The revisited classification of GN in SLE at 10 years: Time to re-evaluate histopathologic lesions

Journal of the American Society of Nephrology

Volumn 26, Issue 12, 2015, Pages 2938-2946

  Wilhelmus, Suzanne ^a   Alpers, Charles E ^b   Cook, H Terence ^c   Ferrario, Franco ^d   Fogo, Agnes B ^e   Haas, Mark ^f   Joh, Kensuke ^g   Noël, Laure Hélène ^h   Seshan, Surya V ⁱ   Bruijn, Jan A ^a   Bajema, Ingeborg M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF WASHINGTON   (United States)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d SAN GERARDO HOSPITAL   (Italy)

^e VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^f CEDARS SINAI MEDICAL CENTER   (United States)

^g TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^h HÔPITAL NECKER ENFANTS MALADES   (France)

ⁱ WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN ANTIBODY COMPLEX; ARTICLE; CELL PROLIFERATION; CHRONICITY; DISEASE CLASSIFICATION; DISEASE COURSE; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; GLOMERULONEPHRITIS; HISTOPATHOLOGY; HUMAN; IMMUNOGLOBULIN A NEPHROPATHY; INTERSTITIAL NEPHRITIS; KIDNEY BIOPSY; LUPUS ERYTHEMATOSUS NEPHRITIS; MESANGIUM CELL; MICROSCOPY; MONOCYTE; PRACTICE GUIDELINE; PRIORITY JOURNAL; VASCULAR LESION; BIOPSY; CAPILLARY; CHRONIC DISEASE; CLASSIFICATION; KIDNEY; NOMENCLATURE; PATHOLOGY; VASCULARIZATION;

BIOPSY; CAPILLARIES; CELL PROLIFERATION; CHRONIC DISEASE; HUMANS; KIDNEY; LUPUS NEPHRITIS; TERMINOLOGY AS TOPIC;

EID: 84952338944     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015040384     Document Type: Article

References (45)

1. Weening JJ, D'Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, Balow JE, Bruijn JA, Cook T, Ferrario F, Fogo AB, Ginzler EM, Hebert L, Hill G, Hill P, Jennette JC, Kong NC, Lesavre P, Lockshin M, Looi LM, Makino H, Moura LA, Nagata M: The classification of glomerulonephritis in systemic lupus erythematosus revisited. J Am Soc Nephrol 15: 241-250, 2004
2. Weening JJ, D'Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, Balow JE, Bruijn JA, Cook T, Ferrario F, Fogo AB, Ginzler EM, Hebert L, Hill G, Hill P, Jennette JC, Kong NC, Lesavre P, Lockshin M, Looi LM, Makino H, Moura LA, Nagata M; International Society of Nephrology Working Group on the Classification of Lupus Nephritis; Renal Pathology Society Working Group on the Classification of Lupus Nephritis: The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int 65: 521-530, 2004
3. Yokoyama H, Wada T, Hara A, Yamahana J, Nakaya I, Kobayashi M, Kitagawa K, Kokubo S, Iwata Y, Yoshimoto K, Shimizu K, Sakai N, Furuichi K; Kanazawa Study Group for Renal Diseases and Hypertension: The outcome and a new ISN/RPS 2003 classification of lupus nephritis in Japanese. Kidney Int 66: 2382-2388, 2004
4. Furness PN, Taub N: Interobserver reproducibility and application of the ISN/RPS classification of lupus nephritis-a UK-wide study. Am J Surg Pathol 30: 1030-1035, 2006
5. Wilhelmus S, Cook HT, Noel LH, Ferrario F, Wolterbeek R, Bruijn JA, Bajema IM: Interobserver agreement on histopathological lesions in class III or IV lupus nephritis. Clin J Am Soc Nephrol 10: 47-53, 2015
6. Corwin HL, Schwartz MM, Lewis EJ: The importance of sample size in the interpretation of the renal biopsy. Am J Nephrol 8: 85-89, 1988
7. Roberts IS, Cook HT, Troyanov S, Alpers CE, Amore A, Barratt J, Berthoux F, Bonsib S, Bruijn JA, Cattran DC, Coppo R, D'Agati V, D'Amico G, Emancipator S, Emma F, Feehally J, Ferrario F, Fervenza FC, Florquin S, Fogo A, Geddes CC, Groene HJ, Haas M, Herzenberg AM, Hill PA, Hogg RJ, Hsu SI, Jennette JC, Joh K, Julian BA, Kawamura T, Lai FM, Li LS, Li PK, Liu ZH, Mackinnon B, Mezzano S, Schena FP, Tomino Y,Walker PD, Wang H, Weening JJ, YoshikawaN, Zhang H; Working Group of the International IgA Nephropathy Network and the Renal Pathology Society: The Oxford classification of IgA nephropathy: Pathology definitions, correlations, and reproducibility. Kidney Int 76: 546-556, 2009
8. Appel GB, Silva FG, Pirani CL, Meltzer JI, Estes D: Renal involvement in systemic lupud erythematosus (SLE): A study of 56 patients emphasizing histologic classification. Medicine (Baltimore) 57: 371-410, 1978
9. Dorland WAN: Dorland's Illustrated Medical Dictionary, 31st Ed., Philadelphia, Saunders, 2007
10. Bonsib SM: Renal anatomy and histology. In: Heptinstall's Pathology of the Kidney, 7th Ed., edited by Jennette J, Olson J, Silva F, D'Agati V, Philadelphia, Wolters Kluwer, 2015, pp 1-66
11. Najafi CC, Korbet SM, Lewis EJ, Schwartz MM, Reichlin M, Evans J; Lupus Nephritis Collaborative Study Group: Significance of histologic patterns of glomerular injury upon long-term prognosis in severe lupus glomerulonephritis. Kidney Int 59: 2156-2163, 2001
12. Haring CM, Rietveld A, van den Brand JA, Berden JH: Segmental and global subclasses of class IV lupus nephritis have similar renal outcomes. J Am Soc Nephrol 23: 149-154, 2012
13. Schwartz MM, Korbet SM, Lewis EJ; Collaborative Study Group: The prognosis and pathogenesis of severe lupus glomerulonephritis. Nephrol Dial Transplant 23: 1298-1306, 2008
14. Schwartz MM, Kawala KS, Corwin HL, Lewis EJ: The prognosis of segmental glomerulonephritis in systemic lupus erythematosus. Kidney Int 32: 274-279, 1987
15. Austin HA 3rd, Muenz LR, Joyce KM, Antonovych TT, Balow JE: Diffuse proliferative lupus nephritis: Identification of specific pathologic features affecting renal outcome. Kidney Int 25: 689-695, 1984
16. Magil AB, PutermanML, Ballon HS, Chan V, Lirenman DS, Rae A, Sutton RA: Prognostic factors in diffuse proliferative lupus glomerulonephritis. Kidney Int 34: 511-517, 1988
17. Esdaile JM, Levinton C, Federgreen W, Hayslett JP, Kashgarian M: The clinical and renal biopsy predictors of long-term outcome in lupus nephritis: A study of 87 patients and review of the literature. Q J Med 72: 779-833, 1989
18. Schwartz MM, Lan SP, Bernstein J, Hill GS, Holley K, Lewis EJ; Lupus Nephritis Collaborative Study Group: Role of pathology indices in the management of severe lupus glomerulonephritis. Kidney Int 42: 743-748, 1992
19. Austin HA 3rd, Boumpas DT, Vaughan EM, Balow JE: High-risk features of lupus nephritis: Importance of race and clinical and histological factors in 166 patients. Nephrol Dial Transplant 10: 1620-1628, 1995
20. Wernick RM, Smith DL, Houghton DC, Phillips DS, Booth JL, Runckel DN, Johnson DS, Brown KK, Gaboury CL: Reliability of histologic scoring for lupus nephritis: A community-based evaluation. Ann Intern Med 119: 805-811, 1993
21. Schwartz MM, Lan SP, Bernstein J, Hill GS, Holley K, Lewis EJ; Lupus Nephritis Collaborative Study Group: Irreproducibility of the activity and chronicity indices limits their utility in the management of lupus nephritis. Am J Kidney Dis 21: 374-377, 1993
22. ErreGL, Bosincu L, Faedda R, Fenu P,Masala A, SannaM, Taras L, LonguMG, PirasM, Soro G, Satta AE, Passiu G: Antiphospholipid syndrome nephropathy (APSN) in patients with lupus nephritis: A retrospective clinical and renal pathology study. Rheumatol Int 34: 535-541, 2014
23. Daugas E, Nochy D, Huong DL, Duhaut P, Beaufils H, Caudwell V, Bariety J, Piette JC, Hill G: Antiphospholipid syndrome nephropathy in systemic lupus erythematosus. J Am Soc Nephrol 13: 42-52, 2002
24. Miranda JM, Jara LJ, Calleja C, SaavedraMA, Bustamante RM, Angeles U: Clinical significance of antiphospholipid syndrome nephropathy (APSN) in patients with systemic lupus erythematosus (SLE). Reumatol Clin 5: 209-213, 2009
25. Dube GK, Markowitz GS, Radhakrishnan J, Appel GB, D'Agati VD: Minimal change disease in systemic lupus erythematosus. Clin Nephrol 57: 120-126, 2002
26. Hertig A, Droz D, Lesavre P, Grünfeld JP, Rieu P: SLE and idiopathic nephrotic syndrome: Coincidence or not? Am J Kidney Dis 40: 1179-1184, 2002
27. Kraft SW, Schwartz MM, Korbet SM, Lewis EJ: Glomerular podocytopathy in patients with systemic lupus erythematosus.JAmSoc Nephrol 16: 175-179, 2005
28. Salvatore SP, Barisoni LM, Herzenberg AM, Chander PN, Nickeleit V, Seshan SV: Collapsing glomerulopathy in 19 patients with systemic lupus erythematosus or lupus-like disease. Clin J Am Soc Nephrol 7: 914-925, 2012
29. Appel GB, Pirani CL, D'Agati V: Renal vascular complications of systemic lupus erythematosus. J Am Soc Nephrol 4: 1499-1515, 1994
30. Banfi G, Bertani T, Boeri V, Faraggiana T, Mazzucco G, Monga G, Sacchi G: Renal vascular lesions as a marker of poor prognosis in patients with lupus nephritis. Gruppo Italiano per lo Studio della Nefrite Lupica (GISNEL). Am J Kidney Dis 18: 240-248, 1991
31. Wu LH, Yu F, Tan Y, Qu Z, Chen MH, Wang SX, Liu G, Zhao MH: Inclusion of renal vascular lesions in the 2003 ISN/RPS system for classifying lupus nephritis improves renal outcome predictions. Kidney Int 83: 715-723, 2013
32. 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,GlotzD,Goldberg JC, Grande J, Halloran PF, Hansen HE, Hartley B, Hayry PJ, Hill CM, Hoffman EO, Hunsicker LG, Lindblad AS,Marcussen N,Mihatsch MJ, Nadasdy T, Nickerson P, Olson TS, Papadimitriou JC, Randhawa PS, Rayner DC, Roberts I, Rose S, Rush D, Salinas-Madrigal L, Salomon DR, Sund S, Taskinen E, Trpkov K, Yamaguchi Y: The Banff 97 working classification of renal allograft pathology. Kidney Int 55: 713-723, 1999
33. Yu F, Wu LH, Tan Y, Li LH, Wang CL, Wang WK,Qu Z, ChenMH,Gao JJ, Li ZY, Zheng X, Ao J, Zhu SN, Wang SX, Zhao MH, Zou WZ, Liu G: Tubulointerstitial lesions of patients with lupus nephritis classified by the 2003 International Society of Nephrology and Renal Pathology Society system. Kidney Int 77: 820-829, 2010
34. Hsieh C, Chang A, Brandt D, Guttikonda R, Utset TO, Clark MR: Predicting outcomes of lupus nephritis with tubulointerstitial inflammation and scarring. Arthritis Care Res (Hoboken) 63: 865-874, 2011
35. Furness PN, Taub N, Assmann KJ, Banfi G, Cosyns JP, Dorman AM, Hill CM, Kapper SK, Waldherr R, Laurinavicius A, Marcussen N, Martins AP, Nogueira M, Regele H, Seron D, Carrera M, Sund S, Taskinen EI, Paavonen T, Tihomirova T, Rosenthal R: International variation in histologic grading is large, and persistent feedback does not improve reproducibility. Am J Surg Pathol 27: 805-810, 2003
36. Farris AB, Adams CD, Brousaides N, Della Pelle PA, Collins AB, Moradi E, Smith RN, Grimm PC, Colvin RB: Morphometric and visual evaluation of fibrosis in renal biopsies. J Am Soc Nephrol 22: 176-186, 2011
37. Cattran DC, Coppo R, Cook HT, Feehally J, Roberts IS, Troyanov S, Alpers CE, Amore A, Barratt J, Berthoux F, Bonsib S, Bruijn JA, D'Agati V, D'Amico G, Emancipator S, Emma F, Ferrario F, Fervenza FC, Florquin S, Fogo A, Geddes CC, Groene HJ, Haas M, Herzenberg AM, Hill PA, Hogg RJ, Hsu SI, Jennette JC, Joh K, Julian BA, Kawamura T, Lai FM, Leung CB, Li LS, Li PK, Liu ZH, Mackinnon B, Mezzano S, Schena FP, Tomino Y, Walker PD, Wang H, Weening JJ, Yoshikawa N, Zhang H; Working Group of the International IgA Nephropathy Network and the Renal Pathology Society: TheOxford classification of IgA nephropathy: Rationale, clinicopathological correlations, and classification. Kidney Int 76: 534-545, 2009
38. Muehrcke RC, Kark RM, Pirani CL, Pollak VE, Steck IE: Histological and clinical evolution of lupus nephritis. Ann RheumDis 14: 371-377, 1955
39. Pollak VE, Pirani CL, Schwartz FD: The natural history of the renal lupus erythematosus manifestations. J LabClinMed 63: 537-550, 1964
40. Pollak VE, Pirani CL, Schwartz FD: The natural history of renal manifestations of systemic lupus erythematosus. J Am Soc Nephrol 8: 1189-1198, 1997
41. Baldwin DS, Lowenstein J, Rothfield NF, GalloG,McCluskey RT: The clinical course of the proliferative and membranous forms of lupus nephritis. Ann Intern Med 73: 929-942, 1970
42. Zimmerman SW, Jenkins PG, Shelf WD, Bloodworth JM Jr., Burkholder PM: Progression from minimal or focal to diffuse proliferative lupus nephritis. Lab Invest 32: 665-672, 1975
43. Baldwin DS, Gluck MC, Lowenstein J, Gallo GR: Lupus nephritis. Clinical course as related to morphologic forms and their transitions. Am J Med 62: 12-30, 1977
44. Churg J, Sobin L: Lupus nephritis. In: Renal Disease: Classification and Atlas of Glomerular Diseases, Tokyo, Igaku-Shoin Medical Publishers, 1982, pp 127-131
45. Churg J, Bernstein J, Glassock RJ: Lupus nephritis. In: Renal Disease: Classification and Atlas of Glomerular Diseases, 2nd Ed., New York, Igaku-Shoin Medical Publishers, 1995, pp 151-177