Immunological Assessment and Monitoring in Kidney Transplantation
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  • 1 Paris Translational Research Center for Organ Transplantation, Institut National de la Santé et de la Recherche Médicale UMR-S970, University of Paris, Paris, France; and
  • | 2 Kidney Transplant Department, Saint Louis Hospital, Assistance Publique–Hôpitaux de Paris, Paris, France
  • | 3 Paris Translational Research Center for Organ Transplantation, Institut National de la Santé et de la Recherche Médicale UMR-S970, University of Paris, Paris, France; and
  • | 4 Kidney Transplant Department, Necker Hospital, Assistance Publique–Hôpitaux de Paris, Paris, France
  • 1

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  • 3

    Loupy A, Vernerey D, Tinel C, Aubert O, Duong van Huyen J-P, Rabant M, et al.: Subclinical rejection phenotypes at 1 year post-transplant and outcome of kidney allografts. J Am Soc Nephrol 26: 17211731, 2015 PubMed

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  • 4

    Lefaucheur C, Gosset C, Rabant M, Viglietti D, Verine J, Aubert O, et al.: T cell-mediated rejection is a major determinant of inflammation in scarred areas in kidney allografts. Am J Transplant 18: 377390, 2018 PubMed

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  • 5

    Loupy A, Lefaucheur C: Antibody-mediated rejection of solid-organ allografts. N Engl J Med 379: 11501160, 2018 PubMed

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    Maggiore U, Leventhal J, Cravedi P: Rethinking clinical endpoints in kidney transplant trials. Curr Opin Organ Transplant 25: 17, 2020 PubMed

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    Haas M, Loupy A, Lefaucheur C, Roufosse C, Glotz D, Seron D, et al.: The Banff 2017 Kidney Meeting Report: Revised diagnostic criteria for chronic active T cell-mediated rejection, antibody-mediated rejection, and prospects for integrative endpoints for next-generation clinical trials. Am J Transplant 18: 293307, 2018 PubMed

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  • 8

    Bestard O, Couzi L, Crespo M, Kessaris N, Thaunat O: Stratifying the humoral risk of candidates to a solid organ transplantation: A proposal of the ENGAGE working group. Transpl Int 34: 10051018, 2021 PubMed

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  • 9

    Terasaki PI, Cai J: Human leukocyte antigen antibodies and chronic rejection: From association to causation. Transplantation 86: 377383, 2008 PubMed

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    Tait BD, Süsal C, Gebel HM, Nickerson PW, Zachary AA, Claas FHJ, et al.: Consensus guidelines on the testing and clinical management issues associated with HLA and non-HLA antibodies in transplantation. Transplantation 95: 1947, 2013 PubMed

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  • 11

    Konvalinka A, Tinckam K: Utility of HLA antibody testing in kidney transplantation. J Am Soc Nephrol 26: 14891502, 2015 PubMed

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    Montgomery RA, Tatapudi VS, Leffell MS, Zachary AA: HLA in transplantation. Nat Rev Nephrol 14: 558570, 2018 PubMed

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    Tambur AR, Campbell P, Chong AS, Feng S, Ford ML, Gebel H, et al.: Sensitization in transplantation: Assessment of risk (STAR) 2019 Working Group Meeting Report. Am J Transplant 20: 26522668, 2020 PubMed

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  • 15

    Loupy A, Haas M, Roufosse C, Naesens M, Adam B, Afrouzian M, et al.: The Banff 2019 Kidney Meeting Report (I): Updates on and clarification of criteria for T cell- and antibody-mediated rejection. Am J Transplant 20: 23182331, 2020

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  • 16

    Senev A, Lerut E, Van Sandt V, Coemans M, Callemeyn J, Sprangers B, et al.: Specificity, strength, and evolution of pretransplant donor-specific HLA antibodies determine outcome after kidney transplantation. Am J Transplant 19: 31003113, 2019 PubMed

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  • 17

    Dipchand AI, Webber S, Mason K, Feingold B, Bentlejewski C, Mahle WT, et al.; CTOTC-04 Investigators: Incidence, characterization, and impact of newly detected donor-specific anti-HLA antibody in the first year after pediatric heart transplantation: A report from the CTOTC-04 study. Am J Transplant 18: 21632174, 2018 PubMed

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  • 18

    Iasella CJ, Ensor CR, Marrari M, Mangiola M, Xu Q, Nolley E, et al.: Donor-specific antibody characteristics, including persistence and complement-binding capacity, increase risk for chronic lung allograft dysfunction. J Heart Lung Transplant 39: 14171425, 2020 PubMed

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  • 19

    Vandevoorde K, Ducreux S, Bosch A, Guillaud O, Hervieu V, Chambon-Augoyard C, et al.: Prevalence, risk factors, and impact of donor-specific alloantibodies after adult liver transplantation. Liver Transpl 24: 10911100, 2018 PubMed

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  • 20

    Huang Y, Dinh A, Heron S, Gasiewski A, Kneib C, Mehler H, et al.: Assessing the utilization of high-resolution 2-field HLA typing in solid organ transplantation. Am J Transplant 19: 19551963, 2019 PubMed

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  • 21

    Smith AG, Pereira S, Jaramillo A, Stoll ST, Khan FM, Berka N, et al.: Comparison of sequence-specific oligonucleotide probe vs next generation sequencing for HLA-A, B, C, DRB1, DRB3/B4/B5, DQA1, DQB1, DPA1, and DPB1 typing: Toward single-pass high-resolution HLA typing in support of solid organ and hematopoietic cell transplant programs. HLA 94: 296306, 2019 PubMed

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  • 22

    Senev A, Emonds M-P, Van Sandt V, Lerut E, Coemans M, Sprangers B, et al.: Clinical importance of extended second field high-resolution HLA genotyping for kidney transplantation. Am J Transplant 20: 33673378, 2020 PubMed

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  • 23

    Redondo-Pachón D, Pérez-Sáez MJ, Mir M, Gimeno J, Llinás L, García C, et al.: Impact of persistent and cleared preformed HLA DSA on kidney transplant outcomes. Hum Immunol 79: 424431, 2018 PubMed

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  • 24

    Mohan S, Palanisamy A, Tsapepas D, Tanriover B, Crew RJ, Dube G, et al.: Donor-specific antibodies adversely affect kidney allograft outcomes. J Am Soc Nephrol 23: 20612071, 2012 PubMed

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  • 25

    Viglietti D, Loupy A, Vernerey D, Bentlejewski C, Gosset C, Aubert O, et al.: Value of donor-specific anti-HLA antibody monitoring and characterization for risk stratification of kidney allograft loss. J Am Soc Nephrol 28: 702715, 2017 PubMed

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  • 26

    Buttigieg J, Ali H, Sharma A, Halawa A: Positive Luminex and negative flow cytometry in kidney transplantation: A systematic review and meta-analysis. Nephrol Dial Transplant 34: 19501960, 2019 PubMed

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  • 27

    Morrison AH, Gupta M, Lloyd K, Trofe-Clark J, Ann Lim M, Limonte C, et al.: Class and kinetics of weakly reactive pretransplant donor-specific HLA antibodies predict rejection in kidney transplant recipients. Transplant Direct 5: e478, 2019 PubMed

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  • 28

    Kamburova EG, Wisse BW, Joosten I, Allebes WA, van der Meer A, Hilbrands LB, et al.: Differential effects of donor-specific HLA antibodies in living versus deceased donor transplant. Am J Transplant 18: 22742284, 2018 PubMed

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  • 29

    Ziemann M, Altermann W, Angert K, Arns W, Bachmann A, Bakchoul T, et al.: Preformed donor-specific HLA antibodies in living and deceased donor transplantation: A multicenter study. Clin J Am Soc Nephrol 14: 10561066, 2019 PubMed

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  • 30

    Michielsen LA, Wisse BW, Kamburova EG, Verhaar MC, Joosten I, Allebes WA, et al.: A paired kidney analysis on the impact of pre-transplant anti-HLA antibodies on graft survival. Nephrol Dial Transplant 34: 10561063, 2019

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  • 31

    Zecher D, Bach C, Staudner C, Böger CA, Bergler T, Banas B, et al.: Characteristics of donor-specific anti-HLA antibodies and outcome in renal transplant patients treated with a standardized induction regimen. Nephrol Dial Transplant 32: 730737, 2017 PubMed

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  • 32

    Lucisano G, Thiruvengadam S, Hassan S, Gueret-Wardle A, Brookes P, Santos-Nunez E, et al.: Donor-specific antibodies detected by single antigen beads alone can help risk stratify patients undergoing retransplantation across a repeat HLA mismatch. Am J Transplant 20: 441450, 2020 PubMed

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  • 33

    Loupy A, Suberbielle-Boissel C, Hill GS, Lefaucheur C, Anglicheau D, Zuber J, et al.: Outcome of subclinical antibody-mediated rejection in kidney transplant recipients with preformed donor-specific antibodies. Am J Transplant 9: 25612570, 2009 PubMed

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  • 34

    Loupy A, Lefaucheur C, Vernerey D, Chang J, Hidalgo LG, Beuscart T, et al.: Molecular microscope strategy to improve risk stratification in early antibody-mediated kidney allograft rejection. J Am Soc Nephrol 25: 22672277, 2014 PubMed

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  • 35

    Snanoudj R, Kamar N, Cassuto E, Caillard S, Metzger M, Merville P, et al.: Epitope load identifies kidney transplant recipients at risk of allosensitization following minimization of immunosuppression. Kidney Int 95: 14711485, 2019 PubMed

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  • 36

    Sharma A, Cherukuri A, Mehta RB, Sood P, Hariharan S: High calcineurin inhibitor intrapatient variability is associated with renal allograft inflammation, chronicity, and graft loss. Transplant Direct 5: e424, 2019 PubMed

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  • 37

    Wiebe C, Rush DN, Nevins TE, Birk PE, Blydt-Hansen T, Gibson IW, et al.: Class II eplet mismatch modulates tacrolimus trough levels required to prevent donor-specific antibody development. J Am Soc Nephrol 28: 33533362, 2017 PubMed

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  • 38

    Mendoza Rojas A, Hesselink DA, van Besouw NM, Baan CC, van Gelder T: Impact of low tacrolimus exposure and high tacrolimus intra-patient variability on the development of de novo anti-HLA donor-specific antibodies in kidney transplant recipients. Expert Rev Clin Immunol 15: 13231331, 2019 PubMed

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  • 39

    Davis S, Wiebe C, Campbell K, Anobile C, Aubrey M, Stites E, et al.: Adequate tacrolimus exposure modulates the impact of HLA class II molecular mismatch: A validation study in an American cohort. Am J Transplant 21: 322328, 2021 PubMed

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  • 40

    Yamamoto T, Watarai Y, Takeda A, Tsujita M, Hiramitsu T, Goto N, et al.: De novo anti-HLA DSA characteristics and subclinical antibody-mediated kidney allograft injury. Transplantation 100: 21942202, 2016 PubMed

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  • 41

    Schinstock CA, Cosio F, Cheungpasitporn W, Dadhania DM, Everly MJ, Samaniego-Picota MD, et al.: The value of protocol biopsies to identify patients with de novo donor-specific antibody at high risk for allograft loss. Am J Transplant 17: 15741584, 2017 PubMed

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  • 42

    Parajuli S, Reville PK, Ellis TM, Djamali A, Mandelbrot DA: Utility of protocol kidney biopsies for de novo donor-specific antibodies. Am J Transplant 17: 32103218, 2017 PubMed

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  • 43

    Wiebe C, Gareau AJ, Pochinco D, Gibson IW, Ho J, Birk PE, et al.: Evaluation of C1q status and titer of de novo donor-specific antibodies as predictors of allograft survival. Am J Transplant 17: 703711, 2017 PubMed

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  • 44

    Bertrand D, Gatault P, Jauréguy M, Garrouste C, Sayegh J, Bouvier N, et al.: Protocol biopsies in patients with subclinical de novo donor-specific antibodies after kidney transplantation: A multicentric study. Transplantation 104: 17261737, 2020 PubMed

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  • 45

    Aubert O, Loupy A, Hidalgo L, Duong van Huyen J-P, Higgins S, Viglietti D, et al.: Antibody-mediated rejection due to preexisting versus de novo donor-specific antibodies in kidney allograft recipients. J Am Soc Nephrol 28: 19121923, 2017 PubMed

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  • 46

    Haas M, Mirocha J, Reinsmoen NL, Vo AA, Choi J, Kahwaji JM, et al.: Differences in pathologic features and graft outcomes in antibody-mediated rejection of renal allografts due to persistent/recurrent versus de novo donor-specific antibodies. Kidney Int 91: 729737, 2017 PubMed

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  • 47

    Lefaucheur C, Louis K, Philippe A, Loupy A, Coates PT: The emerging field of non-human leukocyte antigen antibodies in transplant medicine and beyond. Kidney Int 100: 787798, 2021 PubMed

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  • 48

    Callemeyn J, Lerut E, de Loor H, Arijs I, Thaunat O, Koenig A, et al.: Transcriptional changes in kidney allografts with histology of antibody-mediated rejection without anti-HLA donor-specific antibodies. J Am Soc Nephrol 31: 21682183, 2020 PubMed

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  • 49

    Senev A, Coemans M, Lerut E, Van Sandt V, Daniëls L, Kuypers D, et al.: Histological picture of antibody-mediated rejection without donor-specific anti-HLA antibodies: Clinical presentation and implications for outcome. Am J Transplant 19: 763780, 2019 PubMed

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  • 50

    Bestard O, Grinyó J: Refinement of humoral rejection effector mechanisms to identify specific pathogenic histological lesions with different graft outcomes. Am J Transplant 19: 952953, 2019 PubMed

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  • 51

    Schinstock CA, Mannon RB, Budde K, Chong AS, Haas M, Knechtle S, et al.: Recommended treatment for antibody-mediated rejection after kidney transplantation: The 2019 Expert Consensus From the Transplantation Society Working Group. Transplantation 104: 911922, 2020 PubMed

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  • 52

    Viglietti D, Loupy A, Aubert O, Bestard O, Duong Van Huyen J-P, Taupin J-L, et al.: Dynamic prognostic score to predict kidney allograft survival in patients with antibody-mediated rejection. J Am Soc Nephrol 29: 606619, 2018 PubMed

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  • 53

    Jordan SC, Lorant T, Choi J, Kjellman C, Winstedt L, Bengtsson M, et al.: IgG Endopeptidase in highly sensitized patients undergoing transplantation. N Engl J Med 377: 442453, 2017 PubMed

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  • 54

    Lefaucheur C, Viglietti D, Hidalgo LG, Ratner LE, Bagnasco SM, Batal I, et al.: Complement-activating anti-HLA antibodies in kidney transplantation: Allograft gene expression profiling and response to treatment. J Am Soc Nephrol 29: 620635, 2018 PubMed

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  • 55

    Bailly E, Anglicheau D, Blancho G, Gatault P, Vuiblet V, Chatelet V, et al.: Prognostic value of the persistence of C1q-binding anti-HLA antibodies in acute antibody-mediated rejection in kidney transplantation. Transplantation 102: 688698, 2018 PubMed

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  • 56

    Viglietti D, Bouatou Y, Kheav VD, Aubert O, Suberbielle-Boissel C, Glotz D, et al.: Complement-binding anti-HLA antibodies are independent predictors of response to treatment in kidney recipients with antibody-mediated rejection. Kidney Int 94: 773787, 2018 PubMed

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  • 57

    Tambur AR, Herrera ND, Haarberg KMK, Cusick MF, Gordon RA, Leventhal JR, et al.: Assessing antibody strength: Comparison of MFI, C1q, and titer information. Am J Transplant 15: 24212430, 2015 PubMed

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  • 58

    Gebel HM, Bray RA: A diagnostic ‘C’ saw: The ups and downs of C1q testing. Curr Opin Organ Transplant 24: 402410, 2019 PubMed

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    Tambur AR, Schinstock C, Maguire C, Lowe D, Smith B, Stegall M: Estimating alloantibody levels in highly sensitized renal allograft candidates: Using serial dilutions to demonstrate a treatment effect in clinical trials. Am J Transplant 21: 12781284, 2021 PubMed

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  • 60

    Loupy A, Aubert O, Orandi BJ, Naesens M, Bouatou Y, Raynaud M, et al.: Prediction system for risk of allograft loss in patients receiving kidney transplants: International derivation and validation study. BMJ 366: l4923, 2019 PubMed

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  • 62

    Bouquegneau A, Loheac C, Aubert O, Bouatou Y, Viglietti D, Empana J-P, et al.: Complement-activating donor-specific anti-HLA antibodies and solid organ transplant survival: A systematic review and meta-analysis. PLoS Med 15: e1002572, 2018 PubMed

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  • 63

    Guidicelli G, Guerville F, Lepreux S, Wiebe C, Thaunat O, Dubois V, et al.: Non-complement-binding de novo donor-specific anti-HLA antibodies and kidney allograft survival. J Am Soc Nephrol 27: 615625, 2016 PubMed

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  • 64

    Kamburova EG, Wisse BW, Joosten I, Allebes WA, van der Meer A, Hilbrands LB, et al.: Pretransplant C3d-fixing donor-specific anti-HLA antibodies are not associated with increased risk for kidney graft failure. J Am Soc Nephrol 29: 22792285, 2018 PubMed

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  • 65

    Calp-Inal S, Ajaimy M, Melamed ML, Savchik C, Masiakos P, Colovai A, et al.: The prevalence and clinical significance of C1q-binding donor-specific anti-HLA antibodies early and late after kidney transplantation. Kidney Int 89: 209216, 2016 PubMed

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  • 66

    Comoli P, Cioni M, Tagliamacco A, Quartuccio G, Innocente A, Fontana I, et al.: Acquisition of C3d-binding activity by de novo donor-specific HLA antibodies correlates with graft loss in nonsensitized pediatric kidney recipients. Am J Transplant 16: 21062116, 2016 PubMed

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    Lefaucheur C, Viglietti D, Bentlejewski C, Duong van Huyen J-P, Vernerey D, Aubert O, et al.: IgG donor-specific anti-human HLA antibody subclasses and kidney allograft antibody-mediated injury. J Am Soc Nephrol 27: 293304, 2016 PubMed

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    Thomas KA, Valenzuela NM, Reed EF: The perfect storm: HLA antibodies, complement, FcγRs, and endothelium in transplant rejection. Trends Mol Med 21: 319329, 2015 PubMed

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    Jackson AM, Kanaparthi S, Burrell BE, Lucas DP, Vega RM, Demetris AJ, et al.: IgG4 donor-specific HLA antibody profile is associated with subclinical rejection in stable pediatric liver recipients. Am J Transplant 20: 513524, 2020 PubMed

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    Pineda S, Sigdel TK, Chen J, Jackson AM, Sirota M, Sarwal MM: Novel non-histocompatibility antigen mismatched variants improve the ability to predict antibody-mediated rejection risk in kidney transplant. Front Immunol 8: 1687, 2017 PubMed

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    Zorn E, See SB: Is there a role for natural antibodies in rejection following transplantation? Transplantation 103: 16121619, 2019 PubMed

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    Delville M, Lamarthée B, Pagie S, See SB, Rabant M, Burger C, et al.: Early acute microvascular kidney transplant rejection in the absence of anti-HLA antibodies is associated with preformed IgG antibodies against diverse glomerular endothelial cell antigens. J Am Soc Nephrol 30: 692709, 2019 PubMed

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    Min JW, Lee H, Choi BS, Park CW, Yang CW, Kim YS, et al.: Clinical impact of pre-transplant antibodies against angiotensin II type I receptor and major histocompatibility complex class I-related chain A in kidney transplant patients. Ann Lab Med 38: 450457, 2018 PubMed

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    Philogene MC, Zhou S, Lonze BE, Bagnasco S, Alasfar S, Montgomery RA, et al.: Pre-transplant screening for non-HLA antibodies: Who should be tested? Hum Immunol 79: 195202, 2018 PubMed

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    Pearl MH, Zhang Q, Palma Diaz MF, Grotts J, Rossetti M, Elashoff D, et al.: Angiotensin II type 1 receptor antibodies are associated with inflammatory cytokines and poor clinical outcomes in pediatric kidney transplantation. Kidney Int 93: 260269, 2018 PubMed

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    Lefaucheur C, Viglietti D, Bouatou Y, Philippe A, Pievani D, Aubert O, et al.: Non-HLA agonistic anti-angiotensin II type 1 receptor antibodies induce a distinctive phenotype of antibody-mediated rejection in kidney transplant recipients. Kidney Int 96: 189201, 2019 PubMed

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    Pinelli DF, Friedewald JJ, Haarberg KMK, Radhakrishnan SL, Zitzner JR, Hanshew WE, et al.: Assessing the potential of angiotensin II type 1 receptor and donor specific anti-endothelial cell antibodies to predict long-term kidney graft outcome. Hum Immunol 78: 421427, 2017 PubMed

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    Gareau AJ, Wiebe C, Pochinco D, Gibson IW, Ho J, Rush DN, et al.: Pre-transplant AT1R antibodies correlate with early allograft rejection. Transpl Immunol 46: 2935, 2018 PubMed

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    Fichtner A, Süsal C, Schröder C, Höcker B, Rieger S, Waldherr R, et al.: Association of angiotensin II type 1 receptor antibodies with graft histology, function and survival in paediatric renal transplant recipients. Nephrol Dial Transplant 33: 10651072, 2018 PubMed

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    Pearl MH, Chen L, ElChaki R, Elashoff D, Gjertson DW, Rossetti M, et al.: Endothelin type A receptor antibodies are associated with angiotensin II type 1 receptor antibodies, vascular inflammation, and decline in renal function in pediatric kidney transplantation. Kidney Int Rep 5: 19251936, 2020 PubMed

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    Loupy A, Haas M, Solez K, Racusen L, Glotz D, Seron D, et al.: The Banff 2015 Kidney Meeting Report: Current challenges in rejection classification and prospects for adopting molecular pathology. Am J Transplant 17: 2841, 2017 PubMed

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