25-hydroxyvitamin D sufficiency is associated with lower de novo anti-HLA donor specific antibody and better kidney transplant outcomes.
donor-specific antibodies
graft loss
immunomodulation
kidney transplantation
vitamin D
Journal
HLA
ISSN: 2059-2310
Titre abrégé: HLA
Pays: England
ID NLM: 101675570
Informations de publication
Date de publication:
21 Aug 2023
21 Aug 2023
Historique:
revised:
30
06
2023
received:
09
03
2023
accepted:
28
07
2023
medline:
22
8
2023
pubmed:
22
8
2023
entrez:
21
8
2023
Statut:
aheadofprint
Résumé
T-cell mediated rejection (TCMR), de novo anti-HLA donor-specific antibodies (dnDSAs) and ensuing antibody-mediated rejection (ABMR) reduce kidney transplantation (KT) survival. The immunomodulatory effects of 25-hydroxyvitamin D [25(OH)D] could be beneficial for KT outcomes. We aimed to evaluating the association between 25(OH)D levels, the development of dnDSAs, clinical TCMR and ABMR, and graft survival. This single center retrospective study included 253 KT recipients (KTRs) transplanted without preformed DSA between 2010 and 2013. We measured 25(OH)D in successive serum samples: at KT (M0) and M12 for the entire cohort, and additionally at M24 and/or M36 when sera were available. We assessed graft outcomes up to 5 years post-KT. The proportion of KTRs having sufficient 25(OH)D at KT (M0) was high (81.4%) and then dropped at M12 (71.1%). KTRs with sufficient 25(OH)D at M0 experienced less clinical TCMR (HR, 0.41; 95% CI, 0.19-0.88 in multivariate analysis). A sufficient 25(OH)D at M12 was independently associated with a longer dnDSA-free survival (HR, 0.34; 95% CI, 0.17-0.69). There was no association between 25(OH)D and clinical AMBR. Studying the KTRs with 25(OH)D measurements at M12, M24 and M36 (n = 203), we showed that 25(OH)D sufficiency over the 3 first-years post-KT was associated with a longer graft survival in multivariate analyses (HR, 0.39; 95% CI, 0.22-0.70). To our knowledge, this study is the first showing an association between 25(OH)D sufficiency post-KT and dnDSA occurrence in KTRs. Moreover, we reinforce previously published data showing an association between 25(OH)D, TCMR and graft survival in KT.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Holick MF. Vitamin D deficiency. N Engl J Med. 2007;357:266-281.
Herrmann M, Farrell CJL, Pusceddu I, Fabregat-Cabello N, Cavalier E. Assessment of vitamin D status - a changing landscape. Clin Chem Lab Med. 2017;55:3-26.
Dusso AS, Brown AJ, Slatopolsky E. Vitamin D. Am J Physiol Renal Physiol. 2005;289:F8-F28.
Christakos S, Dhawan P, Verstuyf A, Verlinden L, Carmeliet G. Vitamin D: metabolism, molecular mechanism of action, and pleiotropic effects. Physiol Rev. 2016;96:365-408.
Ravani P, Malberti F, Tripepi G, et al. Vitamin D levels and patient outcome in chronic kidney disease. Kidney Int. 2009;75:88-95.
Melamed ML, Astor B, Michos ED, Hostetter TH, Powe NR, Muntner P. 25-hydroxyvitamin D levels, race, and the progression of kidney disease. J Am Soc Nephrol. 2009;20:2631-2639.
Bienaimé F, Girard D, Anglicheau D, et al. Vitamin D status and outcomes after renal transplantation. J Am Soc Nephrol. 2013;24:831-841.
Keyzer CA, Riphagen IJ, Joosten MM, et al. Associations of 25(OH) and 1,25(OH)2 vitamin D with long-term outcomes in stable renal transplant recipients. J Clin Endocrinol Metab. 2015;100:81-89.
Thorsen IS, Bleskestad IH, Åsberg A, et al. Vitamin D as a risk factor for patient survival after kidney transplantation: a prospective observational cohort study. Clin Transpl. 2019;33:e13517.
Obi Y, Hamano T, Ichimaru N, et al. Vitamin D deficiency predicts decline in kidney allograft function: a prospective cohort study. J Clin Endocrinol Metab. 2014;99:527-535.
Ban TH, Kim JH, Jang HB, et al. Clinical effects of pre-transplant serum 25-hydroxyvitamin D level on post-transplant immunologic and non-immunologic outcomes in kidney transplant recipients. Transpl Immunol. 2017;40:51-56.
Lee JR, Dadhania D, August P, Lee JB, Suthanthiran M, Muthukumar T. Circulating levels of 25-hydroxyvitamin D and acute cellular rejection in kidney allograft recipients. Transplantation. 2014;98:292-299.
Mosca M, Lion-Lambert M, Bienaimé F, et al. Association between 25(OH) vitamin D and graft survival in renal transplanted children. Pediatr Transplant. 2020;24:e13809.
Sellarés J, de Freitas DG, Mengel M, et al. Understanding the causes of kidney transplant failure: the dominant role of antibody-mediated rejection and nonadherence. Am J Transplant. 2012;12:388-399.
Nankivell BJ, Alexander SI. Rejection of the kidney allograft. N Engl J Med. 2010;363:1451-1462.
Ntokou I-SA, Iniotaki AG, Kontou EN, et al. Long-term follow up for anti-HLA donor specific antibodies postrenal transplantation: high immunogenicity of HLA class II graft molecules. Transplant Int. 2011;24:1084-1093.
Cooper JE, Gralla J, Cagle L, Goldberg R, Chan L, Wiseman AC. Inferior kidney allograft outcomes in patients with de novo donor-specific antibodies are due to acute rejection episodes. Transplantation. 2011;91:1103-1109.
Wiebe C, Gibson IW, Blydt-Hansen TD, et al. Evolution and clinical pathologic correlations of de novo donor-specific HLA antibody post kidney transplant. Am J Transplant. 2012;12:1157-1167.
Wiebe C, Gibson IW, Blydt-Hansen TD, et al. Rates and determinants of progression to graft failure in kidney allograft recipients with de novo donor-specific antibody. Am J Transplant. 2015;15:2921-2930.
Böhmig GA, Eskandary F, Doberer K, Halloran PF. The therapeutic challenge of late antibody-mediated kidney allograft rejection. Transplant Int. 2019;32:775-788.
Visentin J, Bachelet T, Borg C, et al. Reassessment of T lymphocytes crossmatches results prediction with Luminex class I single antigen flow beads assay. Transplantation. 2017;101:624-630.
Hutchinson K, Healy M, Crowley V, Louw M, Rochev Y. Verification of Abbott 25-OH-vitamin D assay on the architect system. Pract Lab Med. 2017;7:27-35.
Agborsangaya C, Toriola AT, Grankvist K, et al. The effects of storage time and sampling season on the stability of serum 25-hydroxy vitamin D and androstenedione. Nutr Cancer. 2009;62:51-57.
Office of Dietary Supplements - Vitamin D. Available from https://ods.od.nih.gov/factsheets/VitaminD-HealthProfessional/
Monthly means of solar irradiance, temperature and relative humidity. www.soda-pro.com. Available from http://www.soda-pro.com/web-services/meteo-data/monthly-means-solar-irradiance-temperature-relative-humidity
Davis S, Gralla J, Klem P, et al. Lower tacrolimus exposure and time in therapeutic range increase the risk of de novo donor-specific antibodies in the first year of kidney transplantation. Am J Transplant. 2018;18:907-915.
Davis S, Gralla J, Klem P, Stites E, Wiseman A, Cooper JE. Tacrolimus intra-patient variability, time in therapeutic range, and risk of de novo donor-specific antibodies. Transplantation. 2019;104:881-887.
Wiebe C, Rush DN, Nevins TE, et al. Class II Eplet mismatch modulates tacrolimus trough levels required to prevent donor-specific antibody development. J Am Soc Nephrol. 2017;28:3353-3362.
Kidney Disease: Improving Global Outcomes (KDIGO) Transplant Work Group. KDIGO clinical practice guideline for the care of kidney transplant recipients. Am J Transplant. 2009;9:S1-S155.
Haas M, Sis B, Racusen LC, et al. Banff 2013 meeting report: inclusion of c4d-negative antibody-mediated rejection and antibody-associated arterial lesions. Am J Transplant. 2014;14:272-283.
Visentin J, Vigata M, Daburon S, et al. Deciphering complement interference in anti-human leukocyte antigen antibody detection with flow beads assays. Transplantation. 2014;98:625-631.
Koimtzis G, Stefanopoulos L, Brooker V, et al. The role of vitamin D in kidney transplantation outcomes: a systematic review. Life. 2022;12:1664.
Bertrand D, Gatault P, Jauréguy M, et al. Protocol biopsies in patients with subclinical De novo DSA after kidney transplantation: a multicentric study. Transplantation. 2019;104:1726-1737.
Hullett DA, Cantorna MT, Redaelli C, et al. Prolongation of allograft survival by 1,25-dihydroxyvitamin D3. Transplantation. 1998;66:824-828.
Redaelli CA, Wagner M, Günter-Duwe D, et al. 1alpha,25-dihydroxyvitamin D3 shows strong and additive immunomodulatory effects with cyclosporine a in rat renal allotransplants. Kidney Int. 2002;61:288-296.
Zhang A-B, Zheng S-S, Jia C-K, Wang Y. Effect of 1,25-dihydroxyvitamin D3 on preventing allograft from acute rejection following rat orthotopic liver transplantation. World J Gastroenterol. 2003;9:1067-1071.
Penna G, Roncari A, Amuchastegui S, et al. Expression of the inhibitory receptor ILT3 on dendritic cells is dispensable for induction of CD4+Foxp3+ regulatory T cells by 1,25-dihydroxyvitamin D3. Blood. 2005;106:3490-3497.
Penna G, Adorini L. 1 alpha,25-dihydroxyvitamin D3 inhibits differentiation, maturation, activation, and survival of dendritic cells leading to impaired alloreactive T cell activation. J Immunol Baltim Md. 2000;1950(164):2405-2411.
Griffin MD, Lutz W, Phan VA, Bachman LA, McKean DJ, Kumar R. Dendritic cell modulation by 1alpha,25 dihydroxyvitamin D3 and its analogs: a vitamin D receptor-dependent pathway that promotes a persistent state of immaturity in vitro and in vivo. Proc Natl Acad Sci U S A. 2001;98:6800-6805.
Bhalla AK, Amento EP, Krane SM. Differential effects of 1,25-dihydroxyvitamin D3 on human lymphocytes and monocyte/macrophages: inhibition of interleukin-2 and augmentation of interleukin-1 production. Cell Immunol. 1986;98:311-322.
Rigby WF, Stacy T, Fanger MW. Inhibition of T lymphocyte mitogenesis by 1,25-dihydroxyvitamin D3 (calcitriol). J Clin Invest. 1984;74:1451-1455.
Alroy I, Towers TL, Freedman LP. Transcriptional repression of the interleukin-2 gene by vitamin D3: direct inhibition of NFATp/AP-1 complex formation by a nuclear hormone receptor. Mol Cell Biol. 1995;15:5789-5799.
Rigby WF, Yirinec B, Oldershaw RL, Fanger MW. Comparison of the effects of 1,25-dihydroxyvitamin D3 on T lymphocyte subpopulations. Eur J Immunol. 1987;17:563-566.
Joshi S, Pantalena L-C, Liu XK, et al. 1,25-dihydroxyvitamin D(3) ameliorates Th17 autoimmunity via transcriptional modulation of interleukin-17A. Mol Cell Biol. 2011;31:3653-3669.
Meehan MA, Kerman RH, Lemire JM. 1,25-Dihydroxyvitamin D3 enhances the generation of nonspecific suppressor cells while inhibiting the induction of cytotoxic cells in a human MLR. Cell Immunol. 1992;140:400-409.
Farias AS, Spagnol GS, Bordeaux-Rego P, et al. Vitamin D3 induces IDO+ tolerogenic DCs and enhances Treg, reducing the severity of EAE. CNS Neurosci Ther. 2013;19:269-277.
Daniel C, Sartory NA, Zahn N, Radeke HH, Stein JM. Immune modulatory treatment of trinitrobenzene sulfonic acid colitis with calcitriol is associated with a change of a T helper (Th) 1/Th17 to a Th2 and regulatory T cell profile. J Pharmacol Exp Ther. 2008;324:23-33.
Chen S, Sims GP, Chen XX, Gu YY, Chen S, Lipsky PE. Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. J Immunol Baltim Md. 2007;1950(179):1634-1647.
Rampersad C, Balshaw R, Gibson IW, et al. The negative impact of T-cell mediated rejection on renal allograft survival in the modern era. Am J Transplant. 2021;22:761-771.
Doi Y, Tsujita M, Hamano T, et al. The effect of cholecalciferol supplementation on allograft function in incident kidney transplant recipients: a randomized controlled study. Am J Transplant. 2021;21:3043-3054.
Chonchol M, Greene T, Zhang Y, Hoofnagle AN, Cheung AK. Low vitamin D and high fibroblast growth factor 23 serum levels associate with infectious and cardiac deaths in the HEMO study. J Am Soc Nephrol. 2016;27:227-237.