Skip to main content

Advertisement

Log in

Current status of pediatric renal transplant pathology

  • Educational Review
  • Published:
Pediatric Nephrology Aims and scope Submit manuscript

Abstract

Histopathology is still an indispensable tool for the diagnosis of kidney transplant dysfunction in adult and pediatric patients. This review presents consolidated knowledge, recent developments and future prospects on the biopsy procedure, the diagnostic work-up, classification schemes, the histopathology of rejection, including antibody-mediated forms, ABO-incompatible transplants, protocol biopsies, recurrent and de novo disease, post-transplant lymphoproliferative disorder, infectious complications and drug-induced toxicity. It is acknowledged that frequently the correct diagnosis can only be reached in consensus with clinical, serological, immunogenetical, bacteriological and virological findings. This review shall enhance the understanding of the pediatric nephrologist for the thought processes of nephropathologists with the aim to facilitate teamwork between these specialist groups for the benefit of the patient.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Gough J, Rush D, Jeffery J, Nickerson P, McKenna R, Solez K, Trpkov K (2002) Reproducibility of the Banff schema in reporting protocol biopsies of stable renal allografts. Nephrol Dial Transplant 17(6):1081–1084

    Article  PubMed  Google Scholar 

  2. Haas M, Sis B, Racusen LC, Solez K, Glotz D, Colvin RB, Castro MC, David DS, David-Neto E, Bagnasco SM, Cendales LC, Cornell LD, Demetris AJ, Drachenberg CB, Farver CF, Farris AB 3rd, Gibson IW, Kraus E, Liapis H, Loupy A, Nickeleit V, Randhawa P, Rodriguez ER, Rush D, Smith RN, Tan CD, Wallace WD, Mengel M, as the Banff meeting report writing committee (2014) Banff 2013 meeting report: inclusion of c4d-negative antibody-mediated rejection and antibody-associated arterial lesions. Am J Transplant 14(2):272–283

    Article  CAS  PubMed  Google Scholar 

  3. Parada B, Figueiredo A, Nunes P, Bastos C, Macario F, Roseiro A, Dias V, Rolo F, Mota A (2005) Pediatric renal transplantation: comparative study with renal transplantation in the adult population. Transplant Proc 37(6):2771–2774

    Article  CAS  PubMed  Google Scholar 

  4. Chang A, Gibson IW, Cohen AH, Weening JW, Jennette JC, Fogo AB (2012) A position paper on standardizing the nonneoplastic kidney biopsy report. Hum Pathol 43(8):1192–1196

    Article  PubMed  Google Scholar 

  5. Racusen LC, Solez K, Colvin RB, Bonsib SM, Castro MC, Cavallo T, Croker BP, Demetris AJ, Drachenberg CB, Fogo AB, Furness P, Gaber LW, Gibson IW, Glotz D, Goldberg JC, Grande J, Halloran PF, Hansen HE, Hartley B, Hayry PJ, Hill CM, Hoffman EO, Hunsicker LG, Lindblad AS, Yamaguchi Y (1999) The Banff 97 working classification of renal allograft pathology. Kidney Int 55(2):713–723

    Article  CAS  PubMed  Google Scholar 

  6. Colvin RB, Cohen AH, Saiontz C, Bonsib S, Buick M, Burke B, Carter S, Cavallo T, Haas M, Lindblad A, Manivel JC, Nast CC, Salomon D, Weaver C, Weiss M (1997) Evaluation of pathologic criteria for acute renal allograft rejection: reproducibility, sensitivity, and clinical correlation. J Am Soc Nephrol 8(12):1930–1941

    CAS  PubMed  Google Scholar 

  7. Solez K, Axelsen RA, Benediktsson H, Burdick JF, Cohen AH, Colvin RB, Croker BP, Droz D, Dunnill MS, Halloran PF, Häyry P, Jennette JC, Keown PA, Marcussen N, Mihatsch MJ, Morozumi K, Myers BD, Nast CC, Olsen S, Racusen LC, Ramos EL, Rosen S, Sachs DH, Salomon DR, Sanfilippo F, Verani R, The Banff working classification of kidney transplant pathology (1993) International standardization of criteria for the histologic diagnosis of renal allograft rejection: the Banff working classification of kidney transplant pathology. Kidney Int 44(2):411–422

    Article  CAS  PubMed  Google Scholar 

  8. Moreso F, Seron D, O’Valle F, Ibernon M, Goma M, Hueso M, Cruzado JM, Bestard O, Duarte V, del Moral RG, Grinyo JM (2007) Immunephenotype of glomerular and interstitial infiltrating cells in protocol renal allograft biopsies and histological diagnosis. Am J Transplant 7(12):2739–2747

    Article  CAS  PubMed  Google Scholar 

  9. Sis B, Mengel M, Haas M, Colvin RB, Halloran PF, Racusen LC, Solez K, Baldwin WM 3rd, Bracamonte ER, Broecker V, Cosio F, Demetris AJ, Drachenberg C, Einecke G, Gloor J, Glotz D, Kraus E, Legendre C, Liapis H, Mannon RB, Nankivell BJ, Nickeleit V, Papadimitriou JC, Randhawa P, Regele H, Renaudin K, Rodriguez ER, Seron D, Seshan S, Suthanthiran M, Wasowska BA, Zachary A, Zeevi A (2010) Banff ’09 meeting report: antibody mediated graft deterioration and implementation of Banff working groups. Am J Transplant 10(3):464–471

    Article  CAS  PubMed  Google Scholar 

  10. Bates WD, Davies DR, Welsh K, Gray DW, Fuggle SV, Morris PJ (1999) An evaluation of the Banff classification of early renal allograft biopsies and correlation with outcome. Nephrol Dial Transplant 14(10):2364–2369

    Article  CAS  PubMed  Google Scholar 

  11. Trpkov K, Campbell P, Pazderka F, Cockfield S, Solez K, Halloran PF (1996) Pathologic features of acute renal allograft rejection associated with donor-specific antibody, Analysis using the Banff grading schema. Transplantation 61(11):1586–1592

    Article  CAS  PubMed  Google Scholar 

  12. Mauiyyedi S, Crespo M, Collins AB, Schneeberger EE, Pascual MA, Saidman SL, Tolkoff-Rubin NE, Williams WW, Delmonico FL, Cosimi AB, Colvin RB (2002) Acute humoral rejection in kidney transplantation: II. Morphology, immunopathology, and pathologic classification. J Am Soc Nephrol 13(3):779–787

    PubMed  Google Scholar 

  13. Lefaucheur C, Loupy A, Vernerey D, Duong-Van-Huyen JP, Suberbielle C, Anglicheau D, Verine J, Beuscart T, Nochy D, Bruneval P, Charron D, Delahousse M, Empana JP, Hill GS, Glotz D, Legendre C, Jouven X (2013) Antibody-mediated vascular rejection of kidney allografts: a population-based study. Lancet 381(9863):313–319

    Article  CAS  PubMed  Google Scholar 

  14. Sis B, Bagnasco SM, Cornell LD, Randhawa P, Haas M, Lategan B, Magil AB, Herzenberg AM, Gibson IW, Kuperman M, Sasaki K, Kraus ES, Banff Working G (2015) Isolated endarteritis and kidney transplant survival: a multicenter collaborative study. J Am Soc Nephrol 26(5):1216–1227

    Article  CAS  PubMed  Google Scholar 

  15. Bröcker V, Hirzallah M, Gwinner W, Bockmeyer CL, Wittig J, Zell S, Agustian PA, Schwarz A, Ganzenmuller T, Zilian E, Immenschuh S, Becker JU (2013) Histopathological and clinical findings in renal transplants with Banff type II and III acute cellular rejection without tubulointerstitial infiltrates. Virchows Arch 46:203–211

    Google Scholar 

  16. Seron D, Moreso F, Bover J, Condom E, Gil-Vernet S, Canas C, Fulladosa X, Torras J, Carrera M, Grinyo JM, Alsina J (1997) Early protocol renal allograft biopsies and graft outcome. Kidney Int 51(1):310–316

    Article  CAS  PubMed  Google Scholar 

  17. Gloor JM, Cohen AJ, Lager DJ, Grande JP, Fidler ME, Velosa JA, Larson TS, Schwab TR, Griffin MD, Prieto M, Nyberg SL, Sterioff S, Kremers WK, Stegall MD (2002) Subclinical rejection in tacrolimus-treated renal transplant recipients. Transplantation 73(12):1965–1968

    Article  PubMed  Google Scholar 

  18. Matoza JR, Danguilan RA, Chicano S (2008) Impact of Banff borderline acute rejection among renal allograft recipients. Transplant Proc 40(7):2303–2306

    Article  CAS  PubMed  Google Scholar 

  19. Famulski KS, Einecke G, Sis B, Mengel M, Hidalgo LG, Kaplan B, Halloran PF (2010) Defining the canonical form of T-cell-mediated rejection in human kidney transplants. Am J Transplant 10(4):810–820

    Article  CAS  PubMed  Google Scholar 

  20. Loupy A, Vernerey D, Tinel C, Aubert O, Duong van Huyen JP, Rabant M, Verine J, Nochy D, Empana JP, Martinez F, Glotz D, Jouven X, Legendre C, Lefaucheur C (2015) Subclinical rejection phenotypes at 1 year post-transplant and outcome of kidney allografts. J Am Soc Nephrol 26(7):1721–1731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wu K, Budde K, Lu H, Schmidt D, Liefeldt L, Glander P, Neumayer HH, Rudolph B (2014) The severity of acute cellular rejection defined by Banff classification is associated with kidney allograft outcomes. Transplantation 97(11):1146–1154

    Article  CAS  PubMed  Google Scholar 

  22. Einecke G, Sis B, Reeve J, Mengel M, Campbell PM, Hidalgo LG, Kaplan B, Halloran PF (2009) Antibody-mediated microcirculation injury is the major cause of late kidney transplant failure. Am J Transplant 9(11):2520–2531

    Article  CAS  PubMed  Google Scholar 

  23. El-Zoghby ZM, Stegall MD, Lager DJ, Kremers WK, Amer H, Gloor JM, Cosio FG (2009) Identifying specific causes of kidney allograft loss. Am J Transplant 9(3):527–535

    Article  CAS  PubMed  Google Scholar 

  24. Richardson WP, Colvin RB, Cheeseman SH, Tolkoff-Rubin NE, Herrin JT, Cosimi AB, Collins AB, Hirsch MS, McCluskey RT, Russell PS, Rubin RH (1981) Glomerulopathy associated with cytomegalovirus viremia in renal allografts. N Engl J Med 305(2):57–63

    Article  CAS  PubMed  Google Scholar 

  25. Halloran PF, Wadgymar A, Ritchie S, Falk J, Solez K, Srinivasa NS (1990) The significance of the anti-class I antibody response. I. Clinical and pathologic features of anti-class I-mediated rejection. Transplantation 49(1):85–91

    Article  CAS  PubMed  Google Scholar 

  26. Feucht HE, Felber E, Gokel MJ, Hillebrand G, Nattermann U, Brockmeyer C, Held E, Riethmuller G, Land W, Albert E (1991) Vascular deposition of complement-split products in kidney allografts with cell-mediated rejection. Clin Exp Immunol 86(3):464–470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Sis B, Jhangri GS, Riopel J, Chang J, de Freitas DG, Hidalgo L, Mengel M, Matas A, Halloran PF (2012) A New diagnostic algorithm for antibody-mediated microcirculation inflammation in kidney transplants. Am J Transplant 12:1168–1179

    Article  CAS  PubMed  Google Scholar 

  28. Kikic Z, Kainz A, Kozakowski N, Oberbauer R, Regele H, Bond G, Bohmig GA (2015) Capillary C4d and kidney allograft outcome in relation to morphologic lesions suggestive of antibody-mediated rejection. Clin J Am Soc Nephrol 10(8):1435–1443

    Article  PubMed  PubMed Central  Google Scholar 

  29. Nadasdy GM, Bott C, Cowden D, Pelletier R, Ferguson R, Nadasdy T (2005) Comparative study for the detection of peritubular capillary C4d deposition in human renal allografts using different methodologies. Hum Pathol 36(11):1178–1185

    Article  CAS  PubMed  Google Scholar 

  30. Troxell ML, Weintraub LA, Higgins JP, Kambham N (2006) Comparison of C4d immunostaining methods in renal allograft biopsies. Clin J Am Soc Nephrol 1(3):583–591

    Article  PubMed  Google Scholar 

  31. Solez K, Colvin RB, Racusen LC, Haas M, Sis B, Mengel M, Halloran PF, Baldwin W, Banfi G, Collins AB, Cosio F, David DS, Drachenberg C, Einecke G, Fogo AB, Gibson IW, Glotz D, Iskandar SS, Kraus E, Lerut E, Mannon RB, Mihatsch M, Nankivell BJ, Nickeleit V, Papadimitriou JC, Randhawa P, Regele H, Renaudin K, Roberts I, Seron D, Smith RN, Valente M (2008) Banff 07 classification of renal allograft pathology: updates and future directions. Am J Transplant 8(4):753–760

    Article  CAS  PubMed  Google Scholar 

  32. Mengel M, Chan S, Climenhaga J, Kushner YB, Regele H, Colvin RB, Randhawa P (2013) Banff initiative for quality assurance in transplantation (BIFQUIT): reproducibility of C4d immunohistochemistry in kidney allografts. Am J Transplant 13(5):1235–1245

    Article  CAS  PubMed  Google Scholar 

  33. Kikic Z, Regele H, Nordmeyer V, Wahrmann M, Kletzmayr J, Bartel G, Bohmig GA (2011) Significance of peritubular capillary, glomerular, and arteriolar C4d staining patterns in paraffin sections of early kidney transplant biopsies. Transplantation 91(4):440–446

    PubMed  Google Scholar 

  34. Valente M, Furian L, Della Barbera M, Silvestre C, Marino S, Seveso M, Cozzi E, Rigotti P, Aiello FB (2012) Glomerular c4d immunoreactivity in acute rejection biopsies of renal transplant patients. Transplant Proc 44(7):1897–1900

    Article  CAS  PubMed  Google Scholar 

  35. de Kort H, Willicombe M, Brookes P, Dominy KM, Santos-Nunez E, Galliford JW, Chan K, Taube D, McLean AG, Cook HT, Roufosse C (2013) Microcirculation inflammation associates with outcome in renal transplant patients with de novo donor-specific antibodies. Am J Transplant 13(2):485–492

    Article  PubMed  Google Scholar 

  36. Batal I, Lunz JG 3rd, Aggarwal N, Zeevi A, Sasatomi E, Basu A, Tan H, Shapiro R, Randhawa P (2010) A critical appraisal of methods to grade transplant glomerulitis in renal allograft biopsies. Am J Transplant 10(11):2442–2452

    Article  CAS  PubMed  Google Scholar 

  37. Mihatsch MJ, Zollinger HU, Gudat F, Schuppler J, Riede UN, Thiel G, Brunner F, Enderlin F (1975) Transplantation arteriopathy. Pathol Microbiol (Basel) 43:219–223

    CAS  Google Scholar 

  38. Hill GS, Nochy D, Bruneval P, Duong van Huyen JP, Glotz D, Suberbielle C, Zuber J, Anglicheau D, Empana JP, Legendre C, Loupy A (2011) Donor-specific antibodies accelerate arteriosclerosis after kidney transplantation. J Am Soc Nephrol 22(5):975–983

    Article  PubMed  PubMed Central  Google Scholar 

  39. Zollinger HU, Moppert J, Thiel G, Rohr HP (1973) Morphology and pathogenesis of glomerulopathy in cadaver kidney allografts treated with antilymphocyte globulin. Curr Top Pathol 57:1–48

    CAS  PubMed  Google Scholar 

  40. Habib R, Zurowska A, Hinglais N, Gubler MC, Antignac C, Niaudet P, Broyer M, Gagnadoux MF (1993) A specific glomerular lesion of the graft: allograft glomerulopathy. Kidney Int Suppl 42:S104–S111

    CAS  PubMed  Google Scholar 

  41. Ivanyi B, Fahmy H, Brown H, Szenohradszky P, Halloran PF, Solez K (2000) Peritubular capillaries in chronic renal allograft rejection: a quantitative ultrastructural study. Hum Pathol 31(9):1129–1138

    Article  CAS  PubMed  Google Scholar 

  42. Hsu HC, Suzuki Y, Churg J, Grishman E (1980) Ultrastructure of transplant glomerulopathy. Histopathology 4(4):351–367

    Article  CAS  PubMed  Google Scholar 

  43. Horita S, Nitta K, Kawashima M, Honda K, Onitsuka S, Tokumoto T, Tanabe K, Toma H, Nihei H, Yamaguchi Y (2003) C4d deposition in the glomeruli and peritubular capillaries associated with transplant glomerulopathy. Clin Transplant 17(4):325–330

    Article  CAS  PubMed  Google Scholar 

  44. Racusen L (2007) Chronic transplant glomerulopathy: need for further assessment. Clin J Am Soc Nephrol 2(6):1108–1109

    Article  PubMed  Google Scholar 

  45. Fotheringham J, Angel CA, McKane W (2009) Transplant glomerulopathy: morphology, associations and mechanism. Nephron Clin Pract 113(1):c1–c7, discussion c7

    Article  CAS  PubMed  Google Scholar 

  46. Grau V, Zeuschner P, Immenschuh S, Bockmeyer CL, Zell S, Wittig J, Säuberlich K, Abbas M, Padberg W, Meyer-Schwesinger C, von Brandenstein M, Schlosser M, Dieplinger G, Galliford J, Clarke C, Roufosse C, Becker JU (2016) Immune Complex-type deposits in the fischer-344 to lewis rat model of renal transplantation and a subset of human transplant glomerulopathy. doi:10.1097/TP.0000000000001068

  47. Brocker V, Pfaffenbach A, Habicht A, Chatzikyrkou C, Kreipe HH, Haller H, Scheffner I, Gwinner W, Zilian E, Immenschuh S, Schwarz A, Horn PA, Heinemann FM, Becker JU (2013) Beyond C4d: the ultrastructural appearances of endothelium in ABO-incompatible renal allografts. Nephrol Dial Transplant 28:3101–3109

    Article  PubMed  Google Scholar 

  48. Haas M, Segev DL, Racusen LC, Bagnasco SM, Locke JE, Warren DS, Simpkins CE, Lepley D, King KE, Kraus ES, Montgomery RA (2009) C4d deposition without rejection correlates with reduced early scarring in ABO-incompatible renal allografts. J Am Soc Nephrol 20(1):197–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Fidler ME, Gloor JM, Lager DJ, Larson TS, Griffin MD, Textor SC, Schwab TR, Prieto M, Nyberg SL, Ishitani MB, Grande JP, Kay PA, Stegall MD (2004) Histologic findings of antibody-mediated rejection in ABO blood-group-incompatible living-donor kidney transplantation. Am J Transplant 4(1):101–107

    Article  PubMed  Google Scholar 

  50. Schwarz A, Gwinner W, Hiss M, Radermacher J, Mengel M, Haller H (2005) Safety and adequacy of renal transplant protocol biopsies. Am J Transplant 5(8):1992–1996

    Article  PubMed  Google Scholar 

  51. Cosio FG, El Ters M, Cornell LD, Schinstock CA, Stegall MD (2016) Changing kidney allograft histology early posttransplant: prognostic implications of 1-year protocol biopsies. Am J Transplant 16:194–203

    Article  CAS  PubMed  Google Scholar 

  52. Chapman JR (2012) Do protocol transplant biopsies improve kidney transplant outcomes? Curr Opin Nephrol Hypertens 21(6):580–586

    Article  PubMed  Google Scholar 

  53. NAPRTCS Administrative Office (2015) NAPRTCS annual report 2014. Available at: https://web.emmes.com/study/ped/annlrept/annualrept2014.pdf

  54. Ortiz F, Gelpi R, Koskinen P, Manonelles A, Raisanen-Sokolowski A, Carrera M, Honkanen E, Grinyo JM, Cruzado JM (2012) IgA nephropathy recurs early in the graft when assessed by protocol biopsy. Nephrol Dial Transplant 27(6):2553–2558

    Article  CAS  PubMed  Google Scholar 

  55. IJpelaar DH, Farris AB, Goemaere N, Amann K, Goldschmeding R, Nguyen TQ, Farkash E, van den Heuvel MC, de Heer E, Bruijn JA, Colvin RB, Bajema IM (2008) Fidelity and evolution of recurrent FSGS in renal allografts. J Am Soc Nephrol 19(11):2219–2224

    Article  PubMed  PubMed Central  Google Scholar 

  56. D’Agati V (2003) Pathologic classification of focal segmental glomerulosclerosis. Semin Nephrol 23(2):117–134

    Article  PubMed  Google Scholar 

  57. Ponticelli C, Moroni G, Glassock RJ (2014) De novo glomerular diseases after renal transplantation. Clin J Am Soc Nephrol 9(8):1479–1487

    Article  PubMed  PubMed Central  Google Scholar 

  58. Patrakka J, Ruotsalainen V, Reponen P, Qvist E, Laine J, Holmberg C, Tryggvason K, Jalanko H (2002) Recurrence of nephrotic syndrome in kidney grafts of patients with congenital nephrotic syndrome of the Finnish type: role of nephrin. Transplantation 73(3):394–403

    Article  PubMed  Google Scholar 

  59. Wei C, El Hindi S, Li J, Fornoni A, Goes N, Sageshima J, Maiguel D, Karumanchi SA, Yap HK, Saleem M, Zhang Q, Nikolic B, Chaudhuri A, Daftarian P, Salido E, Torres A, Salifu M, Sarwal MM, Schaefer F, Morath C, Schwenger V, Zeier M, Gupta V, Roth D, Rastaldi MP, Burke G, Ruiz P, Reiser J (2011) Circulating urokinase receptor as a cause of focal segmental glomerulosclerosis. Nat Med 17(8):952–960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Alachkar N, Wei C, Arend LJ, Jackson AM, Racusen LC, Fornoni A, Burke G, Rabb H, Kakkad K, Reiser J, Estrella MM (2013) Podocyte effacement closely links to suPAR levels at time of posttransplantation focal segmental glomerulosclerosis occurrence and improves with therapy. Transplantation 96(7):649–656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Cathelin D, Placier S, Ploug M, Verpont MC, Vandermeersch S, Luque Y, Hertig A, Rondeau E, Mesnard L (2014) Administration of recombinant soluble urokinase receptor per se is not sufficient to induce podocyte alterations and proteinuria in mice. J Am Soc Nephrol 25(8):1662–1668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Spinale JM, Mariani LH, Kapoor S, Zhang J, Weyant R, Song PX, Wong HN, Troost JP, Gadegbeku CA, Gipson DS, Kretzler M, Nihalani D, Holzman LB, Nephrotic Syndrome Study N (2015) A reassessment of soluble urokinase-type plasminogen activator receptor in glomerular disease. Kidney Int 87(3):564–574

    Article  CAS  PubMed  Google Scholar 

  63. Yu CC, Fornoni A, Weins A, Hakroush S, Maiguel D, Sageshima J, Chen L, Ciancio G, Faridi MH, Behr D, Campbell KN, Chang JM, Chen HC, Oh J, Faul C, Arnaout MA, Fiorina P, Gupta V, Greka A, Burke GW 3rd, Mundel P (2013) Abatacept in B7-1-Positive Proteinuric Kidney Disease. N Engl J Med 369:2416–2423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Burkholder PM, Marchand A, Krueger RP (1970) Mixed membranous and proliferative glomerulonephritis. A correlative light, immunofluorescence, and electron microscopic study. Lab Invest 23(5):459–479

    CAS  PubMed  Google Scholar 

  65. Strife CF, McEnery PT, McAdams AJ, West CD (1977) Membranoproliferative glomerulonephritis with disruption of the glomerular basement membrane. Clin Nephrol 7(2):65–72

    CAS  PubMed  Google Scholar 

  66. Fakhouri F, Fremeaux-Bacchi V, Noel LH, Cook HT, Pickering MC (2010) C3 glomerulopathy: a new classification. Nat Rev Nephrol 6(8):494–499

    Article  CAS  PubMed  Google Scholar 

  67. Little MA, Dupont P, Campbell E, Dorman A, Walshe JJ (2006) Severity of primary MPGN, rather than MPGN type, determines renal survival and post-transplantation recurrence risk. Kidney Int 69(3):504–511

    Article  CAS  PubMed  Google Scholar 

  68. Zand L, Lorenz EC, Cosio FG, Fervenza FC, Nasr SH, Gandhi MJ, Smith RJ, Sethi S (2014) Clinical findings, pathology, and outcomes of C3GN after kidney transplantation. J Am Soc Nephrol 25(5):1110–1117

    Article  CAS  PubMed  Google Scholar 

  69. Noris M, Remuzzi G (2010) Thrombotic microangiopathy after kidney transplantation. Am J Transplant 10(7):1517–1523

    Article  CAS  PubMed  Google Scholar 

  70. Sellier-Leclerc AL, Fremeaux-Bacchi V, Dragon-Durey MA, Macher MA, Niaudet P, Guest G, Boudailliez B, Bouissou F, Deschenes G, Gie S, Tsimaratos M, Fischbach M, Morin D, Nivet H, Alberti C, Loirat C (2007) Differential impact of complement mutations on clinical characteristics in atypical hemolytic uremic syndrome. J Am Soc Nephrol 18(8):2392–2400

    Article  CAS  PubMed  Google Scholar 

  71. Lemaire M, Fremeaux-Bacchi V, Schaefer F, Choi M, Tang WH, Le Quintrec M, Fakhouri F, Taque S, Nobili F, Martinez F, Ji W, Overton JD, Mane SM, Nurnberg G, Altmuller J, Thiele H, Morin D, Deschenes G, Baudouin V, Llanas B, Collard L, Majid MA, Simkova E, Nurnberg P, Rioux-Leclerc N, Moeckel GW, Gubler MC, Hwa J, Loirat C, Lifton RP (2013) Recessive mutations in DGKE cause atypical hemolytic-uremic syndrome. Nat Genet 45(5):531–536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Kean JM, Rao S, Wang M, Garcea RL (2009) Seroepidemiology of human polyomaviruses. PLoS Pathog 5(3):e1000363

    Article  PubMed  PubMed Central  Google Scholar 

  73. Schmitt C, Raggub L, Linnenweber-Held S, Adams O, Schwarz A, Heim A (2014) Donor origin of BKV replication after kidney transplantation. J Clin Virol 59(2):120–125

    Article  PubMed  Google Scholar 

  74. Buettner M, Xu H, Bohme R, Seliger B, Jacobi J, Wiesener M, Benz K, Amann K (2012) Predominance of TH2 cells and plasma cells in polyoma virus nephropathy: a role for humoral immunity? Hum Pathol 43(9):1453–1462

    Article  CAS  PubMed  Google Scholar 

  75. Rane S, Nada R, Minz M, Sakhuja V, Joshi K (2012) Spectrum of cytomegalovirus-induced renal pathology in renal allograft recipients. Transplant Proc 44(3):713–716

    Article  CAS  PubMed  Google Scholar 

  76. Kim SS, Hicks J, Goldstein SL (2003) Adenovirus pyelonephritis in a pediatric renal transplant patient. Pediatr Nephrol 18(5):457–461

    PubMed  Google Scholar 

  77. Fonseca LE Jr, Shapiro R, Randhawa PS (2003) Occurrence of urinary tract infection in patients with renal allograft biopsies showing neutrophilic tubulitis. Mod Pathol 16(4):281–285

    Article  PubMed  Google Scholar 

  78. van Krieken JH, Onciu M, Elenitoba-Johnson KSJ, Jaffe ES (2008) Immunodeficiency-associated lymphoproliferative disorders. In: Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman J (eds) WHO classification of tumours of haematopoietic and lymphoid tissue. IARC, Lyon, pp 335–350

  79. Shapiro R, Nalesnik M, McCauley J, Fedorek S, Jordan ML, Scantlebury VP, Jain A, Vivas C, Ellis D, Lombardozzi-Lane S, Randhawa P, Johnston J, Hakala TR, Simmons RL, Fung JJ, Starzl TE (1999) Posttransplant lymphoproliferative disorders in adult and pediatric renal transplant patients receiving tacrolimus-based immunosuppression. Transplantation 68(12):1851–1854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Cleper R, Ben Shalom E, Landau D, Weissman I, Krause I, Konen O, Rahamimov R, Mor E, Bar-Nathan N, Frishberg Y, Davidovits M (2012) Post-transplantation lymphoproliferative disorder in pediatric kidney-transplant recipients—a national study. Pediatr Transplant 16(6):619–626

    Article  PubMed  Google Scholar 

  81. Ryffel B, Weber E, Mihatsch MJ (1994) Nephrotoxicity of immunosuppressants in rats: comparison of macrolides with cyclosporin. Exp Nephrol 2(6):324–333

    CAS  PubMed  Google Scholar 

  82. Mihatsch M, Gudat F, Ryffel B, Thiel G (1994) Cyclosporine nephropathy. In: Tisher CC, Brenner BM (eds) Renal pathology: with clinical and functional correlations, vol 2. JB Lippincott, Philadelphia

    Google Scholar 

  83. Brocker V, Schubert V, Scheffner I, Schwarz A, Hiss M, Becker JU, Scherer R, Haller H, Kreipe HH, Mengel M, Gwinner W (2012) Arteriolar lesions in renal transplant biopsies: prevalence, progression, and clinical significance. Am J Pathol 180(5):1852–1862

    Article  PubMed  Google Scholar 

  84. Snanoudj R, Royal V, Elie C, Rabant M, Girardin C, Morelon E, Kreis H, Fournet JC, Noel LH, Legendre C (2011) Specificity of histological markers of long-term CNI nephrotoxicity in kidney-transplant recipients under low-dose cyclosporine therapy. Am J Transplant 11(12):2635–2646

    Article  CAS  PubMed  Google Scholar 

  85. Halloran PF, Pereira AB, Chang J, Matas A, Picton M, De Freitas D, Bromberg J, Seron D, Sellares J, Einecke G, Reeve J (2013) Potential impact of microarray diagnosis of T cell-mediated rejection in kidney transplants: the INTERCOM study. Am J Transplant 13:2352–2363

    Article  CAS  PubMed  Google Scholar 

  86. Loupy A, Lefaucheur C, Vernerey D, Chang J, Hidalgo LG, Beuscart T, Verine J, Aubert O, Dubleumortier S, Duong van Huyen JP, Jouven X, Glotz D, Legendre C, Halloran PF (2014) Molecular microscope strategy to improve risk stratification in early antibody-mediated kidney allograft rejection. J Am Soc Nephrol 25:2267–2277

    Article  PubMed  PubMed Central  Google Scholar 

  87. Brazdziute E, Laurinavicius A (2011) Digital pathology evaluation of complement C4d component deposition in the kidney allograft biopsies is a useful tool to improve reproducibility of the scoring. Diagn Pathol 6[Suppl 1]:S5

    Article  PubMed  PubMed Central  Google Scholar 

  88. Farris AB, Chan S, Climenhaga J, Adam B, Bellamy CO, Seron D, Colvin RB, Reeve J, Mengel M (2014) Banff fibrosis study: multicenter visual assessment and computerized analysis of interstitial fibrosis in kidney biopsies. Am J Transplant 14(4):897–907

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jan U. Becker.

Ethics declarations

Conflict of interest

The author declares that there is no conflict of interest.

Additional information

Answers

1. d; 2. c; 3. b; 4. a; 5. c

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Becker, J.U. Current status of pediatric renal transplant pathology. Pediatr Nephrol 32, 425–437 (2017). https://doi.org/10.1007/s00467-016-3381-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00467-016-3381-x

Keywords

Navigation