A Japanese cross-sectional multicentre study of biomarkers associated with cardiovascular disease in smokers and non-smokers

Frank Lüdicke, John Magnette, Gizelle Baker, Rolf Weitkunat, Frank Lüdicke, John Magnette, Gizelle Baker, Rolf Weitkunat

Abstract

We performed a cross-sectional, multicentre study in Japan to detect the differences in biomarkers of exposure and cardiovascular biomarkers between smokers and non-smokers. Several clinically relevant cardiovascular biomarkers differed significantly between smokers and non-smokers, including lipid metabolism (high-density lipoprotein cholesterol concentrations - lower in smokers), inflammation (fibrinogen and white blood cell count - both higher in smokers), oxidative stress (8-epi-prostaglandin F2α - higher in smokers) and platelet activation (11-dehydro-thromboxane B2 - higher in smokers) (p ≤ 0.0001). These results provide further evidence showing that cardiovascular biomarkers can discriminate smokers from non-smokers, and could be used to evaluate the risks associated with tobacco products.

Keywords: Biomarkers; Japan; cardiovascular disease; cigarettes; smoking.

References

    1. Allen SS, Hatsukami D, Gorsline J. Cholesterol changes in smoking cessation using the transdermal nicotine system. Transdermal Nicotine Study Group. Prev Med. 1994;23:190–6.
    1. Ambrose JA, Barua RS. The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol. 2004;43:1731–7.
    1. Arai H. Oxidative modification of lipoproteins. Subcell Biochem. 2014;77:103–14.
    1. Arima H, Kubo M, Yonemoto K, et al. High-sensitivity C-reactive protein and coronary heart disease in a general population of Japanese: the Hisayama study. Arterioscler Thromb Vasc Biol. 2008;28:1385–91.
    1. Asthana A, Johnson HM, Piper ME, et al. Effects of smoking intensity and cessation on inflammatory markers in a large cohort of active smokers. Am Heart J. 2010;160:458–63.
    1. Atikçan S, Yurdakul AS, Cimen F, et al. Expression of adhesion molecules in non-smokers, smokers and patients with chronic obstructive pulmonary disease. Turk Respir J. 2004;5:164–8.
    1. Bazzano LA, He J, Muntner P, et al. Relationship between cigarette smoking and novel risk factors for cardiovascular disease in the United States. Ann Intern Med. 2003;138:891–7.
    1. Bergmann S, Siekmeier R, Mix C, Jaross W. Even moderate cigarette smoking influences the pattern of circulating monocytes and the concentration of sICAM-1. Respir Physiol. 1998;114:269–75.
    1. Bermudez EA, Rifai N, Buring JE, et al. Relation between markers of systemic vascular inflammation and smoking in women. Am J Cardiol. 2002;89:1117–19.
    1. Blann A, Bignell A, McCollum C. von Willebrand factor, fibrinogen and other plasma proteins as determinants of plasma viscosity. Atherosclerosis. 1998;139:317–22.
    1. Blann AD, Steele C, McCollum CN. The influence of smoking on soluble adhesion molecules and endothelial cell markers. Thromb Res. 1997;85:433–8.
    1. Bonaterra GA, Zügel S, Kinscherf R. Novel systemic cardiovascular disease biomarkers. Curr Mol Med. 2010;10:180–205.
    1. Cacciapuoti F. Hyper-homocysteinemia: a novel risk factor or a powerful marker for cardiovascular diseases? Pathogenetic and therapeutical uncertainties. J Thromb Thrombolysis. 2011;32:82–8.
    1. Calapai G, Caputi AP, Mannucci C, et al. Cardiovascular biomarkers in groups of established smokers after a decade of smoking. Basic Clin Pharmacol Toxicol. 2009;104:322–8.
    1. Cherubini A, Ruggiero C, Polidori MC, Mecocci P. Potential markers of oxidative stress in stroke. Free Radic Biol Med. 2005;39:841–52.
    1. Davì G, Patrono C. Platelet activation and atherothrombosis. N Engl J Med. 2007;357:2482–94.
    1. Davis CE, Williams DH, Oganov RG, et al. Sex difference in high density lipoprotein cholesterol in six countries. Am J Epidemiol. 1996;143:1100–6.
    1. Davis SS, Roberts LJ., 2nd F2-isoprostanes as an indicator and risk factor for coronary heart disease. Free Radic Biol Med. 2011;50:559–66.
    1. Demerath E, Towne B, Blangero J, Siervogel RM. The relationship of soluble ICAM-1, VCAM-1, P-selectin and E-selectin to cardiovascular disease risk factors in healthy men and women. Ann Hum Biol. 2001;28:664–78.
    1. Dhalla NS, Golfman L, Takeda S, et al. Evidence for the role of oxidative stress in acute ischemic heart disease: a brief review. Can J Cardiol. 1999;15:587–93.
    1. Ehara S, Ueda M, Naruko T, et al. Elevated levels of oxidized low density lipoprotein show a positive relationship with the severity of acute coronary syndromes. Circulation. 2001;103:1955–60.
    1. Eliasson B, Hjalmarson A, Kruse E, et al. Effect of smoking reduction and cessation on cardiovascular risk factors. Nicotine Tob Res. 2001;3:249–55.
    1. Finch JM, Joseph J. Homocysteine, cardiovascular inflammation, and myocardial remodeling. Cardiovasc Hematol Disord Drug Targets. 2010;10:241–5.
    1. Food and Drug Administration (FDA) 2001.
    1. Forey BA, Fry JS, Lee PN, et al. The effect of quitting smoking on HDL-cholesterol – a review based on within-subject changes. Biomark Res. 2013;1:26. doi: 10.1186/2050-7771-1-26.
    1. Frost-Pineda K, Liang Q, Liu J, et al. Biomarkers of potential harm among adult smokers and nonsmokers in the total exposure study. Nicotine Tob Res. 2011;13:182–93.
    1. Gross MD, Bielinski SJ, Suarez-Lopez JR, et al. Circulating soluble intercellular adhesion molecule 1 and subclinical atherosclerosis: the Coronary Artery Risk Development in Young Adults Study. Clin Chem. 2012;58:411–20.
    1. Halvorsen B, Lund Sagen E, Ueland T, et al. Effect of smoking cessation on markers of inflammation and endothelial cell activation among individuals with high risk for cardiovascular disease. Scand J Clin Lab Invest. 2007;67:604–11.
    1. Hansen LK, Grimm RH, Jr, Neaton JD. The relationship of white blood cell count to other cardiovascular risk factors. Int J Epidemiol. 1990;19:881–8.
    1. Holvoet P, Harris TB, Tracy RP, et al. Association of high coronary heart disease risk status with circulating oxidized LDL in the well-functioning elderly: findings from the Health, Aging, and Body Composition study. Arterioscler Thromb Vasc Biol. 2003;23:1444–8.
    1. Holvoet P, Jenny NS, Schreiner PJ, et al. The relationship between oxidized LDL and other cardiovascular risk factors and subclinical CVD in different ethnic groups: the Multi-Ethnic Study of Atherosclerosis (MESA). Atherosclerosis. 2007;194:245–52.
    1. Howard G, Wagenknecht LE, Burke GL, et al. Cigarette smoking and progression of atherosclerosis: The Atherosclerosis Risk in Communities (ARIC) Study. JAMA. 1998;279:119–24.
    1. Hozawa A. Attributable fractions of risk factors for cardiovascular diseases. J Epidemiol. 2011;21:81–6.
    1. Hsu LA, Ko YL, Wu S, et al. Association of soluble intercellular adhesion molecule-1 with insulin resistance and metabolic syndrome in Taiwanese. Metabolism. 2009;58:983–8.
    1. Ishizaka N, Ishizaka Y, Toda E, et al. Relationship between smoking, white blood cell count and metabolic syndrome in Japanese women. Diabetes Res Clin Pract. 2007;78:72–6.
    1. Iso H, Folsom AR, Wu KK, et al. Hemostatic variables in Japanese and Caucasian men. Plasma fibrinogen, factor VIIc, factor VIIIc, and von Willebrand factor and their relations to cardiovascular disease risk factors. Am J Epidemiol. 1989;130:925–34.
    1. Iso H. Lifestyle and cardiovascular disease in Japan. J Atheroscler Thromb. 2011;18:83–8.
    1. Kannel WB. Overview of hemostatic factors involved in atherosclerotic cardiovascular disease. Lipids. 2005;40:1215–20.
    1. Kaperonis EA, Liapis CD, Kakisis JD, et al. Inflammation and atherosclerosis. Eur J Vasc Endovasc Surg. 2006;31:386–93.
    1. Kaptoge S, White IR, Thompson SG, et al. Associations of plasma fibrinogen levels with established cardiovascular disease risk factors, inflammatory markers, and other characteristics: individual participant meta-analysis of 154,211 adults in 31 prospective studies: the fibrinogen studies collaboration. Am J Epidemiol. 2007;166:867–79.
    1. Koundouros E, Odell E, Coward P, et al. Soluble adhesion molecules in serum of smokers and non-smokers, with and without periodontitis. J Periodont Res. 1996;31:596–9.
    1. Lain KY, Luppi P, McGonigal S, et al. Intracellular adhesion molecule concentrations in women who smoke during pregnancy. Obstet Gynecol. 2006;107:588–94.
    1. Lavi S, Prasad A, Yang EH, et al. Smoking is associated with epicardial coronary endothelial dysfunction and elevated white blood cell count in patients with chest pain and early coronary artery disease. Circulation. 2007;115:2621–7.
    1. Lee PN, Forey BA, Fry JS, et al. 2014
    1. Liu J, Liang Q, Frost-Pineda K, et al. Relationship between biomarkers of cigarette smoke exposure and biomarkers of inflammation, oxidative stress, and platelet activation in adult cigarette smokers. Cancer Epidemiol Biomarkers Prev. 2011;20:1760–9.
    1. Lowe FJ, Gregg EO, McEwan M. Evaluation of biomarkers of exposure and potential harm in smokers, former smokers and never-smokers. Clin Chem Lab Med. 2009;47:311–20.
    1. Luo GP, Ni B, Yang X, Wu YZ. von Willebrand factor: more than a regulator of hemostasis and thrombosis. Acta Haematol. 2012;128:158–69.
    1. Martí-Carvajal AJ, Solà I, Lathyris D. Homocysteine-lowering interventions for preventing cardiovascular events. Cochrane Database Syst Rev. 2015;1:CD006612.
    1. Mazzone A, Cusa C, Mazzucchelli I, et al. Cigarette smoking and hypertension influence nitric oxide release and plasma levels of adhesion molecules. Clin Chem Lab Med. 2001;39:822–6.
    1. Micheel CM, Ball JR. 2010
    1. Miller EA, Pankow JS, Millikan RC, et al. Glutathione-S-transferase genotypes, smoking, and their association with markers of inflammation, hemostasis, and endothelial function: the atherosclerosis risk in communities (ARIC) study. Atherosclerosis. 2003;171:265–72.
    1. Miwa K, Fujita M. Sex difference in effects of smoking on serum vitamin E concentrations in a young population. J Cardiol. 2006;48:201–7.
    1. Moffatt RJ, Biggerstaff KD, Stamford BA. Effects of the transdermal nicotine patch on normalization of HDL-C and its subfractions. Prev Med. 2000;31:148–52.
    1. Morrow JD. Quantification of isoprostanes as indices of oxidant stress and the risk of atherosclerosis in humans. Arterioscler Thromb Vasc Biol. 2005;25:279–86.
    1. Morrow JD, Frei B, Longmire AW, et al. Increase in circulating products of lipid peroxidation (F2-isoprostanes) in smokers. Smoking as a cause of oxidative damage. N Engl J Med. 1995;332:1198–203.
    1. Muralikrishna Adibhatla R, Hatcher JF. Phospholipase A2, reactive oxygen species, and lipid peroxidation in cerebral ischemia. Free Radic Biol Med. 2006;40:376–87.
    1. Nam TG. Lipid peroxidation and its toxicological implications. Toxicol Res. 2011;27:1–6.
    1. OECD 2013
    1. Oguogho A, Lupattelli G, Palumbo B, Sinzinger H. Isoprostanes quickly normalize after quitting cigarette smoking in healthy adults. Vasa. 2000;29:103–5.
    1. Ohsawa M, Okayama A, Nakamura M, et al. CRP levels are elevated in smokers but unrelated to the number of cigarettes and are decreased by long-term smoking cessation in male smokers. Prev Med. 2005;41:651–6.
    1. Palmer RM, Stapleton JA, Sutherland G, et al. Effect of nicotine replacement and quitting smoking on circulating adhesion molecule profiles (sICAM-1, sCD44v5, sCD44v6). Eur J Clin Invest. 2002;32:852–7.
    1. Pearson TA, Mensah GA, Alexander RW, et al. Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation. 2003;107:499–511.
    1. Pilz H, Oguogho A, Chehne F, et al. Quitting cigarette smoking results in a fast improvement of in vivo oxidation injury (determined via plasma, serum and urinary isoprostane). Thromb Res. 2000;99:209–21.
    1. Pizzimenti S, Ciamporcero E, Daga M, et al. Interaction of aldehydes derived from lipid peroxidation and membrane proteins. Front Physiol. 2013;4:242. doi: 10.3389/fphys.2013.00242.
    1. Rångemark C, Ciabattoni G, Wennmalm A. Excretion of thromboxane metabolites in healthy women after cessation of smoking. Arterioscler Thromb. 1993;13:777–82.
    1. Reilly M, Delanty N, Lawson JA, FitzGerald GA. Modulation of oxidant stress in vivo in chronic cigarette smokers. Circulation. 1996;94:19–25.
    1. Richard F, Marécaux N, Dallongeville J, et al. Effect of smoking cessation on lipoprotein A-I and lipoprotein A-I:A-II levels. Metabolism. 1997;46:711–15.
    1. Rifai N, Joubran R, Yu H, et al. Inflammatory markers in men with angiographically documented coronary heart disease. Clin Chem. 1999;45:1967–73.
    1. Rohde LE, Hennekens CH, Ridker PM. Cross-sectional study of soluble intercellular adhesion molecule-1 and cardiovascular risk factors in apparently healthy men. Arterioscler Thromb Vasc Biol. 1999;19:1595–9.
    1. Ross R. Atherosclerosis – an inflammatory disease. N Engl J Med. 1999;340:115–26.
    1. Saareks V, Ylitalo P, Alanko J, et al. Effects of smoking cessation and nicotine substitution on systemic eicosanoid production in man. Naunyn Schmiedebergs Arch Pharmacol. 2001;363:556–61.
    1. Scott DA, Poston RN, Wilson RF, et al. The influence of vitamin C on systemic markers of endothelial and inflammatory cell activation in smokers and non-smokers. Inflamm Res. 2005;54:138–44.
    1. Scott DA, Stapleton JA, Wilson RF, et al. Dramatic decline in circulating intercellular adhesion molecule-1 concentration on quitting tobacco smoking. Blood Cells Mol Dis. 2000;26:255–8.
    1. Seet RC, Loke WM, Khoo CM, et al. Acute effects of cigarette smoking on insulin resistance and arterial stiffness in young adults. Atherosclerosis. 2012;224:195–200.
    1. Siems W, Quast S, Carluccio F, et al. Oxidative stress in chronic renal failure as a cardiovascular risk factor. Clin Nephrol. 2002;58:S12–19.
    1. Takeuchi N, Kawamura T, Kanai A, et al. The effect of cigarette smoking on soluble adhesion molecules in middle-aged patients with type 2 diabetes mellitus. Diabet Med. 2002;19:57–64.
    1. Thun MJ, Carter BD, Feskanich D, et al. 50-year trends in smoking-related mortality in the United States. N Engl J Med. 2013;368:351–64.
    1. Uchida K. Role of reactive aldehyde in cardiovascular diseases. Free Radic Biol Med. 2000;28:1685–96.
    1. Ueshima H, Sekikawa A, Miura K, et al. Cardiovascular disease and risk factors in Asia: a selected review. Circulation. 2008;118:2702–9.
    1. Unverdorben M, von Holt K, Winkelmann BR. Smoking and atherosclerotic cardiovascular disease: part II: role of cigarette smoking in cardiovascular disease development. Biomark Med. 2009;3:617–53.
    1. US Department of Health and Human Services . A report of The Surgeon General: how tobacco smoke causes disease: the biology and behavioral basis for smoking attributable disease. Rockville (MD): Department of Health and Human Services, Public Health Services, Centers for Disease Control, Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; 2010.
    1. van Tits LJ, de Waart F, Hak-Lemmers HL, et al. Effects of alpha-tocopherol on superoxide production and plasma intercellular adhesion molecule-1 and antibodies to oxidized LDL in chronic smokers. Free Radic Biol Med. 2001;30:1122–9.
    1. Vlahos R, Bozinovski S. Glutathione peroxidase-1 as a novel therapeutic target for COPD. Redox Rep. 2013;18:142–9.
    1. Voulgaridou GP, Anestopoulos I, Franco R, et al. DNA damage induced by endogenous aldehydes: current state of knowledge. Mutat Res. 2011;711:13–27.
    1. Wakelkamp IM, Gerding MN, van der Meer JW, et al. Smoking and disease severity are independent determinants of serum adhesion molecule levels in Graves’ ophthalmopathy. Clin Exp Immunol. 2002;127:316–20.
    1. Wannamethee SG, Lowe GD, Shaper AG, et al. Associations between cigarette smoking, pipe/cigar smoking, and smoking cessation, and haemostatic and inflammatory markers for cardiovascular disease. Eur Heart J. 2005;26:1765–73.
    1. Winterbourn CC. The biological chemistry of hydrogen peroxide. Methods Enzymol. 2013;528:3–25.
    1. Woodward M, Rumley A, Tunstall-Pedoe H, Lowe GD. Associations of blood rheology and interleukin-6 with cardiovascular risk factors and prevalent cardiovascular disease. Br J Haematol. 1999;104:246–57.
    1. World Health Organisation . 2009.
    1. World Health Organisation . 2013.
    1. Yasue H, Hirai N, Mizuno Y, et al. Low-grade inflammation, thrombogenicity, and atherogenic lipid profile in cigarette smokers. Circ J. 2006;70:8–13.
    1. Yerman T, Gan WQ, Sin DD. The influence of gender on the effects of aspirin in preventing myocardial infarction. BMC Med. 2007;5:29.

Source: PubMed

3
Se inscrever