Journal Information
Vol. 28. Issue. 4.August 2008
Pages 361-473
Vol. 28. Issue. 4.August 2008
Pages 361-473
DOI:
Full text access
Guidelines for indicating, obtaining, processing, and evaluating kidney transplant biopsies
Recomendaciones para la indicación, obtención, procesamiento y evaluación de biopsias en el trasplante renal.
Visits
11686
Daniel Seróna, Fernando Anayab, Roberto Marcénc, Raimundo García del Morald, Eduardo Vázquez Martule, Antonio Alarcónf, Amado Andrésg, Dolores Burgosh, Miguel González Molinah, Luis Capdevilai, Carlos Jiménezj, Federico Oppenheimerk, José María Moralesg, Luis Pallardól, Ana Sánchez Fructuosom
a Servicio de Nefrología, Hospital Universitari de Bellvitge, Barcelona, Barcelona, España,
b Servicio de Nefrología, Hospital Gregorio Marañón, Madrid, Madrid, España,
c Servicio de Nefrología, Hospital Ramón y Cajal, Madrid, Madrid, España,
d Servicio de Nefrología, Hospital Universitario de Granada, Granada, Granada, España,
e Servicio de Nefrología, Complejo Hospitalario Universitario Juan Canalejo, A Coruña, A Coruña, España,
f Servicio de Nefrología, Hospital Universitario Son Dureta, Palma de Mallorca, Islas Baleares, España,
g Servicio de Nefrología, Hospital 12 de Octubre, Madrid, Madrid, España,
h Servicio de Nefrología, Regional Universitario Carlos Haya, Málaga, Málaga, España,
i Servicio de Nefrología, Hospital de la Vall d¿Hebron, Barcelona, Barcelona, España,
j Servicio de Nefrología, Hospital Universitario La Paz, Madrid, Madrid, España,
k Servicio de Nefrología, Hospital Clínic, Barcelona, Barcelona, España,
l Servicio de Nefrología, Hospital Doctor Peset, Valencia, Valencia, España,
m Servicio de Nefrología, Hospital Clínico San Carlos, Madrid, Madrid, España,
Ver más
This item has received
Article information
Abstract
Full Text
Bibliography
Download PDF
Statistics
A pesar de la importante actividad trasplantadora en España (1) lo cierto es que todavía no se ha desarrollado en nuestro país un consenso sobre las situaciones clínicas en las que sería recomendable realizar una biopsia diagnóstica, ni sobre cómo mejorar en la práctica clínica el uso de biopsias de protocolo o de biopsias del donante.
Palabras clave:
aspectos técnicos biopsia
Palabras clave:
Biopsia injerto renal
Palabras clave:
indicaciones de biopsia
Despite the significant transplant activity in Spain,1 no consensus has been reached yet in our country about the clinical situations in which a diagnostic biopsy would be recommended, or about how use of protocol or donor biopsies may be improved in clinical practice. Thus, an overall view detects a high heterogeneity between the different centres and even certain practices that may be considered inadequate.
Keywords:
technical aspects of graft biopsy
Keywords:
kidney graft biopsy
Keywords:
indications of graft biopsy
Full Text

INTRODUCTIÓN

Despite the significant transplant activity in Spain,1 no consensus has been reached yet in our country about the clinical situations in which a diagnostic biopsy would be recommended, or about how use of protocol or donor biopsies may be improved in clinical practice. Thus, an overall view detects a high heterogeneity between the different centres and even certain practices that may be considered inadequate. For instance, despite the significant
evidence advising performance of biopsies in certain donor types or use of protocol biopsies,2,3 a recent epidemiological study demonstrated that the former only account for 3% of all biopsies performed in Spain every year,4 while only two Spanish centres perform serial protocol biopsies. An analysis of diagnostic biopsies also shows significant differences as regards activity in the different centres, with up to 10-fold differences being found in the reported biopsy/transplant ratios in certain cases.4 In addition, no clear agreement appears to exist either about how renal tissue samples should be obtained and processed. There are relevant differences as regards use of different puncture needle gauges, as well as a quite limited use of more specific diagnostic procedures such as immunofluorescence, immunohistochemistry, or electron microscopy.

Because of this situation, a group of clinicians and nephropathologists experienced in kidney transplant jointly
addressed, in a consensus conference held in Toledo in 2007, the various issues of interest related to the indication,
processing, and evaluation of kidney biopsies in transplant patients. The main conclusions and recommendations on
the subject of such consensus group are summarised in this document.

CLINICAL VALUE OF BIOPSY IN KIDNEY TRANSPLANT

Donor biopsy
Multiple studies have shown that the presence of pre-existing lesions in the donor biopsy is associated to the occurrence of acute rejection, a poorer function, development of subsequent lesions, and a reduced graft survival.5-20 Despite methodological differences between the different studies and certain disparate results,21 there is currently a fair amount of agreement in that the finding of glomerular, tubulointerstitial, and vascular lesions in the biopsy at the time of implant represents one of the main donor-dependent factors that may condition kidney graft evolution. Indeed, it has been shown in several series that the finding in the donor biopsy of ~20% glomerulosclerosis is associated to the presence of delayed graft function (DGF) immediately after transplant, and also to a reduced kidney function or long-term graft loss.8,13-15,18 The presence of tubulointerstitial damage inherited from the donor, such as interstitial fibrosis, tubular atrophy, or acute tubular necrosis, also has a relevant role and is correlated to subsequent development in the recipient of glomerulosclerosis and chronic interstitial damage. Such events significantly influence kidney function and survival of the implanted organ18-20 and emphasise the importance of indication for performance of this biopsy in the donor using a good analytical methodology.22

As regards vascular damage, Nankivell et al found in 2001 that small vessel lesions in the donor predicted for detection of typical chronic nephropathy lesion in biopsies taken at 3 months of transplant,17 whereas in the long term, detection of fibrous intimal thickening in the biopsy at the time of implant has been associated to the occurrence and severity of interstitial fibrosis, as well as to a reduced creatinine clearance.12 Based on all the foregoing, it is understandable that interest in performance of donor biopsies has significantly increased in recent years, in parallel to the increasing use of marginal organs from elderly, diabetic, or hypertensive patients. The presence of these factors is obviously associated to development in the kidney of the abovementioned histological lesions,23,24 which are consistently related to poorer graft evolution outcomes,25,26 as already discussed.

Histological evaluation of the potential graft thus represents, together with clinical and laboratory data, a procedure
that has been used to decide whether a single or double transplant should be performed or organs from that donor should be discarded.27-29 This is the main current indication for donor biopsy in many centres, but it should not
be forgotten that taking a sample at time zero, even in optimum donors, is of great help for adequate interpretation by pathologists of potential subsequent lesions in the recipient. Biopsy should therefore not be limited to the study of graft viability.

Finally, it should also be reminded that biopsy performance in donors is of particular interest in the setting of clinical
trials in order to have paired morphological data before and after transplant.

Recipient biopsy
Histological examination of renal biopsy continues to be the test par excellence for diagnostic identification of graft
pathology, and its value is shown by the fact that more than 90% of biopsies performed in kidney transplant patients in Spain are indicated for diagnostic reasons.4 The main value of biopsy lies in the possibility of differentiating in detail the presence of lesions suggesting acute rejection, nephrotoxicity induced by calcineurin inhibitors, or chronic lesions, and also of diagnosing not clinically suspected conditions such as de novo glomerulopathies, disease recurrence, or nephropathy associated to polyomavirus type BK. In this regard, introduction in recent years of the Banff criteria and their respective updates30-33 has allowed for having a reproducible tool34 with a high clinical-pathological correlation35 and internationally accepted for description of acute and chronic lesions of the different kidney compartments. In addition, recent incorporation of new histological
and marker techniques, such as detection of C4d and donor-specific antibodies, has increased the diagnostic and
prognostic capacity of renal biopsy, giving pathologists the possibility of performing increasingly accurate diagnoses. In this regard, the growing volume of evidence accumulated using these procedures recently allowed the Banff conference for proposing introduction of a new concept, late antibody-mediated rejection, as well as criteria required for its diagnosis.33

With regard to protocol biopsies, recent studies have been able to establish the natural history of lesions affecting the renal graft,36 as well as the impact of each of them on transplant prognosis. Use of serial biopsies has revealed that prevalence of interstitial infiltrates and tubulitis in stable grafts, the so-called subclinical rejection (SCR), is maximum during the initial months after transplant, after which prevalence gradually decreases (though SCR may persist for longer than one year in some patients).38 Presence of these acute lesion, even in cases with minimal inflammation, is consistently associated to the occurrence of chronic lesions such as interstitial fibrosis and tubular atrophy (IF/TA)36,39-41 and to a decrease in long-term graft survival, as recently seen in patients with SCR lesions two weeks after transplant followed up for 10 years.42 Once established, IF/TA progresses rapidly during the first months, and despite being clinically silent at the start,36,43,44 it is also related to a poorer kidney function and to
long-term graft loss45,46 even when detected early at 6 months of transplant.47 In fact, the predictive value of IF/TA is independent from other classical markers such as serum creatinine, proteinuria, or acute rejection.48

In this setting, there has been recently an increasing interest in detection of lesion patterns in biopsies that would help predict transplant evolution better and earlier than separate lesion assessment. The combination of IF/TA and vascular damage has been shown to be significantly associated to a poorer 10-year graft survival as compared to IF/AT alone,49 and similar results were seen at 5 years in patients with IF/TA lesions and transplant glomerulopathy.50 Moreover, the combination of acute and chronic lesions also predicts for poorer long-term results, so that IF/TA has a particularly poorer prognosis when it is concomitantly associated to the presence of SCR.41,50,51 In fact, certain lesion patterns found in protocol biopsies within 6 months of transplant, such as the presence of IF/TA plus transplant vasculopathy or IF/TA plus SCR, have shown no less sensitivity and specificity for predicting 7-year graft viability than classical markers such as acute rejection or kidney function.3

It is also particular interesting to note that protocol biopsies could have a significant role for improving graft prognosis. There are two reports on this regard that, despite their methodological limitations, support this statement.

The first report refers to a study where protocol biopsies were performed 1, 2, 3, 6, and 12 months after transplant.
In this study, Rush et al found that detection and early treatment of SCR with corticosteroid boluses resulted in a
decreased progression of lesions at 6 months and a better kidney function at 2 years as compared to the control
group.52 In the second study, Buehrig et al reported that early detection of nephropathy by the polyomavirus using
protocol biopsies within one year of transplant allowed for modifying immunosuppression in early disease stages. At 6 months, graft survival and function in these patients were significantly superior to patients in whom the disease was detected late when a diagnostic biopsy was performed for kidney function impairment.53

In conclusion, the biopsy not only represents the best alternative for diagnostic evaluation of renal graft lesions, but is also a good tool for prognostic and viability assessment of the graft. Based on the available evidence, it has been stated that protocol biopsies could be considered as a surrogate marker for graft survival,54 and several groups of
researchers are currently focusing their efforts on the search for different lesion patterns, as well as new quantitative parameters for assessing these biopsies, that would improve their predictive value.3 Finally, the significant value of protocol biopsies as secondary endpoint in the setting of clinical trials should not be forgotten. A remarkable experience in this field has already been obtained in several studies intended to describe potential differences in the impact of the different immunosuppressive treatments on renal histology.55-58

RECOMMENDATIONS FOR PERFORMING DONOR BIOPSIES (table I)

Indications

Definite indication
In recent years, the growing disparity between the number of patients in a waiting list for receiving a kidney transplant and the number of grafts available has prompted the need for expanding the criteria for considering a kidney adequate to be transplanted (59). In 2001, the UNOS (United Network for Organ Sharing) defined expanded criteria donors (ECD&

Bibliography
[1]
Valentin MO, Garrido G, Martin Escobar E, de la Rosa G, Mahillo B, Dominguez-Gil B, et al. [Donation and kidney transplantation activity in Spain. 2006]. Nefrologia. 2007;27(4):434-8.
[2]
El-Husseini A, Sabry A, Zahran A, Shoker A. Can donor implantation renal biopsy predict long-term renal allograft outcome? Am J Nephrol. 2007;27(2):144-51. [Pubmed]
[3]
Seron D, Moreso F. Protocol biopsies in renal transplantation: prognostic value of structural monitoring. Kidney Int. 2007 Sep;72(6):690-7. [Pubmed]
[4]
Moreso F, Seron D, Blanco J, Suñer M, De Gracia R, Sanchez-Plumed J, et al. Indicación, procesamiento y diagnóstico de biopsias realizadas en España en pacientes con trasplante renal durante el año 2004. Presentado en el Congreso de la Sociedad Española de Nefrología, Cádiz, España. Octubre de 2007 [Póster # 141].
[5]
Gaber LW, Gaber AO, Tolley EA, Hathaway DK. Prediction by postrevascularization biopsies of cadaveric kidney allografts of rejection, graft loss, and preservation nephropathy. Transplantation. 1992 Jun;53(6):1219-25. [Pubmed]
[6]
Lee S, Kim JS, Cho MH, Chae DW, Kim HJ, Nam ES, et al. Relationship of renal implantation biopsies and acute rejection during the immediate posttransplantation period. Transplant Proc. 1998 Nov;30(7):3070-1. [Pubmed]
[7]
Oberbauer R, Rohrmoser M, Regele H, Muhlbacher F, Mayer G. Apoptosis of tubular epithelial cells in donor kidney biopsies predicts early renal allograft function. J Am Soc Nephrol. 1999 Sep;10(9):2006-13. [Pubmed]
[8]
Gaber LW, Moore LW, Alloway RR, Amiri MH, Vera SR, Gaber AO. Glomerulosclerosis as a determinant of posttransplant function of older donor renal allografts. Transplantation. 1995 Aug 27;60(4):334-9.
[9]
Karpinski J, Lajoie G, Cattran D, Fenton S, Zaltzman J, Cardella C, et al. Outcome of kidney transplantation from high-risk donors is determined by both structure and function. Transplantation. 1999 Apr 27;67(8):1162-7.
[10]
Eapen G, Hinduja A, Abraham G, Kuruvilla S, Panicker V, Thirumalai R, et al. Does implantation biopsy help in predicting renal allograft management and outcome? Transplant Proc. 2000 Nov;32(7):1795. [Pubmed]
[11]
Kuypers DR, Chapman JR, O'Connell PJ, Allen RD, Nankivell BJ. Predictors of renal transplant histology at three months. Transplantation. 1999 May 15;67(9):1222-30.
[12]
Bosmans JL, Woestenburg A, Ysebaert DK, Chapelle T, Helbert MJ, Corthouts R, et al. Fibrous intimal thickening at implantation as a risk factor for the outcome of cadaveric renal allografts. Transplantation. 2000 Jun 15;69(11):2388-94.
[13]
Randhawa PS, Minervini MI, Lombardero M, Duquesnoy R, Fung J, Shapiro R, et al. Biopsy of marginal donor kidneys: correlation of histologic findings with graft dysfunction. Transplantation. 2000 Apr 15;69(7):1352-7.
[14]
Cicciarelli J, Cho Y, Mateo R, El-Shahawy M, Iwaki Y, Selby R. Renal biopsy donor group: the influence of glomerulosclerosis on transplant outcomes. Transplant Proc. 2005 Mar;37(2):712-3. [Pubmed]
[15]
Howie AJ, Ferreira MA, Lipkin GW, Adu D. Measurement of chronic damage in the donor kidney and graft survival. Transplantation. 2004 Apr 15;77(7):1058-65.
[16]
Ugarte R, Kraus E, Montgomery RA, Burdick JF, Ratner L, Haas M, et al. Excellent outcomes after transplantation of deceased donor kidneys with high terminal creatinine and mild pathologic lesions. Transplantation. 2005 Sep 27;80(6):794-800.
[17]
Nankivell BJ, Fenton-Lee CA, Kuypers DR, Cheung E, Allen RD, O'Connell PJ, et al. Effect of histological damage on long-term kidney transplant outcome. Transplantation. 2001 Feb 27;71(4):515-23.
[18]
Chapman JR. Longitudinal analysis of chronic allograft nephropathy: clinicopathologic correlations. Kidney Int Suppl. 2005 Dec(99):S108-12. [Pubmed]
[19]
Nankivell BJ, Borrows RJ, Fung CL, O'Connell PJ, Chapman JR, Allen RD. Delta analysis of posttransplantation tubulointerstitial damage. Transplantation. 2004 Aug 15;78(3):434-41.
[20]
Cosio FG, Grande JP, Larson TS, Gloor JM, Velosa JA, Textor SC, et al. Kidney allograft fibrosis and atrophy early after living donor transplantation. Am J Transplant. 2005 May;5(5):1130-6. [Pubmed]
[21]
Lu AD, Desai D, Myers BD, Dafoe DC, Alfrey EJ. Severe glomerular sclerosis is not associated with poor outcome after kidney transplantation. Am J Surg. 2000 Dec;180(6):470-4. [Pubmed]
[22]
Vazquez Martul E, Veiga Barreiro A. Importance of kidney biopsy in graft selection. Transplant Proc. 2003 Aug;35(5):1658-60. [Pubmed]
[23]
Epstein M. Aging and the kidney. J Am Soc Nephrol. 1996 Aug;7(8):1106-22. [Pubmed]
[24]
Baylis C, Corman B. The aging kidney: insights from experimental studies. J Am Soc Nephrol. 1998 Apr;9(4):699-709. [Pubmed]
[25]
Rao KV, Kasiske BL, Odlund MD, Ney AL, Andersen RC. Influence of cadaver donor age on posttransplant renal function and graft outcome. Transplantation. 1990 Jan;49(1):91-5. [Pubmed]
[26]
Terasaki PI, Gjertson DW, Cecka JM, Takemoto S, Cho YW. Significance of the donor age effect on kidney transplants. Clin Transplant. 1997 Oct;11(5 Pt 1):366-72. [Pubmed]
[27]
Remuzzi G, Cravedi P, Perna A, Dimitrov BD, Turturro M, Locatelli G, et al. Long-term outcome of renal transplantation from older donors. N Engl J Med. 2006 Jan 26;354(4):343-52.
[28]
Remuzzi G, Grinyo J, Ruggenenti P, Beatini M, Cole EH, Milford EL, et al. Early experience with dual kidney transplantation in adults using expanded donor criteria. Double Kidney Transplant Group (DKG). J Am Soc Nephrol. 1999 Dec;10(12):2591-8. [Pubmed]
[29]
Lopes JA, Moreso F, Riera L, Carrera M, Ibernon M, Fulladosa X, et al. Evaluation of pre-implantation kidney biopsies: comparison of Banff criteria to a morphometric approach. Kidney Int. 2005 Apr;67(4):1595-600. [Pubmed]
[30]
Solez K, Axelsen RA, Benediktsson H, Burdick JF, Cohen AH, Colvin RB, 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 Aug;44(2):411-22. [Pubmed]
[31]
Racusen LC, Solez K, Colvin RB, Bonsib SM, Castro MC, Cavallo T, et al. The Banff 97 working classification of renal allograft pathology. Kidney Int. 1999 Feb;55(2):713-23. [Pubmed]
[32]
Racusen LC, Colvin RB, Solez K, Mihatsch MJ, Halloran PF, Campbell PM, et al. Antibody-mediated rejection criteria - an addition to the Banff 97 classification of renal allograft rejection. Am J Transplant. 2003 Jun;3(6):708-14. [Pubmed]
[33]
Solez K, Colvin RB, Racusen LC, Sis B, Halloran PF, Birk PE, et al. Banff '05 Meeting Report: differential diagnosis of chronic allograft injury and elimination of chronic allograft nephropathy ('CAN'). Am J Transplant. 2007 Mar;7(3):518-26. [Pubmed]
[34]
Colvin RB, Cohen AH, Saiontz C, Bonsib S, Buick M, Burke B, et al. Evaluation of pathologic criteria for acute renal allograft rejection: reproducibility, sensitivity, and clinical correlation. J Am Soc Nephrol. 1997 Dec;8(12):1930-41. [Pubmed]
[35]
Mueller A, Schnuelle P, Waldherr R, van der Woude FJ. Impact of the Banff '97 classification for histological diagnosis of rejection on clinical outcome and renal function parameters after kidney transplantation. Transplantation. 2000 Mar 27;69(6):1123-7.
[36]
Nankivell BJ, Borrows RJ, Fung CL, O'Connell PJ, Allen RD, Chapman JR. The natural history of chronic allograft nephropathy. N Engl J Med. 2003 Dec 11;349(24):2326-33.
[37]
Rush DN, Jeffery JR, Gough J. Sequential protocol biopsies in renal transplant patients. Clinico-pathological correlations using the Banff schema. Transplantation. 1995 Feb 27;59(4):511-4.
[38]
Nankivell BJ, Borrows RJ, Fung CL, O'Connell PJ, Allen RD, Chapman JR. Natural history, risk factors, and impact of subclinical rejection in kidney transplantation. Transplantation. 2004 Jul 27;78(2):242-9.
[39]
Mengel M, Gwinner W, Schwarz A, Bajeski R, Franz I, Brocker V, et al. Infiltrates in protocol biopsies from renal allografts. Am J Transplant. 2007 Feb;7(2):356-65. [Pubmed]
[40]
Legendre C, Thervet E, Skhiri H, Mamzer-Bruneel MF, Cantarovich F, Noel LH, et al. Histologic features of chronic allograft nephropathy revealed by protocol biopsies in kidney transplant recipients. Transplantation. 1998 Jun 15;65(11):1506-9.
[41]
Moreso F, Ibernon M, Goma M, Carrera M, Fulladosa X, Hueso 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 Apr;6(4):747-52. [Pubmed]
[42]
Choi BS, Shin MJ, Shin SJ, Kim YS, Choi YJ, Moon IS, 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 Jun;5(6):1354-60. [Pubmed]
[43]
Seron D, Moreso F, Fulladosa X, Hueso M, Carrera M, Grinyo JM. Reliability of chronic allograft nephropathy diagnosis in sequential protocol biopsies. Kidney Int. 2002 Feb;61(2):727-33. [Pubmed]
[44]
Fulladosa X, Moreso F, Torras J, Hueso M, Grinyo JM, Seron D. Structural and functional correlations in stable renal allografts. Am J Kidney Dis. 2003 May;41(5):1065-73. [Pubmed]
[45]
Isoniemi HM, Krogerus L, von Willebrand E, Taskinen E, Ahonen J, Hayry P. Histopathological findings in well-functioning, long-term renal allografts. Kidney Int. 1992 Jan;41(1):155-60. [Pubmed]
[46]
Yilmaz S, Tomlanovich S, Mathew T, Taskinen E, Paavonen T, Navarro M, et al. Protocol core needle biopsy and histologic Chronic Allograft Damage Index (CADI) as surrogate end point for long-term graft survival in multicenter studies. J Am Soc Nephrol. 2003 Mar;14(3):773-9. [Pubmed]
[47]
Dimeny E, Wahlberg J, Larsson E, Fellstrom B. Can histopathological findings in early renal allograft biopsies identify patients at risk for chronic vascular rejection? Clin Transplant. 1995 Apr;9(2):79-84. [Pubmed]
[48]
Seron D, Moreso F, Bover J, Condom E, Gil-Vernet S, Canas C, et al. Early protocol renal allograft biopsies and graft outcome. Kidney Int. 1997 Jan;51(1):310-6. [Pubmed]
[49]
Seron D, Moreso F, Ramon JM, Hueso M, Condom E, Fulladosa X, et al. Protocol renal allograft biopsies and the design of clinical trials aimed to prevent or treat chronic allograft nephropathy. Transplantation. 2000 May 15;69(9):1849-55.
[50]
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 Oct;5(10):2464-72. [Pubmed]
[51]
Shishido S, Asanuma H, Nakai H, Mori Y, Satoh H, Kamimaki I, et al. The impact of repeated subclinical acute rejection on the progression of chronic allograft nephropathy. J Am Soc Nephrol. 2003 Apr;14(4):1046-52. [Pubmed]
[52]
Rush D, Nickerson P, Gough J, McKenna R, Grimm P, Cheang M, et al. Beneficial effects of treatment of early subclinical rejection: a randomized study. J Am Soc Nephrol. 1998 Nov;9(11):2129-34. [Pubmed]
[53]
Buehrig CK, Lager DJ, Stegall MD, Kreps MA, Kremers WK, Gloor JM, et al. Influence of surveillance renal allograft biopsy on diagnosis and prognosis of polyomavirus-associated nephropathy. Kidney Int. 2003 Aug;64(2):665-73. [Pubmed]
[54]
Lachenbruch PA, Rosenberg AS, Bonvini E, Cavaille-Coll MW, Colvin RB. Biomarkers and surrogate endpoints in renal transplantation: present status and considerations for clinical trial design. Am J Transplant. 2004 Apr;4(4):451-7. [Pubmed]
[55]
Larson TS, Dean PG, Stegall MD, Griffin MD, Textor SC, Schwab TR, et al. Complete avoidance of calcineurin inhibitors in renal transplantation: a randomized trial comparing sirolimus and tacrolimus. Am J Transplant. 2006 Mar;6(3):514-22. [Pubmed]
[56]
Vincenti F, Larsen C, Durrbach A, Wekerle T, Nashan B, Blancho G, et al. Costimulation blockade with belatacept in renal transplantation. N Engl J Med. 2005 Aug 25;353(8):770-81.
[57]
Solez K, Vincenti F, Filo RS. Histopathologic findings from 2-year protocol biopsies from a U.S. multicenter kidney transplant trial comparing tarolimus versus cyclosporine: a report of the FK506 Kidney Transplant Study Group. Transplantation. 1998 Dec 27;66(12):1736-40.
[58]
Flechner SM, Kurian SM, Solez K, Cook DJ, Burke JT, Rollin H, et al. De novo kidney transplantation without use of calcineurin inhibitors preserves renal structure and function at two years. Am J Transplant. 2004 Nov;4(11):1776-85. [Pubmed]
[59]
Morales J, Andrés A, Pallardó L, Capdevila L, Campistol J, Gil Vernet J, et al. Trasplante renal en pacientes de edad avanzada con un riñón de donante añoso. Nefrologia. 1998;18(Suplemento 5):32-47.
[60]
Rosengard BR, Feng S, Alfrey EJ, Zaroff JG, Emond JC, Henry ML, et al. Report of the Crystal City meeting to maximize the use of organs recovered from the cadaver donor. Am J Transplant. 2002 Sep;2(8):701-11. [Pubmed]
[61]
Whiting JF. Clinical and economic outcomes of the use of expanded criteria donors in renal transplantation. Semin Dial. 2000 Sep-Oct;13(5):316-9. [Pubmed]
[62]
Metzger RA, Delmonico FL, Feng S, Port FK, Wynn JJ, Merion RM. Expanded criteria donors for kidney transplantation. Am J Transplant. 2003;3 Suppl 4:114-25.
[63]
Ojo AO, Leichtman AB, Punch JD, Hanson JA, Dickinson DM, Wolfe RA, et al. Impact of pre-existing donor hypertension and diabetes mellitus on cadaveric renal transplant outcomes. Am J Kidney Dis. 2000 Jul;36(1):153-9. [Pubmed]
[64]
Scheiden R, Sand J, Tanous AM, Knolle U, Capesius C, Wagnon MC, et al. Accuracy of frozen section diagnoses of breast lesions after introduction of a national programme in mammographic screening. Histopathology. 2001 Jul;39(1):74-84. [Pubmed]
[65]
Kok, LP and Boon ME: Microwawes for the art of microscopy. Coulomb Press Leyden, Leyden, 2003, ISBN 90-71421-41-4.
[66]
Junta de Andalucía, Consejería de Salud. Proceso asistencial: Tratamiento sustitutivo de la insuficiencia renal crónica : diálisis y trasplante renal. (consultado en http://www.juntadeandalucia.es/salud/procesos/documentos.asp?idp=154 el 10 de diciembre del 2007).
[67]
Solez K, Colvin RB, Racusen LC, Haas M, Sis B, Mengel M, et al. Banff 07 classification of renal allograft pathology: updates and future directions. Am J Transplant. 2008 Apr;8(4):753-60. [Pubmed]
[68]
Perico N, Cattaneo D, Sayegh MH, Remuzzi G. Delayed graft function in kidney transplantation. Lancet. 2004 Nov 13-19;364(9447):1814-27.
[69]
Koning OH, Ploeg RJ, van Bockel JH, Groenewegen M, van der Woude FJ, Persijn GG, et al. Risk factors for delayed graft function in cadaveric kidney transplantation: a prospective study of renal function and graft survival after preservation with University of Wisconsin solution in multi-organ donors. European Multicenter Study Group. Transplantation. 1997 Jun 15;63(11):1620-8.
[70]
European Best Practice Guidelines for Renal Transplantation (part 1). Nephrol Dial Transplant. 2000;15 Suppl 7:1-85. [Pubmed]
[71]
Vadivel N, Tullius SG, Chandraker A. Chronic allograft nephropathy. Semin Nephrol. 2007 Jul;27(4):414-29. [Pubmed]
[72]
Paul LC, Hayry P, Foegh M, Dennis MJ, Mihatsch MJ, Larsson E, et al. Diagnostic criteria for chronic rejection/accelerated graft atherosclerosis in heart and kidney transplants: joint proposal from the Fourth Alexis Carrel Conference on Chronic Rejection and Accelerated Arteriosclerosis in Transplanted Organs. Transplant Proc. 1993 Apr;25(2):2022-3. [Pubmed]
[73]
Dudley C, Pohanka E, Riad H, Dedochova J, Wijngaard P, Sutter C, et al. Mycophenolate mofetil substitution for cyclosporine a in renal transplant recipients with chronic progressive allograft dysfunction: the "creeping creatinine" study. Transplantation. 2005 Feb 27;79(4):466-75.
[74]
Vidhun J, Masciandro J, Varich L, Salvatierra O, Jr., Sarwal M. Safety and risk stratification of percutaneous biopsies of adult-sized renal allografts in infant and older pediatric recipients. Transplantation. 2003 Aug 15;76(3):552-7.
[75]
Nicholson ML, Wheatley TJ, Doughman TM, White SA, Morgan JD, Veitch PS, et al. A prospective randomized trial of three different sizes of core-cutting needle for renal transplant biopsy. Kidney Int. 2000 Jul;58(1):390-5. [Pubmed]
[76]
Kim D, Kim H, Shin G, Ku S, Ma K, Shin S, et al. A randomized, prospective, comparative study of manual and automated renal biopsies. Am J Kidney Dis. 1998 Sep;32(3):426-31. [Pubmed]
[77]
Mauiyyedi S, Crespo M, Collins AB, Schneeberger EE, Pascual MA, Saidman SL, et al. Acute humoral rejection in kidney transplantation: II. Morphology, immunopathology, and pathologic classification. J Am Soc Nephrol. 2002 Mar;13(3):779-87. [Pubmed]
[78]
Mauiyyedi S, Pelle PD, Saidman S, Collins AB, Pascual M, Tolkoff-Rubin NE, et al. Chronic humoral rejection: identification of antibody-mediated chronic renal allograft rejection by C4d deposits in peritubular capillaries. J Am Soc Nephrol. 2001 Mar;12(3):574-82. [Pubmed]
[79]
Regele H, Bohmig GA, Habicht A, Gollowitzer D, Schillinger M, Rockenschaub S, et al. Capillary deposition of complement split product C4d in renal allografts is associated with basement membrane injury in peritubular and glomerular capillaries: a contribution of humoral immunity to chronic allograft rejection. J Am Soc Nephrol. 2002 Sep;13(9):2371-80. [Pubmed]
[80]
Seemayer CA, Gaspert A, Nickeleit V, Mihatsch MJ. C4d staining of renal allograft biopsies: a comparative analysis of different staining techniques. Nephrol Dial Transplant. 2007 Feb;22(2):568-76. [Pubmed]
[81]
Seron D, O'Valle F, Moreso F, Goma M, Hueso M, Grinyo JM, et al. Immunophenotype of infiltrating cells in protocol renal allograft biopsies from tacrolimus-versus cyclosporine-treated patients. Transplantation. 2007 Mar 15;83(5):649-52.
[82]
Moreso F, Seron D, O'Valle F, Ibernon M, Goma M, Hueso M, et al. Immunephenotype of glomerular and interstitial infiltrating cells in protocol renal allograft biopsies and histological diagnosis. Am J Transplant. 2007 Dec;7(12):2739-47. [Pubmed]
[83]
Kayler LK, Lakkis FG, Morgan C, Basu A, Blisard D, Tan HP, et al. Acute cellular rejection with CD20-positive lymphoid clusters in kidney transplant patients following lymphocyte depletion. Am J Transplant. 2007 Apr;7(4):949-54. [Pubmed]
[84]
Grimbert P, Mansour H, Desvaux D, Roudot-Thoraval F, Audard V, Dahan K, et al. The regulatory/cytotoxic graft-infiltrating T cells differentiate renal allograft borderline change from acute rejection. Transplantation. 2007 Feb 15;83(3):341-6.
[85]
Aita K, Yamaguchi Y, Horita S, Ohno M, Tanabe K, Fuchinoue S, et al. Thickening of the peritubular capillary basement membrane is a useful diagnostic marker of chronic rejection in renal allografts. Am J Transplant. 2007 Apr;7(4):923-9. [Pubmed]
[86]
Ivanyi B, Kemeny E, Szederkenyi E, Marofka F, Szenohradszky P. The value of electron microscopy in the diagnosis of chronic renal allograft rejection. Mod Pathol. 2001 Dec;14(12):1200-8. [Pubmed]
[87]
Oberbauer R, Segoloni G, Campistol JM, Kreis H, Mota A, Lawen J, et al. Early cyclosporine withdrawal from a sirolimus-based regimen results in better renal allograft survival and renal function at 48 months after transplantation. Transpl Int. 2005 Jan;18(1):22-8. [Pubmed]
Idiomas
Nefrología (English Edition)
Article options
Tools
es en

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

Are you a health professional able to prescribe or dispense drugs?