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Published in: Immunity & Ageing 1/2018

Open Access 01-12-2018 | Research

ESRD-associated immune phenotype depends on dialysis modality and iron status: clinical implications

Authors: Didier Ducloux, Mathieu Legendre, Jamal Bamoulid, Jean-Michel Rebibou, Philippe Saas, Cécile Courivaud, Thomas Crepin

Published in: Immunity & Ageing | Issue 1/2018

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Abstract

Background

End-stage renal disease (ESRD) causes premature ageing of the immune system. However, it is not known whether hemodialysis (HD) and peritoneal dialysis (PD) similarly affect the T cell system.

Methods

The aim of our study was to analyse whether dialysis modality may mitigate ESRD-induced immune senescence. We explored a large population of patients (675 ESRD patients) and both confirmed and refined the results in a second cohort (84 patients).

Results

HD patients exhibited higher inflammatory monocytes counts (44/mm3 (1–520) vs 36/mm3 (1–161); p = 0.005). Patients on HD also had higher frequency of CD8 T cells (24% (7–61) vs 22% (8–42); p = 0.003) and reduced CD4/CD8 ratio. Such results were confirmed in the second cohort. Moreover, both CD4 + CD57 + CD28- (3.25% (0–38.2) vs 1.05% (0–28.5); p = 0.068) and CD8 + CD57 + CD28- (38.5% (3.6–76.8) vs 26.1 (2.1–46.9); p = 0.039) T cells frequencies were increased in HD patients. Telomere length did not differ according to dialysis modality, but was inversely related to ferritin levels (r = − 0.33; p = 0.003). There was a trend towards higher telomerase activity in PD patients (11 ± 13 vs 6 ± 11; p = 0.053). Thymic function was not different in PD and HD patients. Patients on PD before transplantation had a higher risk of acute rejection after kidney transplantation (HR, 1.61; 95%CI, 1.02 to 2.56; p = 0.041).

Conclusions

More pronounced inflammation with hemodialysis may induce premature aging of the immune system. This observation correlates with a lower risk of acute kidney rejection in patients previously on HD. Clinical consequences in patients maintained on dialysis should be determined.

Trial registration

Trial registration: NCT02843867, registered July 8, 2016.
Literature
1.
go back to reference Sakhuja A, Nanchal RS, Gupta S, Amer H, Kumar G, Albright RC, Kashani KB. Trends and outcomes of severe sepsis inpatients on maintenance dialysis. Am J Nephrol. 2016;43:97–103.CrossRefPubMed Sakhuja A, Nanchal RS, Gupta S, Amer H, Kumar G, Albright RC, Kashani KB. Trends and outcomes of severe sepsis inpatients on maintenance dialysis. Am J Nephrol. 2016;43:97–103.CrossRefPubMed
2.
go back to reference Stewart JH, Vajdic CM, van Leeuwen MT, Amin J, Webster AC, Chapman JR, McDonald SP, Grulich AE, McCredie MR. The pattern of excess cancer in dialysis and transplantation. Nephrol Dial Transplant. 2009;24:3225–31.CrossRefPubMed Stewart JH, Vajdic CM, van Leeuwen MT, Amin J, Webster AC, Chapman JR, McDonald SP, Grulich AE, McCredie MR. The pattern of excess cancer in dialysis and transplantation. Nephrol Dial Transplant. 2009;24:3225–31.CrossRefPubMed
3.
go back to reference Soni R, Horowitz B, Unruh M. Immunization in end-stage renal disease: opportunity to improve outcomes. Semin Dial. 2013;26:416–26.CrossRefPubMed Soni R, Horowitz B, Unruh M. Immunization in end-stage renal disease: opportunity to improve outcomes. Semin Dial. 2013;26:416–26.CrossRefPubMed
4.
go back to reference Betjes MGH, Huisman M, Weimar W, Litjens NHR. Expansion of cytolytic CD4+CD28- T cells in end-stage renal disease. Kidney Int. 2008;74:760–7.CrossRefPubMed Betjes MGH, Huisman M, Weimar W, Litjens NHR. Expansion of cytolytic CD4+CD28- T cells in end-stage renal disease. Kidney Int. 2008;74:760–7.CrossRefPubMed
5.
go back to reference Crepin T, Legendre M, Courivaud C, Rebibou JM, Ferrand C, Laheurte C, Vauchy C, Gaiffe E, Saas P, Ducloux D, Bamoulid J. Uremia-induced immune senescence and clinical outcomes in chronic disease patients. Nephrol Dial Transplant 2018 (in press). Crepin T, Legendre M, Courivaud C, Rebibou JM, Ferrand C, Laheurte C, Vauchy C, Gaiffe E, Saas P, Ducloux D, Bamoulid J. Uremia-induced immune senescence and clinical outcomes in chronic disease patients. Nephrol Dial Transplant 2018 (in press).
6.
go back to reference Betjes MG, Meijers RW, Litjens NH. Loss of renal function causes premature aging of the immune system. Blood Purif. 2013;36:173–8.CrossRefPubMed Betjes MG, Meijers RW, Litjens NH. Loss of renal function causes premature aging of the immune system. Blood Purif. 2013;36:173–8.CrossRefPubMed
7.
go back to reference Betjes MG. Immune cell dysfunction and inflammation in end-stage renal disease. Nat Rev Nephrol. 2013;9:255–65.CrossRefPubMed Betjes MG. Immune cell dysfunction and inflammation in end-stage renal disease. Nat Rev Nephrol. 2013;9:255–65.CrossRefPubMed
8.
go back to reference Meijers RWH, Litjens NHR, de Wit EA, Langerak AW, van der Spek A, Baan CC, Weimar W, Betjes MGH. Uremia causes premature ageing of the T-cell compartment in end-stage renal disease patients. Immun Ageing. 2012;9:19.CrossRefPubMedPubMedCentral Meijers RWH, Litjens NHR, de Wit EA, Langerak AW, van der Spek A, Baan CC, Weimar W, Betjes MGH. Uremia causes premature ageing of the T-cell compartment in end-stage renal disease patients. Immun Ageing. 2012;9:19.CrossRefPubMedPubMedCentral
9.
go back to reference Bamoulid J, Courivaud C, Crepin T, Carron C, Gaiffe E, Roubiou C, Laheurte C, Moulin B, Frimat L, Rieu P, Mousson C, Durrbach A, Heng A-E, Rebibou JM, Saas P, Ducloux D. Pre-transplant thymic function predicts acute rejection in ATG-treated renal transplant recipients. Kidney Int. 2016;89:1136–43.CrossRefPubMed Bamoulid J, Courivaud C, Crepin T, Carron C, Gaiffe E, Roubiou C, Laheurte C, Moulin B, Frimat L, Rieu P, Mousson C, Durrbach A, Heng A-E, Rebibou JM, Saas P, Ducloux D. Pre-transplant thymic function predicts acute rejection in ATG-treated renal transplant recipients. Kidney Int. 2016;89:1136–43.CrossRefPubMed
10.
go back to reference Ducloux D, Courivaud C, Bamoulid J, Vivet B, Chabroux A, Deschamps M, Rebibou JM, Ferrand C, Chalopin JM, Tiberghien P, Saas P. Prolonged CD4 T cell lymphopenia increases morbidity and mortality after renal transplantation. J Am Soc Nephrol. 2010;21:868–75.CrossRefPubMedPubMedCentral Ducloux D, Courivaud C, Bamoulid J, Vivet B, Chabroux A, Deschamps M, Rebibou JM, Ferrand C, Chalopin JM, Tiberghien P, Saas P. Prolonged CD4 T cell lymphopenia increases morbidity and mortality after renal transplantation. J Am Soc Nephrol. 2010;21:868–75.CrossRefPubMedPubMedCentral
11.
go back to reference Crepin T, Carron C, Roubiou C, Gaugler B, Gaiffe E, Simula-Faivre D, Ferrand C, Tiberghien P, Chalopin J-M, Moulin B, Frimat L, Rieu P, Saas P, Ducloux D, Bamoulid J. ATG-induced accelerated immune senescence: clinical implications in renal transplant recipients. Am J Transplant. 2015;15:1028–38.CrossRefPubMed Crepin T, Carron C, Roubiou C, Gaugler B, Gaiffe E, Simula-Faivre D, Ferrand C, Tiberghien P, Chalopin J-M, Moulin B, Frimat L, Rieu P, Saas P, Ducloux D, Bamoulid J. ATG-induced accelerated immune senescence: clinical implications in renal transplant recipients. Am J Transplant. 2015;15:1028–38.CrossRefPubMed
12.
go back to reference Rostoker G, Griuncelli M, Loridon C, Magna T, Machado G, Drahi G, Dahan H, Janklewicz P, Cohen Y. Reassessment of iron biomarkers for prediction of dialysis iron overload: an MRI study. PLoS One. 2015:e0132006. Rostoker G, Griuncelli M, Loridon C, Magna T, Machado G, Drahi G, Dahan H, Janklewicz P, Cohen Y. Reassessment of iron biomarkers for prediction of dialysis iron overload: an MRI study. PLoS One. 2015:e0132006.
13.
go back to reference Lambie M, Chess J, Donovan L, Kim YL, Do JY, Lee HB, Noh H, Williams PF, Williams AJ, Davison S, Dorval M, Summers A, Williams JD, Bankart J, Davies SJ, Topley N. Independent effects of systemic and peritoneal inflammation on peritoneal dialysis survival. J Am Soc Nephrol. 2013;24:2071–80.CrossRefPubMedPubMedCentral Lambie M, Chess J, Donovan L, Kim YL, Do JY, Lee HB, Noh H, Williams PF, Williams AJ, Davison S, Dorval M, Summers A, Williams JD, Bankart J, Davies SJ, Topley N. Independent effects of systemic and peritoneal inflammation on peritoneal dialysis survival. J Am Soc Nephrol. 2013;24:2071–80.CrossRefPubMedPubMedCentral
14.
go back to reference Pecoits-Filho R, Carvalho MJ, Stenvinkel P, Lindholm B, Heimbürger O. Systemic and intraperitoneal interleukin-6 system during the first year of peritoneal dialysis. Perit Dial Int. 2006;26:53–63.PubMed Pecoits-Filho R, Carvalho MJ, Stenvinkel P, Lindholm B, Heimbürger O. Systemic and intraperitoneal interleukin-6 system during the first year of peritoneal dialysis. Perit Dial Int. 2006;26:53–63.PubMed
15.
go back to reference Cho JH, Hur IK, Kim CD, Park SH, Ryu HM, Yook JM, Choi JY, Choi HJ, Choi HJ, Park JW, Do JY, Kim YL. Impact of systemic and local peritoneal inflammation on peritoneal solute transport rate in new peritoneal dialysis patients: a 1-year prospective study. Nephrol Dial Transplant. 2010;25:1964–73.CrossRefPubMed Cho JH, Hur IK, Kim CD, Park SH, Ryu HM, Yook JM, Choi JY, Choi HJ, Choi HJ, Park JW, Do JY, Kim YL. Impact of systemic and local peritoneal inflammation on peritoneal solute transport rate in new peritoneal dialysis patients: a 1-year prospective study. Nephrol Dial Transplant. 2010;25:1964–73.CrossRefPubMed
16.
go back to reference Oldani S, Finazzi S, Botazzi B, Garlanda C, Baldassarre E, Valaperta S, Cuccovillo I, Albino M, Child M, Montanelli A, Graziani G, Badalamenti S. Plasma pentraxin-3 as a marker of biocompatibility in hemodialysis patients. J Nephrol. 2012;25:120–6.CrossRefPubMed Oldani S, Finazzi S, Botazzi B, Garlanda C, Baldassarre E, Valaperta S, Cuccovillo I, Albino M, Child M, Montanelli A, Graziani G, Badalamenti S. Plasma pentraxin-3 as a marker of biocompatibility in hemodialysis patients. J Nephrol. 2012;25:120–6.CrossRefPubMed
17.
go back to reference Yamamoto T, Nascimento MM, Hayashi SY, Qureshi AR, Waniewski J, Brodin LA, Anderstam B, Lind B, Riella MC, Seeberger A, Lindholm B. Changes in circulating biomarkers during a single hemodialysis session. Hemodialysis Int. 2013;17:59–66.CrossRef Yamamoto T, Nascimento MM, Hayashi SY, Qureshi AR, Waniewski J, Brodin LA, Anderstam B, Lind B, Riella MC, Seeberger A, Lindholm B. Changes in circulating biomarkers during a single hemodialysis session. Hemodialysis Int. 2013;17:59–66.CrossRef
18.
go back to reference Bitla AR, Reddy PE, Manohar SM, Vishnubhotla SV, Pemmaraju Venkata Lakshmi Narasimha SR. Effect of a single hemodialysis session on inflammatory markers. Hemodialysis Int. 2010;14:411–7.CrossRef Bitla AR, Reddy PE, Manohar SM, Vishnubhotla SV, Pemmaraju Venkata Lakshmi Narasimha SR. Effect of a single hemodialysis session on inflammatory markers. Hemodialysis Int. 2010;14:411–7.CrossRef
19.
go back to reference Gollapudi P, Yoon JW, Gollapudi S, Pahl MV, Vaziri ND. Leukocyte toll-like receptor expression in end-stage kidney disease. Am J Nephrol. 2010;31:247–54.CrossRefPubMed Gollapudi P, Yoon JW, Gollapudi S, Pahl MV, Vaziri ND. Leukocyte toll-like receptor expression in end-stage kidney disease. Am J Nephrol. 2010;31:247–54.CrossRefPubMed
20.
go back to reference Ando M, Shibuya A, Tsuchiya K, Akiba T, Nitta K. Reduced expression of toll-like receptor 4 contributes to impaired cytokine response of monocytes in uremic patients. Kidney Int. 2006;70:358–62.CrossRefPubMed Ando M, Shibuya A, Tsuchiya K, Akiba T, Nitta K. Reduced expression of toll-like receptor 4 contributes to impaired cytokine response of monocytes in uremic patients. Kidney Int. 2006;70:358–62.CrossRefPubMed
22.
go back to reference Chiu CP, Dragowska W, Kim NW, Vaziri H, Yui J, Thomas TE, et al. Differential expression of telomerase activity in hematopoietic progen-itors from adult human bone marrow. Stem Cells. 1996;14:239–48.CrossRefPubMed Chiu CP, Dragowska W, Kim NW, Vaziri H, Yui J, Thomas TE, et al. Differential expression of telomerase activity in hematopoietic progen-itors from adult human bone marrow. Stem Cells. 1996;14:239–48.CrossRefPubMed
23.
go back to reference Engelhardt M, Kumar R, Albanell J, Pettengell R, Han W, Moore MA. Telomerase regulation, cell cycle, and telomere stability in primitive hemato-poietic cells. Blood. 1997;90:182–93.PubMed Engelhardt M, Kumar R, Albanell J, Pettengell R, Han W, Moore MA. Telomerase regulation, cell cycle, and telomere stability in primitive hemato-poietic cells. Blood. 1997;90:182–93.PubMed
24.
go back to reference Plunkett FJ, Franzese O, Finney HM, Fletcher JM, Belaramani LL, Salmon M, et al. The loss of telomerase activity in highly differentiated CD8+CD28-CD27- T cells is associated with decreased Akt (Ser473) phos-phorylation. J Immunol. 2007;178:7710–9.CrossRefPubMed Plunkett FJ, Franzese O, Finney HM, Fletcher JM, Belaramani LL, Salmon M, et al. The loss of telomerase activity in highly differentiated CD8+CD28-CD27- T cells is associated with decreased Akt (Ser473) phos-phorylation. J Immunol. 2007;178:7710–9.CrossRefPubMed
25.
go back to reference Akbar AN, Vukmanovic-Stejic M. Telomerase in T lymphocytes: use it and lose it? J Immunol. 2007;178:6689–94.CrossRefPubMed Akbar AN, Vukmanovic-Stejic M. Telomerase in T lymphocytes: use it and lose it? J Immunol. 2007;178:6689–94.CrossRefPubMed
26.
go back to reference Xu D, Erickson S, Szeps M, Gruber A, Sangfelt O, Einhorn S, et al. Interferon alpha down-regulates telomerase reverse transcriptase and telomerase activity in human malignant and nonmalignant hematopoietic cells. Blood. 2000;96:4313–8.PubMed Xu D, Erickson S, Szeps M, Gruber A, Sangfelt O, Einhorn S, et al. Interferon alpha down-regulates telomerase reverse transcriptase and telomerase activity in human malignant and nonmalignant hematopoietic cells. Blood. 2000;96:4313–8.PubMed
27.
go back to reference Reed, J. R., M. Vukmanovic-Stejic, J. M. Fletcher, M. V. Soares, J. E. Cook, C. H. Orteu, S. E. Jackson, K. E. Birch, G. R. Foster, M. Salmon, et al. 2004. Telomere erosion in memory T cells induced by telomerase inhibition at the site of antigenic challenge in vivo. J Exp Med 2004:199; 1433–1443. Reed, J. R., M. Vukmanovic-Stejic, J. M. Fletcher, M. V. Soares, J. E. Cook, C. H. Orteu, S. E. Jackson, K. E. Birch, G. R. Foster, M. Salmon, et al. 2004. Telomere erosion in memory T cells induced by telomerase inhibition at the site of antigenic challenge in vivo. J Exp Med 2004:199; 1433–1443.
28.
go back to reference Kaplan RC, Sinclair E, Landay AL, et al. T cell activation predicts carotid artery stiffness in HIV-infected women. Atherosclerosis. 2011;217:207–13.CrossRefPubMedPubMedCentral Kaplan RC, Sinclair E, Landay AL, et al. T cell activation predicts carotid artery stiffness in HIV-infected women. Atherosclerosis. 2011;217:207–13.CrossRefPubMedPubMedCentral
29.
go back to reference Betjes MG, Litjens NH, Zietse R. Seropositivity for cytomegalovirus in patients with end-stage renal disease is strongly associated with atherosclerotic disease. Nephrol Dial Transplant. 2007;22:3298–303.CrossRefPubMed Betjes MG, Litjens NH, Zietse R. Seropositivity for cytomegalovirus in patients with end-stage renal disease is strongly associated with atherosclerotic disease. Nephrol Dial Transplant. 2007;22:3298–303.CrossRefPubMed
30.
go back to reference Courivaud C, Bamoulid J, Chalopin JM, Gaiffe E, Tiberghien P, Saas P, Ducloux D. Cytomegalovirus exposure and cardiovascular disease in kidney transplant recipients. J Infect Dis. 2013;207:1569–75.CrossRefPubMed Courivaud C, Bamoulid J, Chalopin JM, Gaiffe E, Tiberghien P, Saas P, Ducloux D. Cytomegalovirus exposure and cardiovascular disease in kidney transplant recipients. J Infect Dis. 2013;207:1569–75.CrossRefPubMed
31.
go back to reference Borthwick NJ, Lowdell M, Salmon M, Akbar AN. Loss of CD28 expression on CD8 T cells is induced by IL-2 receptor _ chain signalling cytokines and type I IFN, and increases susceptibility to activation-induced apoptosis. Int Immunol. 2000;12:1005–13.CrossRefPubMed Borthwick NJ, Lowdell M, Salmon M, Akbar AN. Loss of CD28 expression on CD8 T cells is induced by IL-2 receptor _ chain signalling cytokines and type I IFN, and increases susceptibility to activation-induced apoptosis. Int Immunol. 2000;12:1005–13.CrossRefPubMed
32.
go back to reference Betjes MGH, Meijers RWJ, de Wit EA, Weimar W, Litjens NHR. Terminally differentiated CD8+ Temra cells are associated with the risk of acute kidney allograft rejection. Transplantation. 2012;94:63–9.CrossRefPubMed Betjes MGH, Meijers RWJ, de Wit EA, Weimar W, Litjens NHR. Terminally differentiated CD8+ Temra cells are associated with the risk of acute kidney allograft rejection. Transplantation. 2012;94:63–9.CrossRefPubMed
33.
go back to reference Franceschi C, Bonafe M, Valensin S. Human immunosenescence: the prevailing of innate immunity, the failing of clonotypic immunity, and the filling of immunological space. Vaccine. 2000;18:1717–20.CrossRefPubMed Franceschi C, Bonafe M, Valensin S. Human immunosenescence: the prevailing of innate immunity, the failing of clonotypic immunity, and the filling of immunological space. Vaccine. 2000;18:1717–20.CrossRefPubMed
34.
go back to reference Tulunay A, Yavuz S, Direskenell H, Eksioglu-Demiralp E. CD8+CD28-, suppressive T cells in systemic lupus erythematosus. Lupus. 2008;17:630–7.CrossRefPubMed Tulunay A, Yavuz S, Direskenell H, Eksioglu-Demiralp E. CD8+CD28-, suppressive T cells in systemic lupus erythematosus. Lupus. 2008;17:630–7.CrossRefPubMed
35.
go back to reference Cortesini R, LeMaoult J, Ciubotariu R, et al. CD8+CD28j T suppressor cells and the induction of antigen-specific, antigen- presenting cellYmediated suppression of Th reactivity. Immunol Rev. 2001;182:201.CrossRefPubMed Cortesini R, LeMaoult J, Ciubotariu R, et al. CD8+CD28j T suppressor cells and the induction of antigen-specific, antigen- presenting cellYmediated suppression of Th reactivity. Immunol Rev. 2001;182:201.CrossRefPubMed
36.
go back to reference Gerlach UA, Vogt K, Schlickeiser S, Meisel C, Streitz M, Kunkel D, Appelt C, Ahrlich S, Lachmann N, Neuhaus P, Pascher A, Sawitzki B. Elevation of CD4+ differentiated memory T cells is associated with acute cellular and antibody-mediated rejection after liver transplantation. Transplantation 2013; 27–1512–1520. Gerlach UA, Vogt K, Schlickeiser S, Meisel C, Streitz M, Kunkel D, Appelt C, Ahrlich S, Lachmann N, Neuhaus P, Pascher A, Sawitzki B. Elevation of CD4+ differentiated memory T cells is associated with acute cellular and antibody-mediated rejection after liver transplantation. Transplantation 2013; 27–1512–1520.
37.
go back to reference Tang M, Li T, Liu H. A comparison of transplant outcomes in peritoneal and hemodialysis patients: a meta-analysis. Blood Purif. 2016;42:170–6.CrossRefPubMed Tang M, Li T, Liu H. A comparison of transplant outcomes in peritoneal and hemodialysis patients: a meta-analysis. Blood Purif. 2016;42:170–6.CrossRefPubMed
38.
go back to reference Crepin T, Gaiffe E, Courivaud C, Roubiou C, Laheurte C, Moulin B, Frimat L, Rieu P, Mousson C, Durrbach A, Heng A-E, Saas P, Bamoulid J, Ducloux D. Pre-transplant end-stage renal disease-related immune risk profile in kidney transplant recipients predicts post-transplant infections. Transplant Inf Dis. 2016;18:415–22.CrossRef Crepin T, Gaiffe E, Courivaud C, Roubiou C, Laheurte C, Moulin B, Frimat L, Rieu P, Mousson C, Durrbach A, Heng A-E, Saas P, Bamoulid J, Ducloux D. Pre-transplant end-stage renal disease-related immune risk profile in kidney transplant recipients predicts post-transplant infections. Transplant Inf Dis. 2016;18:415–22.CrossRef
39.
go back to reference Wetmore JB, Peng Y, Monda KL, Kats AM, Kim DH, Bradbury BD, Collins AJ, Gilbertson DT. Trends in anemia management practices in patients receiving hemodialysis and peritoneal dialysis: a retrospective cohort analysis. Am J Nephrol. 2015;41:354–61.CrossRefPubMed Wetmore JB, Peng Y, Monda KL, Kats AM, Kim DH, Bradbury BD, Collins AJ, Gilbertson DT. Trends in anemia management practices in patients receiving hemodialysis and peritoneal dialysis: a retrospective cohort analysis. Am J Nephrol. 2015;41:354–61.CrossRefPubMed
40.
go back to reference Liakopoulos V, Roumeliotis S, Gomy X, Dounousi E, Mertens PR. Oxidative stress in hemodialysis patients : a review of literature. Oxidative Med Cell Longev 2017; 2017: 3081856. Liakopoulos V, Roumeliotis S, Gomy X, Dounousi E, Mertens PR. Oxidative stress in hemodialysis patients : a review of literature. Oxidative Med Cell Longev 2017; 2017: 3081856.
41.
go back to reference Shin C, Baik I. Transferrin saturation concentrations associated with telomeric ageing: a population-based study. Br J Nutr. 2017;117:1693–701.CrossRefPubMed Shin C, Baik I. Transferrin saturation concentrations associated with telomeric ageing: a population-based study. Br J Nutr. 2017;117:1693–701.CrossRefPubMed
42.
go back to reference Murillo-Ortiz B, Ramirez Emiliano J, Hernandez Vazquez WI, Martinez-Garza S, Solorio-Meza S, Albarran-Tamayo F, Ramos-Rodriguez E, Benitez-Bribiesca L. Impact of oxidative stress in premature aging and iron overload in hemodialysis patients. Oxidative Med Cell Longev. 2016;2016:1578235.CrossRef Murillo-Ortiz B, Ramirez Emiliano J, Hernandez Vazquez WI, Martinez-Garza S, Solorio-Meza S, Albarran-Tamayo F, Ramos-Rodriguez E, Benitez-Bribiesca L. Impact of oxidative stress in premature aging and iron overload in hemodialysis patients. Oxidative Med Cell Longev. 2016;2016:1578235.CrossRef
43.
go back to reference Kepinska M, Szyller J, Milnerowicz H. The influence of oxidative stress induced by iron on telomere length. Environ Toxicol Pharmacol. 2015;40:931–5.CrossRefPubMed Kepinska M, Szyller J, Milnerowicz H. The influence of oxidative stress induced by iron on telomere length. Environ Toxicol Pharmacol. 2015;40:931–5.CrossRefPubMed
44.
go back to reference Xie Y, Hou W, Song X, Yu Y, Huang J, Sun X, Kang R, Tang D. Ferroptosis: process and function. Cell death Diff. 2016;23:369–79.CrossRef Xie Y, Hou W, Song X, Yu Y, Huang J, Sun X, Kang R, Tang D. Ferroptosis: process and function. Cell death Diff. 2016;23:369–79.CrossRef
Metadata
Title
ESRD-associated immune phenotype depends on dialysis modality and iron status: clinical implications
Authors
Didier Ducloux
Mathieu Legendre
Jamal Bamoulid
Jean-Michel Rebibou
Philippe Saas
Cécile Courivaud
Thomas Crepin
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Immunity & Ageing / Issue 1/2018
Electronic ISSN: 1742-4933
DOI
https://doi.org/10.1186/s12979-018-0121-z

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