Pro-inflammatory Mediators and Oxidative Stress: Therapeutic Markers for Recurrent Angina Pectoris after Coronary Artery Stenting in Elderly Patients

Page: [643 - 654] Pages: 12

  • * (Excluding Mailing and Handling)

Abstract

Background: Pro-inflammatory mediators and oxidative stress are related to the severity of angina pectoris in patients with coronary heart disease.

Objective: We evaluated the effects of pro-inflammatory mediators and oxidative stress on recurrent angina pectoris after coronary artery stenting in elderly patients.

Methods: We determined the expression levels of malondialdehyde (MDA), acrolein (ACR), tumour necrosis factor-α (TNF-α), toll-like receptor 4 (TLR4), superoxide dismutase 3 (SOD3), paraoxonase-1 (PON-1), stromal cell-derived factor-1α (SDF-1α) and endothelial progenitor cells (EPCs) in elderly patients with recurrent angina pectoris after coronary artery stenting.

Results: Levels of MDA, ACR, TNF-α and TLR4 were significantly increased (p<0.001), and levels of SOD3, PON-1, SDF-1α and EPCs were significantly decreased (p<0.001) in the elderly patients with recurrent angina pectoris after coronary artery stenting. MDA, ACR, TNF-α and TLR4 as markers of oxidative stress and pro-inflammatory mediators may have suppressed SOD3, PON-1, SDF-1α and EPCs as markers of anti-oxidative stress/anti-inflammatory responses. Oxidative stress and proinflammatory mediators were important factors involved in recurrent angina pectoris of elderly patients after coronary artery stenting.

Conclusion: Oxidative stress and pro-inflammatory mediators could be considered as potential noninvasive prognostic, predictive, and therapeutic biomarkers for stable recurrent angina and recurrent unstable angina in elderly patients after coronary artery stenting.

Keywords: Pro-inflammatory mediator, oxidative stress, recurrent angina pectoris, coronary artery stenting, elderly, heart disease.

Graphical Abstract

[1]
Javid AZ, Haybar H, Dehghan P, et al. The effects of Melissa officinalis (lemon balm) in chronic stable angina on serum biomarkers of oxidative stress, inflammation and lipid profile. Asia Pac J Clin Nutr 2018; 27(4): 785-91.
[PMID: 30045422]
[2]
Kumari R, Kumar S, Ahmad MK, et al. Promoter variants of TNF-α rs1800629 and IL-10 rs1800871 are independently associated with the susceptibility of coronary artery disease in north Indian. Cytokine 2018; 110: 131-6.
[http://dx.doi.org/10.1016/j.cyto.2018.04.035] [PMID: 29734056]
[3]
Rolski F, Błyszczuk P. Complexity of TNF-α signaling in heart disease. J Clin Med 2020; 9(10): 3267.
[http://dx.doi.org/10.3390/jcm9103267] [PMID: 33053859]
[4]
Colmorten KB, Nexoe AB, Sorensen GL. The dual role of surfactant protein-D in vascular inflammation and development of cardiovascular disease. Front Immunol 2019; 10: 2264.
[http://dx.doi.org/10.3389/fimmu.2019.02264] [PMID: 31616435]
[5]
Sawano M, Katsuki T, Kitai T, et al. Beta blockers versus calcium channel blockers for provocation of vasospastic angina after drug-eluting stent implantation: a multicentre prospective randomised trial. Open Heart 2020; 7(2)e001406
[http://dx.doi.org/10.1136/openhrt-2020-001406] [PMID: 33087441]
[6]
Ljung L, Askling J, Rantapää-Dahlqvist S, Jacobsson L. The risk of acute coronary syndrome in rheumatoid arthritis in relation to tumour necrosis factor inhibitors and the risk in the general population: a national cohort study. Arthritis Res Ther 2014; 16(3): R127.
[http://dx.doi.org/10.1186/ar4584] [PMID: 24941916]
[7]
Dixon WG, Watson KD, Lunt M, Hyrich KL, Silman AJ, Symmons DP. Reduction in the incidence of myocardial infarction in patients with rheumatoid arthritis who respond to anti-tumor necrosis factor alpha therapy: results from the British Society for Rheumatology Biologics Register. Arthritis Rheum 2007; 56(9): 2905-12.
[http://dx.doi.org/10.1002/art.22809] [PMID: 17763428]
[8]
Low AS, Symmons DP, Lunt M, et al. Relationship between exposure to tumour necrosis factor inhibitor therapy and incidence and severity of myocardial infarction in patients with rheumatoid arthritis. Ann Rheum Dis 2017; 76(4): 654-60.
[http://dx.doi.org/10.1136/annrheumdis-2016-209784] [PMID: 28073800]
[9]
Wu JJ, Poon KY, Channual JC, Shen AY. Association between tumor necrosis factor inhibitor therapy and myocardial infarction risk in patients with psoriasis. Arch Dermatol 2012; 148(11): 1244-50.
[http://dx.doi.org/10.1001/archdermatol.2012.2502] [PMID: 22911151]
[10]
Wu JJ, Sundaram M, Cloutier M, et al. The risk of cardiovascular events in psoriasis patients treated with tumor necrosis factor-α inhibitors versus phototherapy: An observational cohort study. J Am Acad Dermatol 2018; 79(1): 60-8.
[http://dx.doi.org/10.1016/j.jaad.2018.02.050] [PMID: 29499292]
[11]
Sargowo D, Ovianti N, Susilowati E, et al. The role of polysaccharide peptide of Ganoderma lucidum as a potent antioxidant against atherosclerosis in high risk and stable angina patients. Indian Heart J 2018; 70(5): 608-14.
[http://dx.doi.org/10.1016/j.ihj.2017.12.007] [PMID: 30392496]
[12]
Papac-Milicevic N, Busch CJ, Binder CJJ-L, Busch C, Binder CJ. Malondialdehyde epitopes as targets of immunity and the implications for atherosclerosis. Adv Immunol 2016; 131: 1-59.
[http://dx.doi.org/10.1016/bs.ai.2016.02.001] [PMID: 27235680]
[13]
Constantinescu MI, Constantinescu DP, Andercou A, Mironiuc IA. Influence of sildenafil and donepezil administration on the serum redox balance in experimentally induced lower limb critical ischemia. Clujul Med 2013; 86(3): 250-8.
[PMID: 26527957]
[14]
Higashi T, Elmeligy E, Mai Y, et al. Glutathione and cysteines suppress cytotoxicity of gas phase of cigarette smoke by direct reacting with unsaturated carbonyl compounds in the gas phase. Biochem Biophys Res Commun 2019; 509(4): 988-93.
[http://dx.doi.org/10.1016/j.bbrc.2019.01.040] [PMID: 30654934]
[15]
Wu X, Li C, Mariyam Z, et al. Acrolein-induced atherogenesis by stimulation of hepatic flavin containing monooxygenase 3 and a protection from hydroxytyrosol. J Cell Physiol 2018; 234(1): 475-85.
[http://dx.doi.org/10.1002/jcp.26600] [PMID: 29953618]
[16]
Li X, Guo D, Zhou H, et al. Side effects of coronary stenting such as severe coronary stenosis and multiple coronary chronic total occlusions in elderly patients via induced proinflammatory and prooxidative stress. Mediators Inflamm 2019; 20197147652
[http://dx.doi.org/10.1155/2019/7147652] [PMID: 31780868]
[17]
Akash MSH, Rehman K, Liaqat A. Tumor Necrosis Factor-Alpha: Role in development of insulin resistance and pathogenesis of type 2 diabetes mellitus. J Cell Biochem 2018; 119(1): 105-10.
[http://dx.doi.org/10.1002/jcb.26174] [PMID: 28569437]
[18]
Lee JL, Sinnathurai P, Buchbinder R, Hill C, Lassere M, March L. Biologics and cardiovascular events in inflammatory arthritis: a prospective national cohort study. Arthritis Res Ther 2018; 20(1): 171.
[http://dx.doi.org/10.1186/s13075-018-1669-x] [PMID: 30086795]
[19]
Xiao X, Yang C, Qu SL, et al. S100 proteins in atherosclerosis. Clin Chim Acta 2020; 502: 293-304.
[http://dx.doi.org/10.1016/j.cca.2019.11.019] [PMID: 31794767]
[20]
Zhang X, Xue C, Xu Q, et al. Caprylic acid suppresses inflammation via TLR4/NF-κB signaling and improves atherosclerosis in ApoE-deficient mice. Nutr Metab (Lond) 2019; 16: 40.
[http://dx.doi.org/10.1186/s12986-019-0359-2] [PMID: 31182969]
[21]
Tang ZH, Peng J, Ren Z, et al. New role of PCSK9 in atherosclerotic inflammation promotion involving the TLR4/NF-κB pathway. Atherosclerosis 2017; 262: 113-22.
[http://dx.doi.org/10.1016/j.atherosclerosis.2017.04.023] [PMID: 28535426]
[22]
Decharatchakul N, Settasatian C, Settasatian N, et al. Association of combined genetic variations in SOD3, GPX3, PON1, and GSTT1 with hypertension and severity of coronary artery disease. Heart Vessels 2020; 35(7): 918-29.
[http://dx.doi.org/10.1007/s00380-020-01564-6] [PMID: 32034489]
[23]
Decharatchakul N, Settasatian C, Settasatian N, et al. Association of genetic polymorphisms in SOD2, SOD3, GPX3, and GSTT1 with hypertriglyceridemia and low HDL-C level in subjects with high risk of coronary artery disease. PeerJ 2019; 7e7407
[http://dx.doi.org/10.7717/peerj.7407] [PMID: 31396447]
[24]
Roxo DF, Arcaro CA, Gutierres VO, et al. Curcumin combined with metformin decreases glycemia and dyslipidemia, and increases paraoxonase activity in diabetic rats. Diabetol Metab Syndr 2019; 11: 33.
[http://dx.doi.org/10.1186/s13098-019-0431-0] [PMID: 31061679]
[25]
Reichert CO, de Macedo CG, Levy D, et al. Paraoxonases (PON) 1, 2, and 3 polymorphisms and PON-1 activities in patients with sickle cell disease. Antioxidants 2019; 8(8): 252.
[http://dx.doi.org/10.3390/antiox8080252] [PMID: 31366068]
[26]
Chang CT, Lim YP, Lee CW, et al. PON-1 carbamylation is enhanced in HDL of uremia patients. Yao Wu Shi Pin Fen Xi 2019; 27(2): 542-50.
[http://dx.doi.org/10.1016/j.jfda.2018.09.007] [PMID: 30987726]
[27]
Shunmoogam N, Naidoo P, Chilton R. Paraoxonase (PON)-1: a brief overview on genetics, structure, polymorphisms and clinical relevance. Vasc Health Risk Manag 2018; 14: 137-43.
[http://dx.doi.org/10.2147/VHRM.S165173] [PMID: 29950852]
[28]
Seemann S, Lupp A. Administration of a CXCL12 analog in endotoxemia is associated with anti-Inflammatory, anti-oxidative and cytoprotective effects in vivo. PLoS One 2015; 10(9)e0138389
[http://dx.doi.org/10.1371/journal.pone.0138389] [PMID: 26375818]
[29]
He F, Luo PF, Tang T, et al. Targeted release of stromal cell-derived factor-1α by reactive oxygen species-sensitive nanoparticles results in bone marrow stromal cell chemotaxis and homing, and repair of vascular injury caused by electrical burns. PLoS One 2018; 13(3)e0194298
[http://dx.doi.org/10.1371/journal.pone.0194298] [PMID: 29529067]
[30]
Bromage DI, Taferner S, He Z, Ziff OJ, Yellon DM, Davidson SM. Stromal cell-derived factor-1α signals via the endothelium to protect the heart against ischaemia-reperfusion injury. J Mol Cell Cardiol 2019; 128: 187-97.
[http://dx.doi.org/10.1016/j.yjmcc.2019.02.002] [PMID: 30738798]
[31]
Sheng ZQ, Li YF, Zheng KL, et al. The relationship between number and function of EPCs and concentration of VEGF165 and SDF-1 in coronary artery spasm. Eur Rev Med Pharmacol Sci 2018; 22(9): 2767-77.
[PMID: 29771429]
[32]
Seang S, Kelesidis T, Huynh D, et al. Low levels of endothelial progenitor cells and their association with systemic inflammation and monocyte activation in older HIV-infected men. AIDS Res Hum Retroviruses 2018; 34(1): 39-45.
[http://dx.doi.org/10.1089/aid.2017.0057] [PMID: 29226690]
[33]
Rakkar K, Othman O, Sprigg N, Bath P, Bayraktutan U. Endothelial progenitor cells, potential biomarkers for diagnosis and prognosis of ischemic stroke: protocol for an observational case-control study. Neural Regen Res 2020; 15(7): 1300-7.
[http://dx.doi.org/10.4103/1673-5374.269028] [PMID: 31960816]
[34]
Owlia M, Dodson JA, King JB, et al. Angina severity, mortality, and healthcare utilization among veterans with stable angina. J Am Heart Assoc 2019; 8(15): e012811
[http://dx.doi.org/10.1161/JAHA.119.012811] [PMID: 31362569]
[35]
Mizukoshi M, Imanishi T, Tanaka A, et al. Clinical classification and plaque morphology determined by optical coherence tomography in unstable angina pectoris. Am J Cardiol 2010; 106(3): 323-8.
[http://dx.doi.org/10.1016/j.amjcard.2010.03.027] [PMID: 20643240]
[36]
Nagueh SF, Abraham TP, Aurigemma GP, et al. Interobserver variability in applying American society of echocardiography/European association of cardiovascular imaging 2016 guidelines for estimation of left ventricular filling pressure. Circ Cardiovasc Imaging 2019; 12(1): e008122
[http://dx.doi.org/10.1161/CIRCIMAGING.118.008122] [PMID: 30632389]
[37]
Dudzińska E, Gryzinska M, Ognik K, Gil-Kulik P, Kocki J. Oxidative stress and effect of treatment on the oxidation product decomposition processes in IBD. Oxid Med Cell Longev 2018; 2018: 7918261
[http://dx.doi.org/10.1155/2018/7918261] [PMID: 30057685]
[38]
Smukowska-Gorynia A, Rzymski P, Marcinkowska J, et al. Prognostic value of oxidative stress markers in patients with pulmonary arterial or chronic thromboembolic pulmonary hypertension. Oxid Med Cell Longev 2019; 2019: 3795320
[http://dx.doi.org/10.1155/2019/3795320] [PMID: 31929853]
[39]
Li X, Zhang F, Zhou H, et al. Potential prognostic, diagnostic and therapeutic markers for in-stent reocclusion in advanced age patients after coronary stenting. Curr Pharm Des 2018; 24(28): 3359-65.
[http://dx.doi.org/10.2174/1381612824666180830141918] [PMID: 30173641]
[40]
Xu P, Elamin E, Elizalde M, et al. Modulation of intestinal epithelial permeability by plasma from patients with Crohn’s disease in a three-dimensional cell culture model. Sci Rep 2019; 9(1): 2030.
[http://dx.doi.org/10.1038/s41598-018-38322-8] [PMID: 30765731]
[41]
Zahran AM, Zahran ZAM, El-Badawy O, et al. Prognostic impact of toll-like receptors 2 and 4 expression on monocytes in Egyptian patients with hepatocellular carcinoma. Immunol Res 2019; 67(2-3): 157-65.
[http://dx.doi.org/10.1007/s12026-019-09075-x] [PMID: 31028612]
[42]
Řádek M, Babuňková E, Špaček M, Kvasnička T, Kvasnička J. Determination of circulating endothelial cells and endothelial progenitor cells using multicolor flow cytometry in patients with thrombophilia. Acta Haematol 2019; 142(2): 113-9.
[http://dx.doi.org/10.1159/000499524] [PMID: 30995655]
[43]
Ying JW, Wen TY, Pei SS, Su LH, Ruan DK. Stromal cell-derived factor-1α promotes recruitment and differentiation of nucleus pulposus-derived stem cells. World J Stem Cells 2019; 11(3): 196-211.
[http://dx.doi.org/10.4252/wjsc.v11.i3.196] [PMID: 30949297]
[44]
Jeong JW, Oh JH, Ji YG, et al. Liquid chromatography-tandem mass spectrometry of recombinant human extracellular superoxide dismutase (rhSOD3) in mouse plasma and its application to pharmacokinetic study. J Pharm Biomed Anal 2019; 164: 590-7.
[http://dx.doi.org/10.1016/j.jpba.2018.11.008] [PMID: 30469108]
[45]
Al-Naimi MS, Hussien NR, Rasheed HA, Al-Kuraishy HM, Al-Gareeb AI. Levothyroxine improves Paraoxonase (PON-1) serum levels in patients with primary hypothyroidism: Case-control study. J Adv Pharm Technol Res 2018; 9(3): 113-8.
[http://dx.doi.org/10.4103/japtr.JAPTR_298_18] [PMID: 30338238]
[46]
Mancini GBJ, Boden WE, Brooks MM, et al. Impact of treatment strategies on outcomes in patients with stable coronary artery disease and type 2 diabetes mellitus according to presenting angina severity: A pooled analysis of three federally-funded randomized trials. Atherosclerosis 2018; 277: 186-94.
[http://dx.doi.org/10.1016/j.atherosclerosis.2018.04.005] [PMID: 29861270]
[47]
Deckers JW. Classification of myocardial infarction and unstable angina: a re-assessment. Int J Cardiol 2013; 167(6): 2387-90.
[http://dx.doi.org/10.1016/j.ijcard.2013.01.008] [PMID: 23384481]
[48]
Sørensen AL, Hasselbalch HC, Nielsen CH, Poulsen HE, Ellervik C. Statin treatment, oxidative stress and inflammation in a Danish population. Redox Biol 2019; 21: 101088
[http://dx.doi.org/10.1016/j.redox.2018.101088] [PMID: 30594900]
[49]
Jorat MV, Tabrizi R, Kolahdooz F, et al. The effects of coenzyme Q10 supplementation on biomarkers of inflammation and oxidative stress in among coronary artery disease: a systematic review and meta-analysis of randomized controlled trials. Inflammopharmacology 2019; 27(2): 233-48.
[http://dx.doi.org/10.1007/s10787-019-00572-x] [PMID: 30758695]
[50]
Liguori I, Russo G, Curcio F, et al. Oxidative stress, aging, and diseases. Clin Interv Aging 2018; 13: 757-72.
[http://dx.doi.org/10.2147/CIA.S158513] [PMID: 29731617]
[51]
Sangsefidi ZS, Yaghoubi F, Hajiahmadi S, Hosseinzadeh M. The effect of coenzyme Q10 supplementation on oxidative stress: A systematic review and meta-analysis of randomized controlled clinical trials. Food Sci Nutr 2020; 8(4): 1766-76.
[http://dx.doi.org/10.1002/fsn3.1492] [PMID: 32328242]
[52]
Crea F, Bairey Merz CN, Beltrame JF, et al. Mechanisms and diagnostic evaluation of persistent or recurrent angina following percutaneous coronary revascularization. Eur Heart J 2019; 40(29): 2455-62.
[http://dx.doi.org/10.1093/eurheartj/ehy857] [PMID: 30608528]
[53]
Cai JG, Luo LM, Tang H, Zhou L. Cytotoxicity of malondialdehyde and cytoprotective effects of taurine via oxidative stress and PGC-1α signal pathway in C2C12 Cells. Mol Biol (Mosk) 2018; 52(4): 616-27.
[http://dx.doi.org/10.1134/S0026898418040043] [PMID: 30113027]
[54]
Chaohui C, Wei H, Hongfeng W, et al. iRhom2 promotes atherosclerosis through macrophage inflammation and induction of oxidative stress. Biochem Biophys Res Commun 2018; 503(3): 1897-904.
[http://dx.doi.org/10.1016/j.bbrc.2018.07.133] [PMID: 30097271]
[55]
Horiyama S, Hatai M, Ichikawa A, Yoshikawa N, Nakamura K, Kunitomo M. Detoxification mechanism of α,β-unsaturated carbonyl compounds in cigarette smoke observed in sheep erythrocytes. Chem Pharm Bull (Tokyo) 2018; 66(7): 721-6.
[http://dx.doi.org/10.1248/cpb.c18-00061] [PMID: 29962455]
[56]
Zirak MR, Mehri S, Karimani A, Zeinali M, Hayes AW, Karimi G. Mechanisms behind the atherothrombotic effects of acrolein, a review. Food Chem Toxicol 2019; 129: 38-53.
[http://dx.doi.org/10.1016/j.fct.2019.04.034] [PMID: 31009736]
[57]
Che Man R, Sulaiman N, Ishak MF, Bt Hj Idrus R, Abdul Rahman MR, Yazid MD. The effects of pro-inflammatory and anti-inflammatory agents for the suppression of intimal hyperplasia: An evidence-based review. Int J Environ Res Public Health 2020; 17(21): 7825.
[http://dx.doi.org/10.3390/ijerph17217825] [PMID: 33114632]
[58]
Oberoi R, Vlacil AK, Schuett J, et al. Anti-tumor necrosis factor-α therapy increases plaque burden in a mouse model of experimental atherosclerosis. Atherosclerosis 2018; 277: 80-9.
[http://dx.doi.org/10.1016/j.atherosclerosis.2018.08.030] [PMID: 30176568]
[59]
Liu P, Zhu W, Chen C, et al. The mechanisms of lysophosphatidylcholine in the development of diseases. Life Sci 2020; 247: 117443
[http://dx.doi.org/10.1016/j.lfs.2020.117443] [PMID: 32084434]
[60]
Chen G, Chen XL, Xu CB, et al. Toll-like receptor protein 4 monoclonal antibody inhibits mmLDL-induced endothelium-dependent vasodilation dysfunction of mouse mesenteric arteries. Microvasc Res 2020; 127: 103923
[http://dx.doi.org/10.1016/j.mvr.2019.103923] [PMID: 31494123]
[61]
Singh RK, Haka AS, Asmal A, et al. TLR4 (toll-like receptor 4)-dependent signaling drives extracellular catabolism of LDL (low-density lipoprotein) aggregates. Arterioscler Thromb Vasc Biol 2020; 40(1): 86-102.
[http://dx.doi.org/10.1161/ATVBAHA.119.313200] [PMID: 31597445]
[62]
Agrahari G, Sah SK, Kim TY. Superoxide dismutase 3 protects mesenchymal stem cells through enhanced autophagy and regulation of FoxO3a trafficking. BMB Rep 2018; 51(7): 344-9.
[http://dx.doi.org/10.5483/BMBRep.2018.51.7.078] [PMID: 29921412]
[63]
Werta KJ, Veleza G, Cross MR, et al. Extracellular superoxide dismutase (SOD3) regulates oxidative stress at the vitreoretinal interface. Free Radic Biol Med 2018; 124: 408-19.
[64]
Wen JJ, Garg NJ. Manganese superoxide dismutase deficiency exacerbates the mitochondrial ROS production and oxidative damage in Chagas disease. PLoS Negl Trop Dis 2018; 12: e0006687
[65]
Lioudaki S, Verikokos C, Kouraklis G, et al. Paraoxonase-1: characteristics and role in atherosclerosis and carotid artery disease. Curr Vasc Pharmacol 2019; 17(2): 141-6.
[http://dx.doi.org/10.2174/1570161115666171129212359] [PMID: 29189170]
[66]
Munjal A, Khandia R. Atherosclerosis: orchestrating cells and biomolecules involved in its activation and inhibition. Adv Protein Chem Struct Biol 2020; 120: 85-122.
[http://dx.doi.org/10.1016/bs.apcsb.2019.11.002] [PMID: 32085889]
[67]
Geng L, Wang S, Li X, et al. Association between Type I interferon and depletion and dysfunction of endothelial progenitor cells in C57BL/6 mice deficient in both apolipoprotein E and Fas ligand. Curr Res Transl Med 2018; 66(3): 71-82.
[http://dx.doi.org/10.1016/j.retram.2018.02.002] [PMID: 30108025]
[68]
Low EL, Baker AH, Bradshaw AC. TGFβ, smooth muscle cells and coronary artery disease: a review. Cell Signal 2019; 53: 90-101.
[http://dx.doi.org/10.1016/j.cellsig.2018.09.004] [PMID: 30227237]
[69]
Nakazaki M, Oka S, Sasaki M, et al. Prevention of neointimal hyperplasia induced by an endovascular stent via intravenous infusion of mesenchymal stem cells. J Neurosurg 2019; 1-13.
[http://dx.doi.org/10.3171/2019.7.JNS19575] [PMID: 31585431]
[70]
Wang P, Liu J, Luo X, et al. A tannic acid-modified fluoride pre-treated Mg-Zn-Y-Nd alloy with antioxidant and platelet-repellent functionalities for vascular stent application. J Mater Chem B Mater Biol Med 2019; 7(46): 7314-25.
[http://dx.doi.org/10.1039/C9TB01587F] [PMID: 31674636]