Skip to main content
Top
Published in: Journal of Interventional Cardiac Electrophysiology 3/2019

01-04-2019

Impact of cardiac resynchronization therapy on circulating IL-17 producing cells in patients with advanced heart failure

Authors: Sílvia Martins, Tiago Carvalheiro, Paula Laranjeira, António Martinho, Luís Elvas, Lino Gonçalves, Cândida Tomaz, Natália António, Artur Paiva

Published in: Journal of Interventional Cardiac Electrophysiology | Issue 3/2019

Login to get access

Abstract

Purpose

IL-17-producing T cells have been implicated in the inflammatory milieu of chronic heart failure (CHF), which implies a dismal prognosis in affected patients. The aim of this study was to evaluate the impact of cardiac resynchronization therapy (CRT) on the frequency and functional activity of Th17 and Tc17 cells, as well as, on IL-17 mRNA expression in patients with CHF.

Methods

Twenty-eight patients with CHF, analyzed before CRT (T0) and 6 months later (T6), and 15 healthy controls (HC) were enrolled in this study. Circulating Th17 and Tc17 cells were evaluated by flow cytometry. The quantification of IL-17A mRNA expression was performed by real-time PCR.

Results

Circulating Tc17 cells tended to be higher in CHF patients submitted to CRT than in HC (0.92% (0.24–3.32) versus 0.60% (0.09–3.68), although not reaching statistical significance. The frequency of Tc17 cells in CHF patients significantly decreases after CRT reaching levels similar to those of HC (0.92% (0.24–3.32) at T0 versus 0.56% (0.21–4.20) at T6, P < 0.05), mainly due to responders to CRT. Additionally, the expression of IL-17 mRNA was detected in a few number of responder patients at T0 (27%) and only detected in one responder at T6 (7%). Conversely, in non-responders, the proportion of patients exhibiting IL-17 mRNA expression increases from baseline (17%) to T6 (42%). No significant differences were observed in Th17 cells between HC, CHF patients in T0 and patients in T6.

Conclusion

The inflammatory response mediated by circulating IL-17 producing cells seems to be suppressed by CRT, particularly in responders.
Literature
1.
go back to reference Batista ML Jr, Lopes RD, Seelaender MC, Lopes AC. Anti-inflammatory effect of physical training in heart failure: role of TNF-alpha and IL-10. Arq Bras Cardiol. 2009;93:643–51 692–700.CrossRefPubMed Batista ML Jr, Lopes RD, Seelaender MC, Lopes AC. Anti-inflammatory effect of physical training in heart failure: role of TNF-alpha and IL-10. Arq Bras Cardiol. 2009;93:643–51 692–700.CrossRefPubMed
2.
go back to reference Heymans S, Hirsch E, Anker SD, Aukrust P, Balligand JL, Cohen-Tervaert JW, et al. Inflammation as a therapeutic target in heart failure? A scientific statement from the translational research Committee of the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail. 2009;11:119–29.CrossRefPubMedPubMedCentral Heymans S, Hirsch E, Anker SD, Aukrust P, Balligand JL, Cohen-Tervaert JW, et al. Inflammation as a therapeutic target in heart failure? A scientific statement from the translational research Committee of the Heart Failure Association of the European Society of Cardiology. Eur J Heart Fail. 2009;11:119–29.CrossRefPubMedPubMedCentral
3.
go back to reference Komamura K. Similarities and differences between the pathogenesis and pathophysiology of diastolic and systolic heart failure. Cardiol Res Pract. 2013;2013:824135.CrossRefPubMedPubMedCentral Komamura K. Similarities and differences between the pathogenesis and pathophysiology of diastolic and systolic heart failure. Cardiol Res Pract. 2013;2013:824135.CrossRefPubMedPubMedCentral
4.
go back to reference Athanassopoulos P, Vaessen LM, Maat AP, Balk AH, Weimar W, Bogers AJ. Peripheral blood dendritic cells in human end-stage heart failure and the early post-transplant period: evidence for systemic Th1 immune responses. Eur J Cardiothorac Surg. 2004;25:619–26.CrossRefPubMed Athanassopoulos P, Vaessen LM, Maat AP, Balk AH, Weimar W, Bogers AJ. Peripheral blood dendritic cells in human end-stage heart failure and the early post-transplant period: evidence for systemic Th1 immune responses. Eur J Cardiothorac Surg. 2004;25:619–26.CrossRefPubMed
6.
go back to reference Aukrust P, Ueland T, Muller F, Andreassen AK, Nordoy I, Aas H, et al. Elevated circulating levels of C-C chemokines in patients with congestive heart failure. Circulation. 1998;97:1136–43.CrossRefPubMed Aukrust P, Ueland T, Muller F, Andreassen AK, Nordoy I, Aas H, et al. Elevated circulating levels of C-C chemokines in patients with congestive heart failure. Circulation. 1998;97:1136–43.CrossRefPubMed
7.
go back to reference Yndestad A, Damas JK, Geir Eiken H, Holm T, Haug T, Simonsen S, et al. Increased gene expression of tumor necrosis factor superfamily ligands in peripheral blood mononuclear cells during chronic heart failure. Cardiovasc Res. 2002;54:175–82.CrossRefPubMed Yndestad A, Damas JK, Geir Eiken H, Holm T, Haug T, Simonsen S, et al. Increased gene expression of tumor necrosis factor superfamily ligands in peripheral blood mononuclear cells during chronic heart failure. Cardiovasc Res. 2002;54:175–82.CrossRefPubMed
8.
go back to reference Seixas-Cambao M, Leite-Moreira AF. Pathophysiology of chronic heart failure. Rev Port Cardiol. 2009;28:439–71.PubMed Seixas-Cambao M, Leite-Moreira AF. Pathophysiology of chronic heart failure. Rev Port Cardiol. 2009;28:439–71.PubMed
9.
go back to reference Yndestad A, Holm AM, Muller F, Simonsen S, Froland SS, Gullestad L, et al. Enhanced expression of inflammatory cytokines and activation markers in T-cells from patients with chronic heart failure. Cardiovasc Res. 2003;60:141–6.CrossRefPubMed Yndestad A, Holm AM, Muller F, Simonsen S, Froland SS, Gullestad L, et al. Enhanced expression of inflammatory cytokines and activation markers in T-cells from patients with chronic heart failure. Cardiovasc Res. 2003;60:141–6.CrossRefPubMed
10.
go back to reference Evans HG, Gullick NJ, Kelly S, Pitzalis C, Lord GM, Kirkham BW, et al. In vivo activated monocytes from the site of inflammation in humans specifically promote Th17 responses. Proc Natl Acad Sci U S A. 2009;106:6232–7.CrossRefPubMedPubMedCentral Evans HG, Gullick NJ, Kelly S, Pitzalis C, Lord GM, Kirkham BW, et al. In vivo activated monocytes from the site of inflammation in humans specifically promote Th17 responses. Proc Natl Acad Sci U S A. 2009;106:6232–7.CrossRefPubMedPubMedCentral
11.
go back to reference Lee YK, Turner H, Maynard CL, Oliver JR, Chen D, Elson CO, et al. Late developmental plasticity in the T helper 17 lineage. Immunity. 2009;30:92–107.CrossRefPubMedPubMedCentral Lee YK, Turner H, Maynard CL, Oliver JR, Chen D, Elson CO, et al. Late developmental plasticity in the T helper 17 lineage. Immunity. 2009;30:92–107.CrossRefPubMedPubMedCentral
12.
go back to reference Yu Q, Watson RR, Marchalonis JJ, Larson DF. A role for T lymphocytes in mediating cardiac diastolic function. Am J Physiol Heart Circ Physiol. 2005;289:H643–51.CrossRefPubMed Yu Q, Watson RR, Marchalonis JJ, Larson DF. A role for T lymphocytes in mediating cardiac diastolic function. Am J Physiol Heart Circ Physiol. 2005;289:H643–51.CrossRefPubMed
13.
go back to reference Li N, Bian H, Zhang J, Li X, Ji X, Zhang Y. The Th17/Treg imbalance exists in patients with heart failure with normal ejection fraction and heart failure with reduced ejection fraction. Clin Chim Acta. 2010;411:1963–8.CrossRefPubMed Li N, Bian H, Zhang J, Li X, Ji X, Zhang Y. The Th17/Treg imbalance exists in patients with heart failure with normal ejection fraction and heart failure with reduced ejection fraction. Clin Chim Acta. 2010;411:1963–8.CrossRefPubMed
14.
go back to reference Yamaoka-Tojo M, Tojo T, Inomata T, Machida Y, Osada K, Izumi T. Circulating levels of interleukin 18 reflect etiologies of heart failure: Th1/Th2 cytokine imbalance exaggerates the pathophysiology of advanced heart failure. J Card Fail. 2002;8:21–7.CrossRefPubMed Yamaoka-Tojo M, Tojo T, Inomata T, Machida Y, Osada K, Izumi T. Circulating levels of interleukin 18 reflect etiologies of heart failure: Th1/Th2 cytokine imbalance exaggerates the pathophysiology of advanced heart failure. J Card Fail. 2002;8:21–7.CrossRefPubMed
15.
go back to reference Zhu ZF, Li JJ, Liu J, Tang TT, Ding YJ, Liao YH, et al. Circulating Th17 cells are not elevated in patients with chronic heart failure. Scand Cardiovasc J. 2012;46:295–300.CrossRefPubMed Zhu ZF, Li JJ, Liu J, Tang TT, Ding YJ, Liao YH, et al. Circulating Th17 cells are not elevated in patients with chronic heart failure. Scand Cardiovasc J. 2012;46:295–300.CrossRefPubMed
16.
go back to reference Lopes A, Machado D, Pedreiro S, Henriques A, Silva I, Tavares B, et al. Different frequencies of Tc17/Tc1 and Th17/Th1 cells in chronic spontaneous urticaria. Int Arch Allergy Immunol. 2013;161:155–62.CrossRefPubMed Lopes A, Machado D, Pedreiro S, Henriques A, Silva I, Tavares B, et al. Different frequencies of Tc17/Tc1 and Th17/Th1 cells in chronic spontaneous urticaria. Int Arch Allergy Immunol. 2013;161:155–62.CrossRefPubMed
17.
go back to reference Henriques A, Gomes V, Duarte C, Pedreiro S, Carvalheiro T, Areias M, et al. Distribution and functional plasticity of peripheral blood Th(c)17 and Th(c)1 in rheumatoid arthritis. Rheumatol Int. 2013;33:2093–9.CrossRefPubMed Henriques A, Gomes V, Duarte C, Pedreiro S, Carvalheiro T, Areias M, et al. Distribution and functional plasticity of peripheral blood Th(c)17 and Th(c)1 in rheumatoid arthritis. Rheumatol Int. 2013;33:2093–9.CrossRefPubMed
18.
go back to reference Henriques A, Ines L, Couto M, Pedreiro S, Santos C, Magalhaes M, et al. Frequency and functional activity of Th17, Tc17 and other T-cell subsets in systemic lupus erythematosus. Cell Immunol. 2010;264:97–103.CrossRefPubMed Henriques A, Ines L, Couto M, Pedreiro S, Santos C, Magalhaes M, et al. Frequency and functional activity of Th17, Tc17 and other T-cell subsets in systemic lupus erythematosus. Cell Immunol. 2010;264:97–103.CrossRefPubMed
19.
go back to reference Hu Y, Ma DX, Shan NN, Zhu YY, Liu XG, Zhang L, et al. Increased number of Tc17 and correlation with Th17 cells in patients with immune thrombocytopenia. PLoS One. 2011;6(10):e26522.CrossRefPubMedPubMedCentral Hu Y, Ma DX, Shan NN, Zhu YY, Liu XG, Zhang L, et al. Increased number of Tc17 and correlation with Th17 cells in patients with immune thrombocytopenia. PLoS One. 2011;6(10):e26522.CrossRefPubMedPubMedCentral
20.
go back to reference Yen HR, Harris TJ, Wada S, Grosso JF, Getnet D, Goldberg MV, et al. Tc17 CD8 T cells: functional plasticity and subset diversity. J Immunol. 2009;183(11):7161–8.CrossRefPubMedPubMedCentral Yen HR, Harris TJ, Wada S, Grosso JF, Getnet D, Goldberg MV, et al. Tc17 CD8 T cells: functional plasticity and subset diversity. J Immunol. 2009;183(11):7161–8.CrossRefPubMedPubMedCentral
21.
go back to reference McMurray JJ, Adamopoulos S, Anker SD, Auricchio A, Bohm M, Dickstein K, et al. ESC guidelines for the diagnosis and treatment of acute and chronic heart failure 2012: the task force for the diagnosis and treatment of acute and chronic heart failure 2012 of the European Society of Cardiology. Developed in collaboration with the heart failure association (HFA) of the ESC. Eur J Heart Fail. 2012;14:803–69.CrossRefPubMed McMurray JJ, Adamopoulos S, Anker SD, Auricchio A, Bohm M, Dickstein K, et al. ESC guidelines for the diagnosis and treatment of acute and chronic heart failure 2012: the task force for the diagnosis and treatment of acute and chronic heart failure 2012 of the European Society of Cardiology. Developed in collaboration with the heart failure association (HFA) of the ESC. Eur J Heart Fail. 2012;14:803–69.CrossRefPubMed
22.
go back to reference Curtis AB, Yancy CW, Albert NM, Stough WG, Gheorghiade M, Heywood JT, et al. Cardiac resynchronization therapy utilization for heart failure: findings from IMPROVE HF. Am Heart J. 2009;158:956–64.CrossRefPubMed Curtis AB, Yancy CW, Albert NM, Stough WG, Gheorghiade M, Heywood JT, et al. Cardiac resynchronization therapy utilization for heart failure: findings from IMPROVE HF. Am Heart J. 2009;158:956–64.CrossRefPubMed
23.
go back to reference Yu CM, Gorcsan J 3rd, Bleeker GB, Zhang Q, Schalij MJ, Suffoletto MS, et al. Usefulness of tissue Doppler velocity and strain dyssynchrony for predicting left ventricular reverse remodeling response after cardiac resynchronization therapy. Am J Cardiol. 2007;100:1263–70.CrossRefPubMed Yu CM, Gorcsan J 3rd, Bleeker GB, Zhang Q, Schalij MJ, Suffoletto MS, et al. Usefulness of tissue Doppler velocity and strain dyssynchrony for predicting left ventricular reverse remodeling response after cardiac resynchronization therapy. Am J Cardiol. 2007;100:1263–70.CrossRefPubMed
24.
go back to reference Steffel J, Rempel H, Breitenstein A, Schmidt S, Namdar M, Krasniqi N, et al. Comprehensive cardiac resynchronization therapy (CRT) optimization in the real world. Cardiol J. 2014;21:316–24.CrossRefPubMed Steffel J, Rempel H, Breitenstein A, Schmidt S, Namdar M, Krasniqi N, et al. Comprehensive cardiac resynchronization therapy (CRT) optimization in the real world. Cardiol J. 2014;21:316–24.CrossRefPubMed
26.
go back to reference Brouwers C, Spindler H, Larsen ML, Eiskær H, Videbæk L, Pedersen MS, et al. Association between psychological measures and brain natriuretic peptide in heart failure patients. Scand Cardiovasc J. 2012;46(3):154–62.CrossRefPubMed Brouwers C, Spindler H, Larsen ML, Eiskær H, Videbæk L, Pedersen MS, et al. Association between psychological measures and brain natriuretic peptide in heart failure patients. Scand Cardiovasc J. 2012;46(3):154–62.CrossRefPubMed
27.
go back to reference Michelucci A, Ricciardi G, Sofi F, Gori AM, Pirolo F, Pieragnoli P, et al. Relation of inflammatory status to major adverse cardiac events and reverse remodeling in patients undergoing cardiac resynchronization therapy. J Card Fail. 2007;13(3):207–10.CrossRefPubMed Michelucci A, Ricciardi G, Sofi F, Gori AM, Pirolo F, Pieragnoli P, et al. Relation of inflammatory status to major adverse cardiac events and reverse remodeling in patients undergoing cardiac resynchronization therapy. J Card Fail. 2007;13(3):207–10.CrossRefPubMed
28.
go back to reference Osmancik P, Herman D, Stros P, Linkova H, Vondrak K, Paskova E. Changes and prognostic impact of apoptotic and inflammatory cytokines in patients treated with cardiac resynchronization therapy. Cardiology. 2013;124(3):190–8.CrossRefPubMed Osmancik P, Herman D, Stros P, Linkova H, Vondrak K, Paskova E. Changes and prognostic impact of apoptotic and inflammatory cytokines in patients treated with cardiac resynchronization therapy. Cardiology. 2013;124(3):190–8.CrossRefPubMed
29.
go back to reference Lappegard KT, Bjørnstad H, Mollnes TE, Hovland A. Effect of cardiac resynchronization therapy on inflammation in congestive heart failure: a review. Scand J Immunol. 2015;82(3):191–8.CrossRefPubMed Lappegard KT, Bjørnstad H, Mollnes TE, Hovland A. Effect of cardiac resynchronization therapy on inflammation in congestive heart failure: a review. Scand J Immunol. 2015;82(3):191–8.CrossRefPubMed
30.
go back to reference Glick A, Michowitz Y, Keren G, George J. Neurohormonal and inflammatory markers as predictors of short-term outcome in patients with heart failure and cardiac resynchronization therapy. Isr Med Assoc J. 2006;8(6):391–5.PubMed Glick A, Michowitz Y, Keren G, George J. Neurohormonal and inflammatory markers as predictors of short-term outcome in patients with heart failure and cardiac resynchronization therapy. Isr Med Assoc J. 2006;8(6):391–5.PubMed
31.
go back to reference Shinohara T, Takahashi N, Saito S, Okada N, Wakisaka O, et al. Effect of cardiac resynchronization therapy on cardiac sympathetic nervous dysfunction and serum C-reactive protein level. Pacing Clin Electrophysiol. 2011;34(10):1225–30.CrossRefPubMed Shinohara T, Takahashi N, Saito S, Okada N, Wakisaka O, et al. Effect of cardiac resynchronization therapy on cardiac sympathetic nervous dysfunction and serum C-reactive protein level. Pacing Clin Electrophysiol. 2011;34(10):1225–30.CrossRefPubMed
34.
go back to reference Antonio N, Teixeira R, Lourenco C, Saraiva F, Coelho L, Martins R, et al. Which echocardiographic definition should be used to define response to cardiac resynchronization therapy? Rev Port Cardiol. 2009;28:943–58.PubMed Antonio N, Teixeira R, Lourenco C, Saraiva F, Coelho L, Martins R, et al. Which echocardiographic definition should be used to define response to cardiac resynchronization therapy? Rev Port Cardiol. 2009;28:943–58.PubMed
35.
go back to reference Kydd AC, Khan FZ, Ring L, Pugh PJ, Virdee MS, Dutka DP. Development of a multiparametric score to predict left ventricular remodelling and prognosis after cardiac resynchronization therapy. Eur J Heart Fail. 2014;16(11):1206–13.CrossRefPubMed Kydd AC, Khan FZ, Ring L, Pugh PJ, Virdee MS, Dutka DP. Development of a multiparametric score to predict left ventricular remodelling and prognosis after cardiac resynchronization therapy. Eur J Heart Fail. 2014;16(11):1206–13.CrossRefPubMed
36.
go back to reference Doltra A, Bijnens B, Tolosana JM, Borras R, Khatib M, Penela D, et al. Mechanical abnormalities detected with conventional echocardiography are associated with response and midterm survival in CRT. JACC Cardiovasc Imaging. 2014;7:969–79.CrossRefPubMed Doltra A, Bijnens B, Tolosana JM, Borras R, Khatib M, Penela D, et al. Mechanical abnormalities detected with conventional echocardiography are associated with response and midterm survival in CRT. JACC Cardiovasc Imaging. 2014;7:969–79.CrossRefPubMed
37.
go back to reference Rordorf R, Savastano S, Sanzo A, Spazzolini C, De Amici M, Camporotondo R, et al. Tumor necrosis factor-alpha predicts response to cardiac resynchronization therapy in patients with chronic heart failure. Circ J. 2014;78:2232–9.CrossRefPubMed Rordorf R, Savastano S, Sanzo A, Spazzolini C, De Amici M, Camporotondo R, et al. Tumor necrosis factor-alpha predicts response to cardiac resynchronization therapy in patients with chronic heart failure. Circ J. 2014;78:2232–9.CrossRefPubMed
38.
go back to reference Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3:RESEARCH0034.CrossRefPubMedPubMedCentral Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3:RESEARCH0034.CrossRefPubMedPubMedCentral
40.
go back to reference Cai YH, Ma ZJ, Lu XY, He EL, You MY. Study on the effect and mechanism of the dysfunction of CD4(+) T cells in the disease process of chronic cardiac failure. Asian Pac J Trop Med. 2016;9:682–7.CrossRefPubMed Cai YH, Ma ZJ, Lu XY, He EL, You MY. Study on the effect and mechanism of the dysfunction of CD4(+) T cells in the disease process of chronic cardiac failure. Asian Pac J Trop Med. 2016;9:682–7.CrossRefPubMed
41.
go back to reference Li XF, Pan D, Zhang WL, Zhou J, Liang JJ. Association of NT-proBNP and interleukin-17 levels with heart failure in elderly patients. Genet Mol Res. 2016;15. Li XF, Pan D, Zhang WL, Zhou J, Liang JJ. Association of NT-proBNP and interleukin-17 levels with heart failure in elderly patients. Genet Mol Res. 2016;15.
42.
go back to reference Sandip C, Tan L, Huang J, Li Q, Ni L, Cianflone K, et al. Common variants in IL-17A/IL-17RA axis contribute to predisposition to and progression of congestive heart failure. Medicine (Baltimore). 2016;95:e4105.CrossRef Sandip C, Tan L, Huang J, Li Q, Ni L, Cianflone K, et al. Common variants in IL-17A/IL-17RA axis contribute to predisposition to and progression of congestive heart failure. Medicine (Baltimore). 2016;95:e4105.CrossRef
43.
go back to reference Min X, Lu M, Tu S, Wang X, Zhou C, Wang S, et al. Serum cytokine profile in relation to the severity of coronary artery disease. Biomed Res Int. 2017;2017:4013685.PubMedPubMedCentral Min X, Lu M, Tu S, Wang X, Zhou C, Wang S, et al. Serum cytokine profile in relation to the severity of coronary artery disease. Biomed Res Int. 2017;2017:4013685.PubMedPubMedCentral
44.
go back to reference Milovanovic M, Pesic G, Nikolic V, Jevtovic-Stoimenov T, Vasic K, Jovic Z, et al. Vitamin D deficiency is associated with increased IL-17 and TNFalpha levels in patients with chronic heart failure. Arq Bras Cardiol. 2012;98:259–65.CrossRefPubMed Milovanovic M, Pesic G, Nikolic V, Jevtovic-Stoimenov T, Vasic K, Jovic Z, et al. Vitamin D deficiency is associated with increased IL-17 and TNFalpha levels in patients with chronic heart failure. Arq Bras Cardiol. 2012;98:259–65.CrossRefPubMed
45.
go back to reference Lappegard KT, Bjornstad H. Anti-inflammatory effect of cardiac resynchronization therapy. Pacing Clin Electrophysiol. 2006;29:753–8.CrossRefPubMed Lappegard KT, Bjornstad H. Anti-inflammatory effect of cardiac resynchronization therapy. Pacing Clin Electrophysiol. 2006;29:753–8.CrossRefPubMed
46.
go back to reference Yu CM, Bleeker GB, Fung JW, Schalij MJ, Zhang Q, et al. Left ventricular reverse remodeling but not clinical improvement predicts long-term survival after cardiac resynchronization therapy. Circulation. 2005;112(11):1580–6.CrossRefPubMed Yu CM, Bleeker GB, Fung JW, Schalij MJ, Zhang Q, et al. Left ventricular reverse remodeling but not clinical improvement predicts long-term survival after cardiac resynchronization therapy. Circulation. 2005;112(11):1580–6.CrossRefPubMed
48.
go back to reference Mesquita D Jr, Cruvinel WM, Camara NO, Kallas EG, Andrade LE. Autoimmune diseases in the TH17 era. Braz J Med Biol Res. 2009;42:476–86.CrossRefPubMed Mesquita D Jr, Cruvinel WM, Camara NO, Kallas EG, Andrade LE. Autoimmune diseases in the TH17 era. Braz J Med Biol Res. 2009;42:476–86.CrossRefPubMed
49.
go back to reference Adamopoulos S, Parissis JT, Kremastinos DT. A glossary of circulating cytokines in chronic heart failure. Eur J Heart Fail. 2001;3:517–26.CrossRefPubMed Adamopoulos S, Parissis JT, Kremastinos DT. A glossary of circulating cytokines in chronic heart failure. Eur J Heart Fail. 2001;3:517–26.CrossRefPubMed
50.
go back to reference Xu WH, Hu XL, Liu XF, Bai P, Sun YC. Peripheral Tc17 and Tc17/interferon-gamma cells are increased and associated with lung function in patients with chronic obstructive pulmonary disease. Chin Med J (Engl). 2016;129:909–16.CrossRef Xu WH, Hu XL, Liu XF, Bai P, Sun YC. Peripheral Tc17 and Tc17/interferon-gamma cells are increased and associated with lung function in patients with chronic obstructive pulmonary disease. Chin Med J (Engl). 2016;129:909–16.CrossRef
51.
go back to reference Hayes MD, Ovcinnikovs V, Smith AG, Kimber I, Dearman RJ. The aryl hydrocarbon receptor: differential contribution to T helper 17 and T cytotoxic 17 cell development. PLoS One. 2014;9(9):e106955.CrossRefPubMedPubMedCentral Hayes MD, Ovcinnikovs V, Smith AG, Kimber I, Dearman RJ. The aryl hydrocarbon receptor: differential contribution to T helper 17 and T cytotoxic 17 cell development. PLoS One. 2014;9(9):e106955.CrossRefPubMedPubMedCentral
Metadata
Title
Impact of cardiac resynchronization therapy on circulating IL-17 producing cells in patients with advanced heart failure
Authors
Sílvia Martins
Tiago Carvalheiro
Paula Laranjeira
António Martinho
Luís Elvas
Lino Gonçalves
Cândida Tomaz
Natália António
Artur Paiva
Publication date
01-04-2019
Publisher
Springer US
Published in
Journal of Interventional Cardiac Electrophysiology / Issue 3/2019
Print ISSN: 1383-875X
Electronic ISSN: 1572-8595
DOI
https://doi.org/10.1007/s10840-018-0491-3

Other articles of this Issue 3/2019

Journal of Interventional Cardiac Electrophysiology 3/2019 Go to the issue