The significance of histological diagnosis in renal allograft biopsies in 2014

Transplant International

Volumn 28, Issue 2, 2015, Pages 136-145

  Broecker, Verena ^a   Mengel, Michael ^b  

^a CAMBRIDGE UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

antibody mediated rejection; Banff; histopathology; kidney biopsy; transplantation

Indexed keywords

ACUTE GRAFT REJECTION; ANTIBODY MEDIATED REJECTION; ANTIBODY SCREENING; BK VIRUS INFECTION; BK VIRUS NEPHROPATHY; CLINICAL DECISION MAKING; DIAGNOSTIC ACCURACY; DIAGNOSTIC APPROACH ROUTE; GENE EXPRESSION; GLOMERULITIS; HISTOLOGY; HISTOPATHOLOGY; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; KIDNEY ALLOGRAFT; KIDNEY BIOPSY; KIDNEY DISEASE; KIDNEY TRANSPLANTATION; PATIENT DECISION MAKING; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; RENAL GRAFT DYSFUNCTION; REVIEW; SENSITIVITY AND SPECIFICITY; THROMBOTIC THROMBOCYTOPENIC PURPURA; VIREMIA; VIRUS LOAD; ALLOTRANSPLANTATION; BIOPSY; BK VIRUS; COMPLICATION; DONOR; GRAFT REJECTION; IMMUNOLOGY; KIDNEY; PATHOLOGY; POLYOMAVIRUS INFECTION; T LYMPHOCYTE;

CALCINEURIN INHIBITOR;

BIOPSY; BK VIRUS; CALCINEURIN INHIBITORS; GRAFT REJECTION; HUMANS; KIDNEY; KIDNEY TRANSPLANTATION; POLYOMAVIRUS INFECTIONS; T-LYMPHOCYTES; TISSUE DONORS; TRANSPLANTATION, HOMOLOGOUS;

EID: 84920946490     PISSN: 09340874     EISSN: 14322277     Source Type: Journal    
DOI: 10.1111/tri.12446     Document Type: Review

References (92)

1. Kreis H, Noël L-H, Legendre C,. The first transplant kidney biopsy ever performed. Am J Transplant 2013; 13: 1367.
2. Williams WW, Taheri D, Tolkoff-Rubin N, Colvin RB,. Clinical role of the renal transplant biopsy. Nat Rev Nephrol 2012; 8: 110.
3. John R, Herzenberg AM,. Our approach to a renal transplant biopsy. J Clin Pathol 2010; 63: 26.
4. Parfrey PS, Kuo YL, Hanley JA, et al,. The diagnostic and prognostic value of renal allograft biopsy. Transplantation 1984; 38: 586.
5. Matas AJ, Tellis VA, Sablay L, Quinn T, Soberman R, Veith FJ,. The value of needle renal allograft biopsy. III. A prospective study. Surgery 1985; 98: 922.
6. Waltzer WC, Miller F, Arnold A, Jao S, Anaise D, Rapaport FT,. Value of percutaneous core needle biopsy in the differential diagnosis of renal transplant dysfunction. J Urol 1987; 137: 1117.
7. Kiss D, Landmann J, Mihatsch M, Huser B, Brunner FP, Thiel G,. Risks and benefits of graft biopsy in renal transplantation under cyclosporin-A. Clin Nephrol 1992; 38: 132.
8. Kon SP, Templar J, Dodd SM, Rudge CJ, Raftery MJ,. Diagnostic contribution of renal allograft biopsies at various intervals after transplantation. Transplantation 1997; 63: 547.
9. Pascual M, Vallhonrat H, Cosimi AB, et al,. The clinical usefulness of the renal allograft biopsy in the cyclosporine era: a prospective study. Transplantation 1999; 67: 737.
10. Al-Awwa IA, Hariharan S, First MR,. Importance of allograft biopsy in renal transplant recipients: correlation between clinical and histological diagnosis. Am J Kidney Dis 1998; 31 (6 Suppl. 1): S15.
11. Colvin RB, Cohen AH, Saiontz C, et al,. Evaluation of pathologic criteria for acute renal allograft rejection: reproducibility, sensitivity, and clinical correlation. J Am Soc Nephrol 1997; 8: 1930.
12. Halloran PF, Reeve JP, Pereira AB, Hidalgo LG, Famulski KS,. Antibody-mediated rejection, T cell-mediated rejection, and the injury-repair response: new insights from the Genome Canada studies of kidney transplant biopsies. Kidney Int 2014; 85: 258.
13. Dare AJ, Pettigrew GJ, Saeb-Parsy K,. Preoperative assessment of the deceased-donor kidney: from macroscopic appearance to molecular biomarkers. Transplantation 2014; 97: 797.
14. Henderson LK, Nankivell BJ, Chapman JR,. Surveillance protocol kidney transplant biopsies: their evolving role in clinical practice. Am J Transplant 2011; 11: 1570.
15. Cosio FG, Grande JP, Wadei H, Larson TS, Griffin MD, Stegall MD,. Predicting subsequent decline in kidney allograft function from early surveillance biopsies. Am J Transplant 2005; 5: 2464.
16. Schwarz A, Mengel M, Gwinner W, et al,. Risk factors for chronic allograft nephropathy after renal transplantation: a protocol biopsy study. Kidney Int 2005; 67: 341.
17. Moreso F, Ibernon M, Gomà M, et al,. Subclinical rejection associated with chronic allograft nephropathy in protocol biopsies as a risk factor for late graft loss. Am J Transplant 2006; 6: 747.
18. Mengel M, Chapman JR, Cosio FG, et al,. Protocol biopsies in renal transplantation: insights into patient management and pathogenesis. Am J Transplant 2007; 7: 512.
19. Mengel M, Gwinner W, Schwarz A, et al,. Infiltrates in protocol biopsies from renal allografts. Am J Transplant 2007; 7: 356.
20. Stegall MD, Park WD, Larson TS, et al,. The histology of solitary renal allografts at 1 and 5 years after transplantation. Am J Transplant [Internet]. 2010 Nov 9 [cited 2011 Jan 5]; Available from: http://www.ncbi.nlm.nih.gov/pubmed/21062418.
21. Nankivell BJ, Borrows RJ, Fung CL-S, O'Connell PJ, Allen RDM, Chapman JR,. The natural history of chronic allograft nephropathy. N Engl J Med 2003; 349: 2326.
22. Moulin B, Merville P, Renaudin K, et al,. Evaluation of protocol biopsy utility 12 months after renal transplantation: a multicenter observational analysis. J Transplant 2012; 2012: 781263.
23. Rush D, Nickerson P, Gough J, et al,. Beneficial effects of treatment of early subclinical rejection: a randomized study. J Am Soc Nephrol 1998; 9: 2129.
24. Rush D, Arlen D, Boucher A, et al,. Lack of benefit of early protocol biopsies in renal transplant patients receiving TAC and MMF: a randomized study. Am J Transplant 2007; 7: 2538.
25. Mengel M, Sis B, Haas M, et al,. Banff 2011 Meeting report: new concepts in antibody-mediated rejection. Am J Transplant 2012; 12: 563.
26. Caplin B, Veighey K, Mahenderan A, et al,. Early changes in scores of chronic damage on transplant kidney protocol biopsies reflect donor characteristics, but not future graft function. Clin Transplant 2013; 27: E669.
27. Mengel M, Chang J, Kayser D, et al,. The molecular phenotype of 6-week protocol biopsies from human renal allografts: reflections of prior injury but not future course. Am J Transplant [Internet]. 2010 Nov 29 [cited 2011 Jan 2]; Available from: http://www.ncbi.nlm.nih.gov/pubmed/21114657.
28. Loupy A, Suberbielle-Boissel C, Hill GS, et al,. Outcome of subclinical antibody-mediated rejection in kidney transplant recipients with preformed donor-specific antibodies. Am J Transplant 2009; 9: 2561.
29. Bentall A, Cornell LD, Gloor JM, et al,. Five-year outcomes in living donor kidney transplants with a positive crossmatch. Am J Transplant 2013; 13: 76.
30. Gloor JM, Cosio FG, Rea DJ, et al,. Histologic findings one year after positive crossmatch or ABO blood group incompatible living donor kidney transplantation. Am J Transplant 2006; 6: 1841.
31. Sellarés J, De Freitas DG, Mengel M, et al,. Understanding the causes of kidney transplant failure: the dominant role of antibody-mediated rejection and nonadherence. Am J Transplant 2012; 12: 388.
32. 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.
33. Halloran PF, De Freitas DG, Einecke G, et al,. The molecular phenotype of kidney transplants. Am J Transplant 2010; 10: 2215.
34. Halloran PF,. T cell-mediated rejection of kidney transplants: a personal viewpoint. Am J Transplant 2010; 10: 1126.
35. 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].
36. Lee JR, Muthukumar T, Dadhania D, et al,. Urinary cell mRNA profiles predictive of human kidney allograft status. Immunol Rev 2014; 258: 218.
37. Famulski KS, De Freitas DG, Kreepala C, et al,. Molecular phenotypes of acute kidney injury in kidney transplants. J Am Soc Nephrol 2012; 23: 948.
38. Mihatsch MJ, Thiel G, Basler V, et al,. Morphological patterns in cyclosporine-treated renal transplant recipients. Transplant Proc 1985; 17 (4 Suppl. 1): 101.
39. Solez K, Colvin RB, Racusen LC, et al,. Banff 07 classification of renal allograft pathology: updates and future directions. Am J Transplant 2008; 8: 753.
40. 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.
41. Lefaucheur C, Loupy A, Vernerey D, et al,. Antibody-mediated vascular rejection of kidney allografts: a population-based study. Lancet 2013; 381: 313.
42. Racusen LC, Solez K, Colvin RB, et al,. The Banff 97 working classification of renal allograft pathology. Kidney Int 1999; 55: 713.
43. De Freitas DG, Sellarés J, Mengel M, et al,. The nature of biopsies with "borderline rejection" and prospects for eliminating this category. Am J Transplant 2012; 12: 191.
44. Bröcker V, Hirzallah M, Gwinner W, et al,. Histopathological and clinical findings in renal transplants with Banff type II and III acute cellular rejection without tubulointerstitial infiltrates. Virchows Arch 2014; 464: 203.
45. 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.
46. 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.
47. Batal I, Lunz JG 3rd, Aggarwal N, et al,. A critical appraisal of methods to grade transplant glomerulitis in renal allograft biopsies. Am J Transplant 2010; 10: 2442.
48. Gibson IW, Gwinner W, Bröcker V, et al,. Peritubular capillaritis in renal allografts: prevalence, scoring system, reproducibility and clinicopathological correlates. Am J Transplant 2008; 8: 819.
49. Bagnasco SM, Zachary AA, Racusen LC, et al,. Time course of pathologic changes in kidney allografts of positive crossmatch HLA-incompatible transplant recipients. Transplantation 2014; 97: 440.
50. Sharif A, Kraus ES, Zachary AA, et al,. Histologic phenotype on 1-year posttransplantation biopsy and allograft survival in HLA-incompatible kidney transplants. Transplantation 2014; 97: 541.
51. Satoskar AA, Pelletier R, Adams P, et al,. De novo thrombotic microangiopathy in renal allograft biopsies-role of antibody-mediated rejection. Am J Transplant 2010; 10: 1804.
52. 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: 1235-45.
53. Haas M,. Pathology of C4d-negative antibody-mediated rejection in renal allografts. Curr Opin Organ Transplant 2013; 18: 319.
54. Loupy A, Hill GS, Suberbielle C, et al,. Significance of C4d Banff scores in early protocol biopsies of kidney transplant recipients with preformed donor-specific antibodies (DSA). Am J Transplant 2011; 11: 56.
55. 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.
56. 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.
57. El-Zoghby ZM, Stegall MD, Lager DJ, et al,. Identifying specific causes of kidney allograft loss. Am J Transplant 2009; 9: 527.
58. Bröcker V, Schubert V, Scheffner I, et al,. Arteriolar lesions in renal transplant biopsies: prevalence, progression, and clinical significance. Am J Pathol 2012; 180: 1852.
59. Snanoudj R, Royal V, Elie C, et al,. Specificity of histological markers of long-term CNI nephrotoxicity in kidney-transplant recipients under low-dose cyclosporine therapy. Am J Transplant [Internet]. 2011 Aug 30 [cited 2011 Sep 8]; Available from: http://www.ncbi.nlm.nih.gov/pubmed/21883915.
60. Briganti EM, Russ GR, McNeil JJ, Atkins RC, Chadban SJ,. Risk of renal allograft loss from recurrent glomerulonephritis. N Engl J Med 2002; 347: 103.
61. Sprangers B, Kuypers DR,. Recurrence of glomerulonephritis after renal transplantation. Transplant Rev (Orlando) 2013; 27: 126.
62. Choy BY, Chan TM, Lai KN,. Recurrent glomerulonephritis after kidney transplantation. Am J Transplant 2006; 6: 2535.
63. El-Zoghby ZM, Grande JP, Fraile MG, Norby SM, Fervenza FC, Cosio FG,. Recurrent idiopathic membranous nephropathy: early diagnosis by protocol biopsies and treatment with anti-CD20 monoclonal antibodies. Am J Transplant 2009; 9: 2800.
64. Ortiz F, Gelpi R, Koskinen P, et al,. IgA nephropathy recurs early in the graft when assessed by protocol biopsy. Nephrol Dial Transplant 2012; 27: 2553.
65. Liapis G, Singh HK, Derebail VK, Gasim AMH, Kozlowski T, Nickeleit V,. Diagnostic significance of peritubular capillary basement membrane multilaminations in kidney allografts: old concepts revisited. Transplantation 2012; 94: 620.
66. Hill GS, Nochy D, Bruneval P, et al,. Donor-specific antibodies accelerate arteriosclerosis after kidney transplantation. JASN 2011; 22: 975.
67. Mengel M, Reeve J, Bunnag S, et al,. Scoring total inflammation is superior to the current Banff inflammation score in predicting outcome and the degree of molecular disturbance in renal allografts. Am J Transplant 2009; 9: 1859.
68. Nankivell BJ, Borrows RJ, Fung CLS, O'Connell PJ, Chapman JR, Allen RDM,. Delta analysis of posttransplantation tubulointerstitial damage. Transplantation 2004; 78: 434.
69. Tait BD, Süsal C, Gebel HM, et al,. Consensus guidelines on the testing and clinical management issues associated with HLA and non-HLA antibodies in transplantation. Transplantation 2013; 95: 19.
70. Buob D, Grimbert P, Glowacki F, et al,. Three-year outcome of isolated glomerulitis on 3-month protocol biopsies of donor HLA antibody negative patients. Transpl Int 2012; 25: 663.
71. Roufosse CA, Shore I, Moss J, et al,. Peritubular capillary basement membrane multilayering on electron microscopy. Transplant J 2012; 94: 269.
72. Wavamunno MD, O'Connell PJ, Vitalone M, et al,. Transplant glomerulopathy: ultrastructural abnormalities occur early in longitudinal analysis of protocol biopsies. Am J Transplant 2007; 7: 2757.
73. Bröcker V, Pfaffenbach A, Habicht A, et al,. Beyond C4d: the ultrastructural appearances of endothelium in ABO-incompatible renal allografts. Nephrol Dial Transplant 2013; 28: 3101.
74. Hirsch HH, Randhawa P,. AST infectious diseases community of practice. BK polyomavirus in solid organ transplantation. Am J Transplant 2013; 13 (Suppl. 4): 179.
75. Hirsch HH, Babel N, Comoli P, et al,. European perspective on human polyomavirus infection, replication and disease in solid organ transplantation. Clin Microbiol Infect 2014; 20 (Suppl. 7): 74-88.
76. Drachenberg CB, Papadimitriou JC, Hirsch HH, et al,. Histological patterns of polyomavirus nephropathy: correlation with graft outcome and viral load. Am J Transplant 2004; 4: 2082.
77. Menter T, Mayr M, Schaub S, Mihatsch MJ, Hirsch HH, Hopfer H,. Pathology of resolving polyomavirus-associated nephropathy. Am J Transplant 2013; 13: 1474.
78. Feucht HE,. Complement C4d in graft capillaries-the missing link in the recognition of humoral alloreactivity. Am J Transplant 2003; 3: 646.
79. Colvin RB, Smith RN,. Antibody-mediated organ-allograft rejection. Nat Rev Immunol 2005; 5: 807.
80. Sis B, Halloran PF,. Endothelial transcripts uncover a previously unknown phenotype: C4d-negative antibody-mediated rejection. Curr Opin Organ Transplant 2010; 15: 42.
81. Sellarés J, Reeve J, Loupy A, et al,. Molecular diagnosis of antibody-mediated rejection in human kidney transplants. Am J Transplant 2013; 13: 971.
82. Halloran PF, Pereira AB, Chang J, et al,. Potential impact of microarray diagnosis of T cell-mediated rejection in kidney transplants: The INTERCOM Study. Am J Transplant 2013; 13: 2352-63.
83. Halloran PF, Pereira AB, Chang J, et al,. Microarray diagnosis of antibody-mediated rejection in kidney transplant biopsies: an international prospective study (INTERCOM). Am J Transplant 2013; 13: 2865.
84. Mannon RB, Matas AJ, Grande J, et al,. Inflammation in areas of tubular atrophy in kidney allograft biopsies: a potent predictor of allograft failure. Am J Transplant 2010; 10: 2066.
85. Mengel M, Sis B, Halloran PF,. SWOT analysis of Banff: strengths, weaknesses, opportunities and threats of the international Banff consensus process and classification system for renal allograft pathology. Am J Transplant 2007; 7: 2221.
86. Cosio FG, Grande JP, Larson TS, et al,. Kidney allograft fibrosis and atrophy early after living donor transplantation. Am J Transplant 2005; 5: 1130.
87. Gwinner W, Hinzmann K, Erdbruegger U, et al,. Acute tubular injury in protocol biopsies of renal grafts: prevalence, associated factors and effect on long-term function. Am J Transplant 2008; 8: 1684.
88. Mengel M, Bogers J, Bosmans J-L, et al,. Incidence of C4d stain in protocol biopsies from renal allografts: results from a multicenter trial. Am J Transplant 2005; 5: 1050.
89. Serõn D, Moreso F, Fulladosa X, Hueso M, Carrera M, Grinyõ JM,. Reliability of chronic allograft nephropathy diagnosis in sequential protocol biopsies. Kidney Int 2002; 61: 727.
90. Lerut E, Naesens M, Kuypers DR, Vanrenterghem Y, Van Damme B,. Subclinical peritubular capillaritis at 3 months is associated with chronic rejection at 1 year. Transplantation 2007; 83: 1416.
91. Gloor JM, Sethi S, Stegall MD, et al,. Transplant glomerulopathy: subclinical incidence and association with alloantibody. Am J Transplant 2007; 7: 2124.
92. Choi BS, Shin MJ, Shin SJ, et al,. Clinical significance of an early protocol biopsy in living-donor renal transplantation: ten-year experience at a single center. Am J Transplant 2005; 5: 1354.