Abstract
Substantial epidemiological and experimental studies have shown that ambient fine particulate matter (PM2.5) exposure can lead to myocardial damage in human and animal through the mechanism of inflammation and oxidative stress. The purpose of the current study was to investigate whether selenium yeast (SeY) supplementation could prevent cardiovascular injury caused by PM2.5 in rats. Fifty-six Sprague-Dawley rats were randomly divided into seven groups: saline control group; solvent control group, low-, middle-, and high-dose Se pretreatment groups, PM2.5 exposure group, and high-dose Se control group. The rats were pretreated with different concentration of dietary SeY for 28 days, then were exposed to PM2.5 by intratracheal instillation every other day, a total of three times. The levels of inflammatory markers (tumor necrosis factor-alpha (TNF-α), interleukin-1beta (IL-1β), soluble intercellular adhesion molecule-1 (sICAM-1), and oxidative responses-related indicators total antioxidant capacity (T-AOC), total superoxide dismutase (T-SOD), glutathione peroxidase (GSH-Px), and malondialdehyde (MDA) were measured in blood and myocardium of the left ventricle. The results showed that although PM2.5 caused a decrease of T-AOC, T-AOD, and GSH-Px and increase of MDA and sICM-1, pretreatment with SeY induced a dose-dependent increase in these anti-oxidative indicators and a decrease in oxidative indicators. In addition, the levels of TNF-α and IL-1β in Se pretreatment groups were significantly lower than that in PM2.5 exposure group. The results indicated that Se supplementation could effectively prevent cardiovascular inflammation and oxidative stress induced by PM2.5. The results also indicated that the nutritional supplementation might be an effective way to protecting people’s health from air pollution.
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References
Ando M, Shima M, Adachi M, Tsunetoshi Y (2001) The role of intercellular adhesion molecule-1 (ICAM-1), vascular cell adhesion molecule-1 (VCAM-1), and regulated on activation, normal T-cell expressed and secreted (RANTES) in the relationship between air pollution and asthma among children. Arch Environ Health 56:227–233. https://doi.org/10.1080/00039890109604446
Atkinson RW, Kang S, Anderson HR, Mills IC, Walton HA (2014) Epidemiological time series studies of PM2.5 and daily mortality and hospital admissions: a systematic review and meta-analysis. Thorax 69:660–665. https://doi.org/10.1136/thoraxjnl-2013-204492
Bains M, Hall ED (2012) Antioxidant therapies in traumatic brain and spinal cord injury. Biochim Biophys Acta 1822:675–684. https://doi.org/10.1016/j.bbadis.2011.10.017
Betancor MB, Almaida-Pagan PF, Sprague M, Hernandez A, Tocher DR (2015) Roles of selenoprotein antioxidant protection in zebrafish, Danio rerio, subjected to dietary oxidative stress. Fish Physiol Biochem 41:705–720. https://doi.org/10.1007/s10695-015-0040-2
Brook RD, Rajagopalan S, Pope CA, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, Peters A, Siscovick D, Smith SC, Whitsel L, Kaufman JD, on behalf of the American Heart Association Council on Epidemiology and Prevention, Council on the Kidney in Cardiovascular Disease, and Council on Nutrition, Physical Activity and Metabolism (2010) Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation 121:2331–2378. https://doi.org/10.1161/CIR.0b013e3181dbece1
Chaabane M et al (2016) Improvement of heart redox states contributes to the beneficial effects of selenium against penconazole-induced cardiotoxicity in adult rats. Biol Trace Elem Res 169:261–270. https://doi.org/10.1007/s12011-015-0426-0
Damaceno-Rodrigues NR, Veras MM, Negri EM, Zanchi ACT, Rhoden CR, Saldiva PHN, Dolhnikoff M, Caldini EG (2009) Effect of pre- and postnatal exposure to urban air pollution on myocardial lipid peroxidation levels in adult mice. Inhal Toxicol 21:1129–1137. https://doi.org/10.3109/08958370902798430
Delfino RJ, Staimer N, Tjoa T, Polidori A, Arhami M, Gillen DL, Kleinman MT, Vaziri ND, Longhurst J, Zaldivar F, Sioutas C (2008) Circulating biomarkers of inflammation, antioxidant activity, and platelet activation are associated with primary combustion aerosols in subjects with coronary artery disease. Environ Health Perspect 116:898–906. https://doi.org/10.1289/ehp.11189
Delfino RJ, Staimer N, Vaziri ND (2011) Air pollution and circulating biomarkers of oxidative stress. Air Qual Atmos Health 4:37–52. https://doi.org/10.1007/s11869-010-0095-2
Dockery DW (2009) Health effects of particulate air pollution. Ann Epidemiol 19:257–263. https://doi.org/10.1016/j.annepidem.2009.01.018
Driscoll KE, Costa DL, Hatch G, Henderson R, Oberdorster G, Salem H, Schlesinger RB (2000) Intratracheal instillation as an exposure technique for the evaluation of respiratory tract toxicity: uses and limitations. Toxicol Sci 55:24–35. https://doi.org/10.1093/toxsci/55.1.24
Du X et al (2017) Combined effects of vitamin E and omega-3 fatty acids on protecting ambient PM2.5-induced cardiovascular injury in rats. Chemosphere 173:14–21. https://doi.org/10.1016/j.chemosphere.2017.01.042
Fairweather-Tait SJ, Bao Y, Broadley MR, Collings R, Ford D, Hesketh JE, Hurst R (2011) Selenium in human health and disease. Antioxid Redox Signal 14:1337–1383. https://doi.org/10.1089/ars.2010.3275
Fang SC, Eisen EA, Cavallari JM, Mittleman MA, Christiani DC (2010) Circulating adhesion molecules after short-term exposure to particulate matter among welders. Occup Environ Med 67:11–16. https://doi.org/10.1136/oem.2008.043794
Flores-Mateo G, Carrillo-Santisteve P, Elosua R, Guallar E, Marrugat J, Bleys J, Covas MI (2009) Antioxidant enzyme activity and coronary heart disease: meta-analyses of observational studies. Am J Epidemiol 170:135–147. https://doi.org/10.1093/aje/kwp112
Gorr MW, Velten M, Nelin TD, Youtz DJ, Sun Q, Wold LE (2014) Early life exposure to air pollution induces adult cardiac dysfunction. Am J Physiol Heart Circ Physiol 307:H1353–H1360. https://doi.org/10.1152/ajpheart.00526.2014
Gurgueira SA, Lawrence J, Coull B, Murthy GG, Gonzalez-Flecha B (2002) Rapid increases in the steady-state concentration of reactive oxygen species in the lungs and heart after particulate air pollution inhalation. Environ Health Perspect 110:749–755
Han Y, Zhu T (2015) Health effects of fine particles (PM2.5) in ambient air. Sci China Life Sci 58:624–626. https://doi.org/10.1007/s11427-015-4878-4
Han W, Dan W, Shuo Y, Fang Z, Wenjun D (2011) Oxidative stress induced by urban fine particles in cultured EA.hy926 cells. Hum Exp Toxicol 30:579–590. https://doi.org/10.1177/0960327110374207
Hennig B, Ettinger AS, Jandacek RJ, Koo S, McClain C, Seifried H, Silverstone A, Watkins B, Suk WA (2007) Using nutrition for intervention and prevention against environmental chemical toxicity and associated diseases. Environ Health Perspect 115:493–495. https://doi.org/10.1289/ehp.9549
Hoeft B, Weber P, Eggersdorfer M (2012) Micronutrients—a global perspective on intake, health benefits and economics. Int J Vitam Nutr Res 82:316–320. https://doi.org/10.1024/0300-9831/a000125
Ju W, Li X, Li Z, Wu GR, Fu XF, Yang XM, Zhang XQ, Gao XB (2017) The effect of selenium supplementation on coronary heart disease: a systematic review and meta-analysis of randomized controlled trials. J Trace Elem Med Biol 44:8–16. https://doi.org/10.1016/j.jtemb.2017.04.009
Karottki DG, Spilak M, Frederiksen M, Gunnarsen L, Brauner EV, Kolarik B, Andersen ZJ, Sigsgaard T, Barregard L, Strandberg B, Sallsten G, Møller P, Loft S (2013) An indoor air filtration study in homes of elderly: cardiovascular and respiratory effects of exposure to particulate matter. Environ Health 12:116. https://doi.org/10.1186/1476-069X-12-116
Kendall M (2007) Fine airborne urban particles (PM2.5) sequester lung surfactant and amino acids from human lung lavage. Am J Physiol Lung Cell Mol Physiol 293:L1053–L1058. https://doi.org/10.1152/ajplung.00131.2007
Kryukov GV, Castellano S, Novoselov SV, Lobanov AV, Zehtab O, Guigo R, Gladyshev VN (2003) Characterization of mammalian selenoproteomes. Science 300:1439–1443. https://doi.org/10.1126/science.1083516
Leite HP, Nogueira PCK, Iglesias SBDO, de Oliveira SV, Sarni ROS (2015) Increased plasma selenium is associated with better outcomes in children with systemic inflammation. Nutrition 31:485–490. https://doi.org/10.1016/j.nut.2014.09.008
Li RJ, Kou XJ, Geng H, **e JF, Tian JJ, Cai ZW, Dong C (2015) Mitochondrial damage: an important mechanism of ambient PM2.5 exposure-induced acute heart injury in rats. J Hazard Mater 287:392–401. https://doi.org/10.1016/j.jhazmat.2015.02.006
Li W, Wilker EH, Dorans KS, Rice MB, Schwartz J, Coull BA, Koutrakis P, Gold DR, Keaney JF Jr, Lin H, Vasan RS, Benjamin EJ, Mittleman MA (2016a) Short-term exposure to air pollution and biomarkers of oxidative stress: the Framingham heart study. J Am Heart Assoc 5:e002742. https://doi.org/10.1161/JAHA.115.002742
Li X, Zhang Y, Yuan Y, Sun Y, Qin Y, Deng Z, Li H (2016b) Protective effects of selenium, vitamin E, and purple carrot anthocyanins on D-galactose-induced oxidative damage in blood, liver, heart and kidney rats. Biol Trace Elem Res 173:433–442. https://doi.org/10.1007/s12011-016-0681-8
Liu CP, Fu J, Xu FP, Wang XS, Li S (2015a) The role of heat shock proteins in oxidative stress damage induced by Se deficiency in chicken livers. Biometals 28:163–173. https://doi.org/10.1007/s10534-014-9812-x
Liu G, Yang G, Guan G, Zhang Y, Ren W, Yin J, Aguilar YM, Luo W, Fang J, Yu X, Li T, Yin Y (2015b) Effect of dietary selenium yeast supplementation on porcine circovirus type 2 (PCV2) infections in mice. PLoS One 10:e0115833. https://doi.org/10.1371/journal.pone.0115833
Liu J, Yang Y, Zeng X, Bo L, Jiang S, du X, **e Y, Jiang R, Zhao J, Song W (2017) Investigation of selenium pretreatment in the attenuation of lung injury in rats induced by fine particulate matters. Environ Sci Pollut Res 24:4008–4017. https://doi.org/10.1007/s11356-016-8173-0
Manzanares Castro W (2007) Selenium in critically ill patients with systemic inflammatory response. Nutr Hosp 22:295–306
McConnell R, Wu W, Berhane K, Liu F, Verma G, Peden D, Diaz-Sanchez D, Fruin S (2013) Inflammatory cytokine response to ambient particles varies due to field collection procedures. Am J Respir Cell Mol Biol 48:497–502. https://doi.org/10.1165/rcmb.2012-0320OC
Meo SA, Suraya F (2015) Effect of environmental air pollution on cardiovascular diseases. Eur Rev Med Pharmacol Sci 19:4890–4897
Merkord J, Gorl N, Lemke M, Berg A, Weber H, Ramer R, Hennighausen G (2017) Influence of daily oral prophylactic selenium treatment on the dibutyltin dichloride (DBTC)-induced pancreatitis in rats. EXCLI J 16:89–100. https://doi.org/10.17179/excli2016-466
Naziroglu M (2007) New molecular mechanisms on the activation of TRPM2 channels by oxidative stress and ADP-ribose. Neurochem Res 32:1990–2001. https://doi.org/10.1007/s11064-007-9386-x
Naziroglu M, Yildiz K, Tamturk B, Erturan I, Flores-Arce M (2012) Selenium and psoriasis. Biol Trace Elem Res 150:3–9. https://doi.org/10.1007/s12011-012-9479-5
Nemmar A, Holme JA, Rosas I, Schwarze PE, Alfaro-Moreno E (2013) Recent advances in particulate matter and nanoparticle toxicology: a review of the in vivo and in vitro studies. Biomed Res Int 2013:279371. https://doi.org/10.1155/2013/279371
Papp LV, Lu J, Holmgren A, Khanna KK (2007) From selenium to selenoproteins: synthesis, identity, and their role in human health. Antioxid Redox Signal 9:775–806. https://doi.org/10.1089/ars.2007.1528
Pei Y, Jiang R, Zou Y, Wang Y, Zhang S, Wang G, Zhao J, Song W (2016) Effects of fine particulate matter (PM2.5) on systemic oxidative stress and cardiac function in ApoE(−/−) mice. Int J Environ Res Public Health 13:484. https://doi.org/10.3390/ijerph13050484
Peter S et al (2015) Nutritional solutions to reduce risks of negative health impacts of air pollution. Nutrients 7:10398–10416. https://doi.org/10.3390/nu7125539
Pfeiler S, Winkels H, Kelm M, Gerdes N (2017) IL-1 family cytokines in cardiovascular disease. Cytokine. https://doi.org/10.1016/j.cyto.2017.11.009
Polichetti G, Cocco S, Spinali A, Trimarco V, Nunziata A (2009) Effects of particulate matter (PM10, PM2.5 and PM1) on the cardiovascular system. Toxicology 261:1–8. https://doi.org/10.1016/j.tox.2009.04.035
Porfire AS, Leucuta SE, Kiss B, Loghin F, Parvu AE (2014) Investigation into the role of Cu/Zn-SOD delivery system on its antioxidant and antiinflammatory activity in rat model of peritonitis. Pharmacol Rep 66:670–676. https://doi.org/10.1016/j.pharep.2014.03.011
Prasad S, Sung B, Aggarwal BB (2012) Age-associated chronic diseases require age-old medicine: role of chronic inflammation. Prev Med 54(Suppl):S29–S37. https://doi.org/10.1016/j.ypmed.2011.11.011
Rayman MP (2012) Selenium and human health. Lancet 379:1256–1268. https://doi.org/10.1016/S0140-6736(11)61452-9
Riediker M, Cascio WE, Griggs TR, Herbst MC, Bromberg PA, Neas L, Williams RW, Devlin RB (2004) Particulate matter exposure in cars is associated with cardiovascular effects in healthy young men. Am J Respir Crit Care Med 169:934–940. https://doi.org/10.1164/rccm.200310-1463OC
Roman M, Jitaru P, Barbante C (2014) Selenium biochemistry and its role for human health. Metallomics 6:25–54. https://doi.org/10.1039/c3mt00185g
Romieu I, Castro-Giner F, Kunzli N, Sunyer J (2008) Air pollution, oxidative stress and dietary supplementation: a review. Eur Respir J 31:179–197. https://doi.org/10.1183/09031936.00128106
Stupin A, Cosic A, Novak S, Vesel M, Jukic I, Popovic B, Karalic K, Loncaric Z, Drenjancevic I (2017) Reduced dietary selenium impairs vascular function by increasing oxidative stress in Sprague-Dawley rat aortas. Int J Environ Res Public Health 14. https://doi.org/10.3390/ijerph14060591
Sun Q, Hong X, Wold LE (2010) Cardiovascular effects of ambient particulate air pollution exposure. Circulation 121:2755–2765. https://doi.org/10.1161/CIRCULATIONAHA.109.893461
Tsai DH, Amyai N, Marques-Vidal P, Wang JL, Riediker M, Mooser V, Paccaud F, Waeber G, Vollenweider P, Bochud M (2012) Effects of particulate matter on inflammatory markers in the general adult population. Part Fibre Toxicol 9:24. https://doi.org/10.1186/1743-8977-9-24
Vermylen J, Nemmar A, Nemery B, Hoylaerts MF (2005) Ambient air pollution and acute myocardial infarction. J Thromb Haemost 3:1955–1961. https://doi.org/10.1111/j.1538-7836.2005.01471.x
Villarreal-Calderon R, Reed W, Palacios-Moreno J, Keefe S, Herritt L, Brooks D, Torres-Jardón R, Calderón-Garcidueñas L (2012) Urban air pollution produces up-regulation of myocardial inflammatory genes and dark chocolate provides cardioprotection. Exp Toxicol Pathol 64:297–306. https://doi.org/10.1016/j.etp.2010.09.002
Wang G, Jiang R, Zhao Z, Song W (2013) Effects of ozone and fine particulate matter (PM(2.5)) on rat system inflammation and cardiac function. Toxicol Lett 217:23–33. https://doi.org/10.1016/j.toxlet.2012.11.009
Wang GH, Zhao JZ, Jiang RF, Song WM (2015) Rat lung response to ozone and fine particulate matter (PM2.5) exposures. Environ Toxicol 30:343–356. https://doi.org/10.1002/tox.21912
Wegner CD, Gundel RH, Reilly P, Haynes N, Letts LG, Rothlein R (1990) Intercellular adhesion molecule-1 (ICAM-1) in the pathogenesis of asthma. Science 247:456–459
Yang T, Luo F, Shen Y, An J, Li X, Liu X, Ying B, Liao Z, Dong J, Guo L, Wang T, Xu D, Chen L, Wen F (2012) Quercetin attenuates airway inflammation and mucus production induced by cigarette smoke in rats. Int Immunopharmacol 13:73–81. https://doi.org/10.1016/j.intimp.2012.03.006
Zhao JZ, **e YQ, Qian XL, Jiang RF, Song WM (2010) Acute effects of fine particles on cardiovascular system: differences between the spontaneously hypertensive rats and wistar Kyoto rats. Toxicol Lett 193:50–60. https://doi.org/10.1016/j.toxlet.2009.12.002
Zhao J, Li L, Qian C, Jiang R, Song W (2012) Investigation on the characteristics and space-time distribution of fine particles in the atmosphere of residential area in Shanghai City. Wei Sheng Yan Jiu 41:35–39
Zhao J, Gao Z, Tian Z, **e Y, **n F, Jiang R, Kan H, Song W (2013) The biological effects of individual-level PM(2.5) exposure on systemic immunity and inflammatory response in traffic policemen. Occup Environ Med 70:426–431. https://doi.org/10.1136/oemed-2012-100864
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This study was supported by the National Key Research and Development Program of China (2016YFC0206600) and the National Natural Science Foundation of China (No. 91543119 and 81673125).
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Zeng, X., Liu, J., Du, X. et al. The protective effects of selenium supplementation on ambient PM2.5-induced cardiovascular injury in rats. Environ Sci Pollut Res 25, 22153–22162 (2018). https://doi.org/10.1007/s11356-018-2292-8
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DOI: https://doi.org/10.1007/s11356-018-2292-8