; COMPLEMENT SYSTEM PROTEINS; GRAFT REJECTION; GRAFT SURVIVAL; HUMANS; ISOANTIBODIES; KIDNEY; KIDNEY TRANSPLANTATION; PREDICTIVE VALUE OF TESTS; RISK ASSESSMENT; RISK FACTORS; TREATMENT OUTCOME;

EID: 84927636315     PISSN: 10624821     EISSN: 14736543     Source Type: Journal    
DOI: 10.1097/MNH.0000000000000069     Document Type: Review

References (77)

1. Wolfe RA, Ashby VB, Milford EL, et al. Comparison of mortality in all patients on dialysis, patients on dialysis awaiting transplantation, and recipients of a first cadaveric transplant. N Engl J Med 1999; 341:1725-1730.
2. Hariharan S, Johnson CP, Bresnahan BA, et al. Improved graft survival after renal transplantation in the United States, 1988 to 1996. N Engl J Med 2000; 342:605-612.
3. Meier-Kriesche HU, Schold JD, Srinivas TR, Kaplan B. Lack of improvement in renal allograft survival despite a marked decrease in acute rejection rates over the most recent era. Am J Transplant 2004; 4:378-383.
4. Sellares J, de Freitas DG, MengelM, et al. Understanding the causes of kidney transplant failure: the dominant role of antibody-mediated rejection and nonadherence. Am J Transplant 2012; 12:388-399.
5. Feucht HE, Schneeberger H, Hillebrand G, et al. Capillary deposition of C4d complement fragment and early renal graft loss. Kidney Int 1993; 43:1333-1338.
6. Lefaucheur C, Loupy A, Vernerey D, et al. Antibody-mediated vascular rejection of kidney allografts: a population-based study. Lancet 2013; 381:313-319.
7. Naesens M, Kuypers DR, De Vusser K, et al. Chronic histological damage in early indication biopsies is an independent risk factor for late renal allograft failure. Am J Transplant 2013; 13:86-99.
8. Gaston RS, Cecka JM, Kasiske BL, et al. Evidence for antibody-mediated injury as a major determinant of late kidney allograft failure. Transplantation 2010; 90:68-74.
9. Einecke G, Sis B, Reeve J, et al. Antibody-mediated microcirculation injury is the major cause of late kidney transplant failure. Am J Transplant 2009; 9:2520-2531.
10. Gloor JM, Winters JL, Cornell LD, et al. Baseline donor-specific antibody levels and outcomes in positive crossmatch kidney transplantation. Am J Transplant 2010; 10:582-589.
11. Lefaucheur C, Loupy A, Hill GS, et al. Preexisting donor-specific HLA antibodies predict outcome in kidney transplantation. J Am Soc Nephrol 2010; 21:1398-1406.
12. El Ters M, Grande JP, Keddis MT, et al. Kidney allograft survival after acute rejection, the value of follow-up biopsies. Am J Transplant 2013; 13:2334-2341.
13. Colvin RB. Antibody-mediated renal allograft rejection: diagnosis and pathogenesis. J Am Soc Nephrol 2007; 18:1046-1056.
14. Hill GS, Nochy D, Bruneval P, et al. Donor-specific antibodies accelerate arteriosclerosis after kidney transplantation. J Am Soc Nephrol 2011; 22:975-983.
15. Mauiyyedi S, Pelle PD, Saidman S, et al. Chronic humoral rejection: identification of antibody-mediated chronic renal allograft rejection by C4d deposits in peritubular capillaries. J Am Soc Nephrol 2001; 12:574-582.
16. Solez K, Colvin RB, Racusen LC, et al. Banff '05 Meeting Report: differential diagnosis of chronic allograft injury and elimination of chronic allograft nephropathy ('CAN'). Am J Transplant 2007; 7:518-526.
17. Mengel M, Sis B, Haas M, et al. Banff 2011 Meeting report: new concepts in antibody-mediated rejection. Am J Transplant 2012; 12:563-570.
18. Loupy A, Hill GS, Jordan SC. The impact of donor-specific anti-HLA antibodies on late kidney allograft failure. Nat Rev Nephrol 2012; 8:348-357.
19. Haas M, Sis B, Racusen LC, et al. Banff 2013 meeting report: inclusion of c4d-negative antibody-mediated rejection and antibody-associated arterial lesions. Am J Transplant 2014; 14:272-283.
20. Racusen LC, Solez K, Colvin RB, et al. The Banff 97 working classification of renal allograft pathology. Kidney Int 1999; 55:713-723.
21. Solez K, Benediktsson H, Burdick JF, et al. International standardization of criteria for the histologic diagnosis of renal allograft rejection the Banff working classification of kidney transplant pathology. Kidney Int 1993; 44:411-422.
22. Halloran PF, Schlaut J, Solez K, Srinivasa NS. The significance of the anticlass I antibody response. II. Clinical and pathologic features of renal transplants with anticlass I-like antibody. Transplantation 1992; 53:550-555.
23. Loupy A, Hill GS, Suberbielle C, et al. Significance of C4d Banff scores in early protocol biopsies of kidney transplant recipients with preformed donorspecific antibodies (DSA). Am J Transplant 2011; 11:56-65.
24. Cohen D, Colvin RB, Daha MR, et al. Pros and cons for C4d as a biomarker. Kidney Int 2012; 81:628-639.
25. Haas M. Pathology of C4d-negative antibody-mediated rejection in renal allografts. Curr Opin Organ Transplant 2013; 8:319-326.
26. Loupy A, Suberbielle-Boissel C, Hill GS, et al. Outcome of subclinical antibody-mediated rejection in kidney transplant recipients with preformed donorspecific antibodies. Am J Transplant 2009; 9:2561-2570.
27. Sis B, Jhangri GS, Bunnag S, et al. Endothelial gene expression in kidney transplants with alloantibody indicates antibody-mediated damage despite lack of C4d staining. Am J Transplant 2009; 9:2312-2323.
28. Mohan S, Palanisamy A, Tsapepas D, et al. Donor-specific antibodies adversely affect kidney allograft outcomes. J Am Soc Nephrol 2012; 23:2061-2071.
29. Mengel M, Chan S, Climenhaga J, et al. Banff initiative for quality assurance in transplantation (BIFQUIT): reproducibility of C4d immunohistochemistry in kidney allografts. Am J Transplant 2013; 13:1235-1245.
30. Farkash EA, Colvin RB. Diagnostic challenges in chronic antibody-mediated rejection. Nat Rev Nephrol 2012; 8:255-257.
31. Stegall MD, Diwan T, Raghavaiah S, et al. Terminal complement inhibition decreases antibody-mediated rejection in sensitized renal transplant recipients. Am J Transplant 2011; 11:2405-2413.
32. Stegall MD, Chedid MF, Cornell LD. The role of complement in antibodymediated rejection in kidney transplantation. Nat Rev Nephrol 2012; 8:670-678.
33. Haas M, Montgomery RA, Segev DL, et al. Subclinical acute antibodymediated rejection in positive crossmatch renal allografts. Am J Transplant 2007; 7:576-585.
34. Naesens M, Salvatierra O, Benfield M, et al. Subclinical inflammation and chronic renal allograft injury in a randomized trial on steroid avoidance in pediatric kidney transplantation. Am J Transplant 2012; 12:2730-2743.
35. Lerut E, Naesens M, Kuypers DR, et al. Subclinical peritubular capillaritis at 3 months is associated with chronic rejection at 1 year. Transplantation 2007; 83:1416-1422.
36. Moreso F, Carrera M, Goma M, et al. Early subclinical rejection as a risk factor for late chronic humoral rejection. Transplantation 2012; 93:41-46.
37. Papadimitriou JC, Drachenberg CB, Ramos E, et al. Antibody-mediated allograft rejection: morphologic spectrum and serologic correlations in surveillance and for cause biopsies. Transplantation 2013; 95:128-136.
38. Wiebe C, Gibson IW, Blydt-Hansen TD, et al. Evolution and clinical pathologic correlations of de novo donor-specific HLA antibody post kidney transplant. Am J Transplant 2012; 12:1157-1167.
39. de Kort H, Willicombe M, Brookes P, et al. Microcirculation inflammation associates with outcome in renal transplant patients with de novo donorspecific antibodies. Am J Transplant 2013; 13:485-492.
40. Henderson LK, Nankivell BJ, Chapman JR. Surveillance protocol kidney transplant biopsies: their evolving role in clinical practice. Am J Transplant 2011; 11:1570-1575.
41. Lefaucheur C, Nochy D, Hill GS, et al. Determinants of poor graft outcome in patients with antibody-mediated acute rejection. Am J Transplant 2007; 7:832-841.
42. Gibson IW, Gwinner W, Brocker V, et al. Peritubular capillaritis in renal allografts: prevalence, scoring system, reproducibility and clinicopathological correlates. Am J Transplant 2008; 8:819-825.
43. Loupy A, Lefaucheur C, Vernerey D, et al. Complement-binding anti-HLA antibodies and kidney-allograft survival. N Engl J Med 2013; 369:1215-1226.
44. Lefaucheur C, Loupy A, Zeevi A. Complement-binding anti-HLA antibodies and kidney transplantation. N Engl J Med 2014; 2014:85-86.
45. Zeevi A, Lunz J, Feingold B, et al. Persistent strong anti-HLA antibody at high titer is complement binding and associated with increased risk of antibodymediated rejection in heart transplant recipients. J Heart Lung Transplant 2013; 32:98-105.
46. Arnold ML, Ntokou IS, Doxiadis II, et al. Donor specific HLA antibodies: evaluating the risk for graft loss in renal transplant recipients with isotype switch from complement fixing IgG1/IgG3 to noncomplement fixing IgG2/ IgG4 anti-HLA alloantibodies. Transpl Int 2013; 27:253-261.
47. Hirohashi T, Chase CM, Della Pelle P, et al. A novel pathway of chronic allograft rejection mediated by NK cells and alloantibody. Am J Transplant 2012; 12:313-321.
48. Anegón I, Cuturi M, Trinchieri G, Perussia B. Interaction of Fc receptor (CD16) ligands induces transcription of interleukin 2 receptor (CD25) and lymphokine genes and expression of their products in human natural killer cells. J Exp Med 1988; 167:452-472.
49. Hidalgo LG, Sis B, Sellares J, et al. NK cell transcripts and NK cells in kidney biopsies from patients with donor-specific antibodies: evidence for NK cell involvement in antibody-mediated rejection. Am J Transplant 2010; 10: 1812-1822.
50. King KE, Warren DS, Samaniego-Picota M, et al. Antibody, complement and accommodation in ABO-incompatible transplants. Curr Opin Immunol 2004; 16:545-549.
51. Mizutani K, Terasaki P, Rosen A, et al. Serial ten-year follow-up of HLA and MICA antibody production prior to kidney graft failure. Am J Transplant 2005; 5:2265-2272.
52. Taniguchi M, Rebellato LM, Cai J, et al. Higher risk of kidney graft failure in the presence of antiangiotensin II type-1 receptor antibodies. Am J Transplant 2013; 13:2577-2589.
53. Giral M, Foucher Y, Dufay A, et al. Pretransplant sensitization against angiotensin II type 1 receptor is a risk factor for acute rejection and graft loss. Am J Transplant 2013; 13:2567-2576.
54. Quackenbush J. Microarray analysis and tumor classification. N Engl J Med 2006; 354:2463-2472.
55. Halloran PF, Pereira AB, Chang J, et al. Microarray diagnosis of antibodymediated rejection in kidney transplant biopsies: an international prospective study (INTERCOM). Am J Transplant 2013; 13:2865-2874.
56. Hidalgo LG, Sellares J, Sis B, et al. Interpreting NK cell transcripts versus T cell transcripts in renal transplant biopsies. Am J Transplant 2012; 12: 1180-1191.
57. Loupy A, Lefaucheur C, Vernerey D, et al. Molecular microscope strategy to improve risk stratification in early antibody-mediated kidney allograft rejection. J Am Soc Nephrol 2014. [Epub ahead of print]
58. Lobo PI, Spencer CE, Stevenson WC, Pruett TL. Evidence demonstrating poor kidney graft survival when acute rejections are associated with IgG donor-specific lymphocytotoxin. Transplantation 1995; 59:357-360.
59. Archdeacon P, Chan M, Neuland C, et al. Summary of FDA antibody-mediated rejection workshop. Am J Transplant 2011; 11:896-906.
60. Crespo M, Pascual M, Tolkoff-Rubin N, et al. Acute humoral rejection in renal allograft recipients: I. Incidence, serology and clinical characteristics. Transplantation 2001; 71:652-658.
61. Montgomery RA, Zachary AA, Racusen LC, et al. Plasmapheresis and intravenous immune globulin provides effective rescue therapy for refractory humoral rejection and allows kidneys to be successfully transplanted into cross-match-positive recipients. Transplantation 2000; 70:887-895.
62. Rocha PN, Butterly DW, Greenberg A, et al. Beneficial effect of plasmapheresis and intravenous immunoglobulin on renal allograft survival of patients with acute humoral rejection. Transplantation 2003; 75:1490-1495.
63. Becker YT, Becker BN, Pirsch JD, Sollinger HW. Rituximab as treatment for refractory kidney transplant rejection. Am J Transplant 2004; 4:996-1001.
64. Faguer S, Kamar N, Guilbeaud-Frugier C, et al. Rituximab therapy for acute humoral rejection after kidney transplantation. Transplantation 2007; 83:1277-1280.
65. Bohmig GA, Wahrmann M, Regele H, et al. Immunoadsorption in severe C4dpositive acute kidney allograft rejection: a randomized controlled trial. Am J Transplant 2007; 7:117-121.
66. Everly MJ, Everly JJ, Susskind B, et al. Bortezomib provides effective therapy for antibody-and cell-mediated acute rejection. Transplantation 2008; 86:1754-1761.
67. Walsh RC, Everly JJ, Brailey P, et al. Proteasome inhibitor-based primary therapy for antibody-mediated renal allograft rejection. Transplantation 2010; 89:277-284.
68. Lefaucheur C, Nochy D, Andrade J, et al. Comparison of combination Plasmapheresis/IVIg/anti-CD20 versus high-dose IVIg in the treatment of antibody-mediated rejection. Am J Transplant 2009; 9:1099-1107.
69. Brown CM, Abraham KA, O'Kelly P, et al. Long-term experience of plasmapheresis in antibody-mediated rejection in renal transplantation. Transplant Proc 2009; 41:3690-3692.
70. Locke JE, Magro CM, Singer AL, et al. The use of antibody to complement protein C5 for salvage treatment of severe antibody-mediated rejection. Am J Transplant 2009; 9:231-235.
71. Kocak B, Arpali E, Demiralp E, et al. Eculizumab for salvage treatment of refractory antibody-mediated rejection in kidney transplant patients: case reports. Transplant Proc 2013; 45:1022-1025.
72. Smith RN, Malik F, Goes N, et al. Partial therapeutic response to Rituximab for the treatment of chronic alloantibody mediated rejection of kidney allografts. Transpl Immunol 2012; 27:107-113.
73. Billing H, Rieger S, Susal C, et al. IVIG and rituximab for treatment of chronic antibody-mediated rejection: a prospective study in paediatric renal transplantation with a 2-year follow-up. Transpl Int 2012; 25:1165-1173.
74. Everly MJ, Rebellato LM, Ozawa M, et al. Beyond histology: lowering human leukocyte antigen antibody to improve renal allograft survival in acute rejection. Transplantation 2010; 89:962-967.
75. Burns JM, Cornell LD, Perry DK, et al. Alloantibody levels and acute humoral rejection early after positive crossmatch kidney transplantation. Am J Transplant 2008; 8:2684-2694.
76. Stegall MD, Park WD, Larson TS, et al. The histology of solitary renal allografts at 1 and 5 years after transplantation. Am J Transplant 2011; 11:698-707.
77. Gloor J, Cosio F, Rea D, et al. Histologic findings one year after positive crossmatch or ABO blood group incompatible living donor kidney transplantation. Am J Transplant 2006; 6:1841-1847.