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Published in: Cardiovascular Drugs and Therapy 4/2015

01-08-2015 | ORIGINAL ARTICLE

Gender-Related Differences in Atherosclerosis

Authors: Pankaj Mathur, Bohuslav Ostadal, Francesco Romeo, Jawahar L. Mehta

Published in: Cardiovascular Drugs and Therapy | Issue 4/2015

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Abstract

Atherosclerotic cardiovascular disease (CVD) is the leading cause of morbidity and mortality globally. Considerable research has been done over the last several decades to understand the pathophysiology of atherosclerosis. It is widely believed that estrogen is responsible for the protection of women from CVD in the premenopausal age group. However, hormone replacement therapy has failed to decrease CVD events in clinical studies which points to the complexity of the relationship between vascular biology and estrogen hormones. Interestingly, preponderance of vascular and connective tissue disorders in women also points to an inherent role of hormones and tissue factors in maintenance of vascular endothelial function. The differential effect of GPER, lipoprotein A, TLRs, leucocyte-platelet aggregate markers in men and women also suggests inherent gender-related differences in the pathophysiology of atherosclerosis. A better understanding of the pathophysiology is likely to open ways to improve evidence-based treatment of CVD in women.
Literature
1.
go back to reference Go AS, Mozaffarian D, Roger VL, Benjamin EJ, et al. American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Executive summary: heart disease and stroke statistics–2014 update: a report from the American Heart Association. Circulation. 2014;129(3):399–410.CrossRefPubMed Go AS, Mozaffarian D, Roger VL, Benjamin EJ, et al. American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Executive summary: heart disease and stroke statistics–2014 update: a report from the American Heart Association. Circulation. 2014;129(3):399–410.CrossRefPubMed
4.
go back to reference Steinberg D. Research related to underlying mechanisms in atherosclerosis. Circulation. 1979;60(7):1559–65.CrossRefPubMed Steinberg D. Research related to underlying mechanisms in atherosclerosis. Circulation. 1979;60(7):1559–65.CrossRefPubMed
5.
go back to reference Parthasarathy S, Quinn MT, Steinberg D. Is oxidized low density lipoprotein involved in the recruitment and retention of monocyte/macrophages in the artery wall during the initiation of atherosclerosis? Basic Life Sci. 1988;49:375–80.PubMed Parthasarathy S, Quinn MT, Steinberg D. Is oxidized low density lipoprotein involved in the recruitment and retention of monocyte/macrophages in the artery wall during the initiation of atherosclerosis? Basic Life Sci. 1988;49:375–80.PubMed
6.
go back to reference Davignon J, Ganz P. Role of endothelial dysfunction in atherosclerosis. Circulation. 2004;109(23 Suppl 1):III27–32.PubMed Davignon J, Ganz P. Role of endothelial dysfunction in atherosclerosis. Circulation. 2004;109(23 Suppl 1):III27–32.PubMed
7.
go back to reference Duvall WL. Cardiovascular disease in women. Mt Sinay J Med. 2003;70:293–305. Duvall WL. Cardiovascular disease in women. Mt Sinay J Med. 2003;70:293–305.
8.
go back to reference Fejfar Z. Prevention against ischaemic heart disease: a critical review. In: Oliver MF, editor. Modern trends in cardiology – 3. London: Butterworths; 1975. p. 465–95. Fejfar Z. Prevention against ischaemic heart disease: a critical review. In: Oliver MF, editor. Modern trends in cardiology – 3. London: Butterworths; 1975. p. 465–95.
9.
go back to reference Ostadal B, Ostadal P. Sex-based differences in cardiac ischaemic injury and protection: therapeutic implications. BJP. 2014;171:541–54.CrossRef Ostadal B, Ostadal P. Sex-based differences in cardiac ischaemic injury and protection: therapeutic implications. BJP. 2014;171:541–54.CrossRef
10.
go back to reference Ostadal B, Netuka I, Maly J, Besik J, Ostadalova I. Gender differences in cardiac ischemic injury and protection-experimental aspects. Exp Biol Med (Maywood). 2009;234:1011–9.CrossRef Ostadal B, Netuka I, Maly J, Besik J, Ostadalova I. Gender differences in cardiac ischemic injury and protection-experimental aspects. Exp Biol Med (Maywood). 2009;234:1011–9.CrossRef
11.
go back to reference Davis KB, Chaitman B, Ryan T, Bittner V, Kennedy JW. Comparison of 15-year survival for men and women after initial medical or surgical treatment for coronary artery disease: a CASS Registry study. J Am Coll Cardiol. 1995;25:1000–9.CrossRefPubMed Davis KB, Chaitman B, Ryan T, Bittner V, Kennedy JW. Comparison of 15-year survival for men and women after initial medical or surgical treatment for coronary artery disease: a CASS Registry study. J Am Coll Cardiol. 1995;25:1000–9.CrossRefPubMed
12.
go back to reference Njolstad I, Arnesen E, Lund-Larsen PD. Smoking, serum lipids, blood pressure, and sex differences in myocardial infarction. A 12-year follow-up of the Finnmark study. Circulation. 1996;93:450–6.CrossRefPubMed Njolstad I, Arnesen E, Lund-Larsen PD. Smoking, serum lipids, blood pressure, and sex differences in myocardial infarction. A 12-year follow-up of the Finnmark study. Circulation. 1996;93:450–6.CrossRefPubMed
13.
go back to reference Stokes J, Kannel WB, Wolf PA, Cupples LA, D’Agostino RB. The relative importance of selected risk factors for various manifestations of cardiovascular disease among men and women from 35 to 64 years old: 30 years of follow-up in the Framingham Study. Circulation. 1987;75:V65–73.PubMed Stokes J, Kannel WB, Wolf PA, Cupples LA, D’Agostino RB. The relative importance of selected risk factors for various manifestations of cardiovascular disease among men and women from 35 to 64 years old: 30 years of follow-up in the Framingham Study. Circulation. 1987;75:V65–73.PubMed
14.
go back to reference Kardys I, Vliegenthart R, Oudkerk M, Hofman A, Witteman JC. The female advantage in cardiovascular disease: do vascular beds contribute equally? Am J Epidemiol. 2007;166(4):403–12.CrossRefPubMed Kardys I, Vliegenthart R, Oudkerk M, Hofman A, Witteman JC. The female advantage in cardiovascular disease: do vascular beds contribute equally? Am J Epidemiol. 2007;166(4):403–12.CrossRefPubMed
15.
go back to reference Farb A, Burke AP, Tang AL, et al. Coronary plaque erosion without rupture into a lipid core. A frequent cause of coronary thrombosis in sudden coronary death. Circulation. 1996;93:1354–63.CrossRefPubMed Farb A, Burke AP, Tang AL, et al. Coronary plaque erosion without rupture into a lipid core. A frequent cause of coronary thrombosis in sudden coronary death. Circulation. 1996;93:1354–63.CrossRefPubMed
16.
go back to reference Burke AP, Farb A, Malcom GT, Liang Y, Smialek J, Virmani R. Effect of risk factors on the mechanism of acute thrombosis and sudden coronary death in women. Circulation. 1998;97:2110–6.CrossRefPubMed Burke AP, Farb A, Malcom GT, Liang Y, Smialek J, Virmani R. Effect of risk factors on the mechanism of acute thrombosis and sudden coronary death in women. Circulation. 1998;97:2110–6.CrossRefPubMed
17.
go back to reference Yahagi K, Davis HR, Arbustini E, Virmani R. Sex differences in coronary artery disease: pathological observations. Atherosclerosis. 2015;239(1):260–7.CrossRefPubMed Yahagi K, Davis HR, Arbustini E, Virmani R. Sex differences in coronary artery disease: pathological observations. Atherosclerosis. 2015;239(1):260–7.CrossRefPubMed
18.
go back to reference Ferrante G, Nakano M, Prati F, et al. High levels of systemic myeloperoxidase are associated with coronary plaque erosion in patients with acute coronary syndromes: a clinicopathological study. Circulation. 2010;122:2505–13.CrossRefPubMed Ferrante G, Nakano M, Prati F, et al. High levels of systemic myeloperoxidase are associated with coronary plaque erosion in patients with acute coronary syndromes: a clinicopathological study. Circulation. 2010;122:2505–13.CrossRefPubMed
19.
go back to reference Kolodgie FD, Burke AP, Farb A, et al. Differential accumulation of proteoglycans and hyaluronan in culprit lesions: insights into plaque erosion. Arterioscler Thromb Vasc Biol. 2002;22:1642–8.CrossRefPubMed Kolodgie FD, Burke AP, Farb A, et al. Differential accumulation of proteoglycans and hyaluronan in culprit lesions: insights into plaque erosion. Arterioscler Thromb Vasc Biol. 2002;22:1642–8.CrossRefPubMed
20.
go back to reference Johnson BD, Shaw LJ, Buchthal SD, Bairey Merz CN, Kim HW, Scott KN, et al. Prognosis in women with myocardial ischemia in the absence of obstructive coronary disease: results from the National Institutes of Health-National Heart, Lung, and Blood Institute-Sponsored Women’s Ischemia Syndrome Evaluation (WISE). Circulation. 2004;109(24):2993–9.CrossRefPubMed Johnson BD, Shaw LJ, Buchthal SD, Bairey Merz CN, Kim HW, Scott KN, et al. Prognosis in women with myocardial ischemia in the absence of obstructive coronary disease: results from the National Institutes of Health-National Heart, Lung, and Blood Institute-Sponsored Women’s Ischemia Syndrome Evaluation (WISE). Circulation. 2004;109(24):2993–9.CrossRefPubMed
21.
go back to reference Johnson BD, Shaw LJ, Pepine CJ, Reis SE, Kelsey SF, Sopko G, et al. Persistent chest pain predicts cardiovascular events in women without obstructive coronary artery disease: results from the NIH-NHLBI-sponsored Women’s Ischaemia Syndrome Evaluation (WISE) study. Eur Heart J. 2006;27(12):1408–15.CrossRefPubMed Johnson BD, Shaw LJ, Pepine CJ, Reis SE, Kelsey SF, Sopko G, et al. Persistent chest pain predicts cardiovascular events in women without obstructive coronary artery disease: results from the NIH-NHLBI-sponsored Women’s Ischaemia Syndrome Evaluation (WISE) study. Eur Heart J. 2006;27(12):1408–15.CrossRefPubMed
22.
go back to reference Buchthal SD, den Hollander JA, Merz CN, Rogers WJ, Pepine CJ, Reichek N, et al. Abnormal myocardial phosphorus-31 nuclear magnetic resonance spectroscopy in women with chest pain but normal coronary angiograms. N Engl J Med. 2000;342(12):829–35.CrossRefPubMed Buchthal SD, den Hollander JA, Merz CN, Rogers WJ, Pepine CJ, Reichek N, et al. Abnormal myocardial phosphorus-31 nuclear magnetic resonance spectroscopy in women with chest pain but normal coronary angiograms. N Engl J Med. 2000;342(12):829–35.CrossRefPubMed
23.
go back to reference Han SH, Bae JH, Holmes Jr DR, Lennon RJ, Eeckhout E, Barsness GW, et al. Sex differences in atheroma burden and endothelial function in patients with early coronary atherosclerosis. Eur Heart J. 2008;29(11):1359–69.CrossRefPubMed Han SH, Bae JH, Holmes Jr DR, Lennon RJ, Eeckhout E, Barsness GW, et al. Sex differences in atheroma burden and endothelial function in patients with early coronary atherosclerosis. Eur Heart J. 2008;29(11):1359–69.CrossRefPubMed
24.
go back to reference Kern MJ, Bach RG, Mechem CJ, Caracciolo EA, Aguirre FV, Miller LW, et al. Variations in normal coronary vasodilatory reserve stratified by artery, gender, heart transplantation and coronary artery disease. J Am Coll Cardiol. 1996;28:1154–60.CrossRefPubMed Kern MJ, Bach RG, Mechem CJ, Caracciolo EA, Aguirre FV, Miller LW, et al. Variations in normal coronary vasodilatory reserve stratified by artery, gender, heart transplantation and coronary artery disease. J Am Coll Cardiol. 1996;28:1154–60.CrossRefPubMed
25.
go back to reference Reynolds HR, Srichai MB, Iqbal SN, Slater JN, Mancini GB, Feit F, et al. Mechanisms of myocardial infarction in women without angiographically obstructive coronary artery disease. Circulation. 2011;124(13):1414–25.PubMedCentralCrossRefPubMed Reynolds HR, Srichai MB, Iqbal SN, Slater JN, Mancini GB, Feit F, et al. Mechanisms of myocardial infarction in women without angiographically obstructive coronary artery disease. Circulation. 2011;124(13):1414–25.PubMedCentralCrossRefPubMed
26.
go back to reference Iqbal SN, Feit F, Mancini GB, Wood D, Patel R, Pena-Sing I, et al. Characteristics of plaque disruption by intravascular ultrasound in women presenting with myocardial infarction without obstructive coronary artery disease. Am Heart J. 2014;167(5):715–22.CrossRefPubMed Iqbal SN, Feit F, Mancini GB, Wood D, Patel R, Pena-Sing I, et al. Characteristics of plaque disruption by intravascular ultrasound in women presenting with myocardial infarction without obstructive coronary artery disease. Am Heart J. 2014;167(5):715–22.CrossRefPubMed
27.
go back to reference Sangiorgi G, Roversi S, Biondi Zoccai G, Modena MG, Servadei F, Ippoliti A, et al. Sex-related differences in carotid plaque features and inflammation. J Vasc Surg. 2013;57(2):338–44.CrossRefPubMed Sangiorgi G, Roversi S, Biondi Zoccai G, Modena MG, Servadei F, Ippoliti A, et al. Sex-related differences in carotid plaque features and inflammation. J Vasc Surg. 2013;57(2):338–44.CrossRefPubMed
28.
go back to reference Gaubitz M. Epidemiology of connective tissue disorders. Rheumatology (Oxford). 2006;45 Suppl 3:iii3–4. Gaubitz M. Epidemiology of connective tissue disorders. Rheumatology (Oxford). 2006;45 Suppl 3:iii3–4.
29.
go back to reference Sun H, Mohri M, Shimokawa H, Usui M, Urakami L, Takeshita A. Coronary microvascular spasm causes myocardial ischemia in patients with vasospastic angina. J Am Coll Cardiol. 2002;39(5):847–51.CrossRefPubMed Sun H, Mohri M, Shimokawa H, Usui M, Urakami L, Takeshita A. Coronary microvascular spasm causes myocardial ischemia in patients with vasospastic angina. J Am Coll Cardiol. 2002;39(5):847–51.CrossRefPubMed
30.
go back to reference Mohri M, Koyanagi M, Egashira K, Tagawa H, Ichiki T, Shimokawa H, et al. Angina pectoris caused by coronary microvascular spasm. Lancet. 1998;351(9110):1165–9.CrossRefPubMed Mohri M, Koyanagi M, Egashira K, Tagawa H, Ichiki T, Shimokawa H, et al. Angina pectoris caused by coronary microvascular spasm. Lancet. 1998;351(9110):1165–9.CrossRefPubMed
31.
go back to reference Reis SE, Holubkov R, Conrad Smith AJ, Kelsey SF, Sharaf BL, Reichek N, et al. Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study. Am Heart J. 2001;141(5):735–41.CrossRefPubMed Reis SE, Holubkov R, Conrad Smith AJ, Kelsey SF, Sharaf BL, Reichek N, et al. Coronary microvascular dysfunction is highly prevalent in women with chest pain in the absence of coronary artery disease: results from the NHLBI WISE study. Am Heart J. 2001;141(5):735–41.CrossRefPubMed
32.
go back to reference Harder DR, Coulson PB. Estrogen receptors and effects of estrogen on membrane electrical properties of coronary vascular smooth muscle. J Cell Physiol. 1979;100:375–82.CrossRefPubMed Harder DR, Coulson PB. Estrogen receptors and effects of estrogen on membrane electrical properties of coronary vascular smooth muscle. J Cell Physiol. 1979;100:375–82.CrossRefPubMed
33.
go back to reference Sudhir K, Chou TM, Mullen WL, Hausmann D, Collins P, Yock PG, et al. Mechanisms of estrogen-induced vasodilation: in vivo studies in canine coronary conductance and resistance arteries. J Am Coll Cardiol. 1995;26(3):807–14.CrossRefPubMed Sudhir K, Chou TM, Mullen WL, Hausmann D, Collins P, Yock PG, et al. Mechanisms of estrogen-induced vasodilation: in vivo studies in canine coronary conductance and resistance arteries. J Am Coll Cardiol. 1995;26(3):807–14.CrossRefPubMed
34.
go back to reference Wilson TA, Nicolosi RJ, Lawton CW, Babiak J. Gender differences in response to a hypercholesterolemic diet in hamsters: effects on plasma lipoprotein cholesterol concentrations and early aortic atherosclerosis. Atherosclerosis. 1999;146(1):83–91.CrossRefPubMed Wilson TA, Nicolosi RJ, Lawton CW, Babiak J. Gender differences in response to a hypercholesterolemic diet in hamsters: effects on plasma lipoprotein cholesterol concentrations and early aortic atherosclerosis. Atherosclerosis. 1999;146(1):83–91.CrossRefPubMed
35.
go back to reference Hayashi T, Fukuto JM, Ignarro LJ, Chaudhuri G. Gender differences in atherosclerosis: possible role of nitric oxide. J Cardiovasc Pharmacol. 1995;26(5):792–802.CrossRefPubMed Hayashi T, Fukuto JM, Ignarro LJ, Chaudhuri G. Gender differences in atherosclerosis: possible role of nitric oxide. J Cardiovasc Pharmacol. 1995;26(5):792–802.CrossRefPubMed
36.
go back to reference Huang A, Kaley G. Gender-specific regulation of cardiovascular function: estrogen as key player. Microcirculation. 2004;11(1):9–38.CrossRefPubMed Huang A, Kaley G. Gender-specific regulation of cardiovascular function: estrogen as key player. Microcirculation. 2004;11(1):9–38.CrossRefPubMed
37.
go back to reference Wagner AH, Schroeter MR, Hecker M. 17beta-e stradiol inhibition of NADPH oxidase expression in human endothelial cells. FASEB J. 2001;15(12):2121–30.CrossRefPubMed Wagner AH, Schroeter MR, Hecker M. 17beta-e stradiol inhibition of NADPH oxidase expression in human endothelial cells. FASEB J. 2001;15(12):2121–30.CrossRefPubMed
38.
go back to reference Haas E, Bhattacharya I, Brailoiu E, Damjanović M, Brailoiu GC, Gao X, et al. Regulatory role of G protein-coupled estrogen receptor for vascular function and obesity. Circ Res. 2009;104(3):288–91.PubMedCentralCrossRefPubMed Haas E, Bhattacharya I, Brailoiu E, Damjanović M, Brailoiu GC, Gao X, et al. Regulatory role of G protein-coupled estrogen receptor for vascular function and obesity. Circ Res. 2009;104(3):288–91.PubMedCentralCrossRefPubMed
39.
go back to reference Meyer MR, Fredette NC, Howard TA, Hu C, Ramesh C, Daniel C, et al. G protein-coupled estrogen receptor protects from atherosclerosis. Sci Rep. 2014;4:7564.PubMedCentralCrossRefPubMed Meyer MR, Fredette NC, Howard TA, Hu C, Ramesh C, Daniel C, et al. G protein-coupled estrogen receptor protects from atherosclerosis. Sci Rep. 2014;4:7564.PubMedCentralCrossRefPubMed
40.
go back to reference Huang A, Koller A. Endothelin and prostaglandin H2 enhance arteriolar myogenic tone in hypertension. Hypertension. 1997;30:1210–5.CrossRefPubMed Huang A, Koller A. Endothelin and prostaglandin H2 enhance arteriolar myogenic tone in hypertension. Hypertension. 1997;30:1210–5.CrossRefPubMed
41.
go back to reference Huang A, Sun D, Koller A, Kaley G. Gender difference in myogenic tone of rat arterioles is due to estrogen-induced, enhanced release of NO. Am J Physiol. 1997;272:H1804–9.PubMed Huang A, Sun D, Koller A, Kaley G. Gender difference in myogenic tone of rat arterioles is due to estrogen-induced, enhanced release of NO. Am J Physiol. 1997;272:H1804–9.PubMed
42.
43.
go back to reference Ng MK, Quinn CM, McCrohon JA, Nakhla S, Jessup W, Handelsman DJ, et al. Androgens up-regulate atherosclerosis-related genes in macrophages from males but not females: molecular insights into gender differences in atherosclerosis. J Am Coll Cardiol. 2003;42(7):1306–13.CrossRefPubMed Ng MK, Quinn CM, McCrohon JA, Nakhla S, Jessup W, Handelsman DJ, et al. Androgens up-regulate atherosclerosis-related genes in macrophages from males but not females: molecular insights into gender differences in atherosclerosis. J Am Coll Cardiol. 2003;42(7):1306–13.CrossRefPubMed
44.
go back to reference McCrohon JA, Death AK, Nakhla N, et al. Androgen receptor expression is greater in macrophages from male than from female donors. A sex difference with implications for atherogenesis. Circulation. 2000;101(3):224–6.CrossRefPubMed McCrohon JA, Death AK, Nakhla N, et al. Androgen receptor expression is greater in macrophages from male than from female donors. A sex difference with implications for atherogenesis. Circulation. 2000;101(3):224–6.CrossRefPubMed
45.
go back to reference Ling S, Dai A, Williams MR, Myles K, et al. Testosterone (T) enhances apoptosis-related damage in human vascular endothelial cells. Endocrinology. 2002;143(3):1119–25.CrossRefPubMed Ling S, Dai A, Williams MR, Myles K, et al. Testosterone (T) enhances apoptosis-related damage in human vascular endothelial cells. Endocrinology. 2002;143(3):1119–25.CrossRefPubMed
46.
go back to reference Hulley S, Grandy D, Bush T, Furberk C, Herrington D, Riggs B, et al. Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. JAMA. 1998;280:605–12.CrossRefPubMed Hulley S, Grandy D, Bush T, Furberk C, Herrington D, Riggs B, et al. Randomized trial of estrogen plus progestin for secondary prevention of coronary heart disease in postmenopausal women. JAMA. 1998;280:605–12.CrossRefPubMed
47.
go back to reference Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg CH, Hutchison F, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women’s Health Initiative randomized control trial. JAMA. 2002;288:321–33.CrossRefPubMed Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg CH, Hutchison F, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women’s Health Initiative randomized control trial. JAMA. 2002;288:321–33.CrossRefPubMed
48.
go back to reference Nuedling S, Karas RH, Mendelsohn ME, Katzenellenbogen JA, Katzenellenbogen BS, Meyer R, et al. Activation of estrogen receptor beta is a prerequisite for estrogen-dependent upregulation of nitric oxide synthases in neonatal rat cardiac myocytes. FEBS Lett. 2001;502(3):103–8.CrossRefPubMed Nuedling S, Karas RH, Mendelsohn ME, Katzenellenbogen JA, Katzenellenbogen BS, Meyer R, et al. Activation of estrogen receptor beta is a prerequisite for estrogen-dependent upregulation of nitric oxide synthases in neonatal rat cardiac myocytes. FEBS Lett. 2001;502(3):103–8.CrossRefPubMed
49.
go back to reference Ghanam K, Lavagna C, Burgaud JL, Javellaud J, Ea-Kim L, Oudart N. Involvement of cyclooxygenase 2 in the protective effect of 17beta-estradiol on hypercholesterolemic rabbit aorta. Biochem Biophys Res Commun. 2000;275:696–703.CrossRefPubMed Ghanam K, Lavagna C, Burgaud JL, Javellaud J, Ea-Kim L, Oudart N. Involvement of cyclooxygenase 2 in the protective effect of 17beta-estradiol on hypercholesterolemic rabbit aorta. Biochem Biophys Res Commun. 2000;275:696–703.CrossRefPubMed
50.
go back to reference Santos RL, Marin EB, Goncalves WL, Bissoli NS, Abreu GR, Moyses MR. Sex differences in the coronary vasodilatation induced by 17 β-oestradiol in the isolated perfused heart from spontaneously hypertensive rats. Acta Physiol (Oxf). 2010;200:203–10.CrossRef Santos RL, Marin EB, Goncalves WL, Bissoli NS, Abreu GR, Moyses MR. Sex differences in the coronary vasodilatation induced by 17 β-oestradiol in the isolated perfused heart from spontaneously hypertensive rats. Acta Physiol (Oxf). 2010;200:203–10.CrossRef
51.
go back to reference Murphy E, Steenbergen C. Gender-based differences in mechanisms of protection in myocardial ischemia-reperfusion injury. Cardiovasc Res. 2007;75:478–86.CrossRefPubMed Murphy E, Steenbergen C. Gender-based differences in mechanisms of protection in myocardial ischemia-reperfusion injury. Cardiovasc Res. 2007;75:478–86.CrossRefPubMed
52.
go back to reference Villablanca AC, Tenwolde A, Lee M, Huck M, Mumenthaler S, Rutledge JC. 17beta-estradiol prevents early-stage atherosclerosis in estrogen receptor-alpha deficient female mice. J Cardiovasc Transl Res. 2009;2(3):289–99.PubMedCentralCrossRefPubMed Villablanca AC, Tenwolde A, Lee M, Huck M, Mumenthaler S, Rutledge JC. 17beta-estradiol prevents early-stage atherosclerosis in estrogen receptor-alpha deficient female mice. J Cardiovasc Transl Res. 2009;2(3):289–99.PubMedCentralCrossRefPubMed
53.
go back to reference Takada Y, Kato C, Kondo S, Korenaga R, Ando J. Cloning of cDNAs encoding G protein-coupled receptor expressed in human endothelial cells exposed to fluid shear stress. Biochem Biophys Res Commun. 1997;240:737–41.CrossRefPubMed Takada Y, Kato C, Kondo S, Korenaga R, Ando J. Cloning of cDNAs encoding G protein-coupled receptor expressed in human endothelial cells exposed to fluid shear stress. Biochem Biophys Res Commun. 1997;240:737–41.CrossRefPubMed
54.
go back to reference Sack MN, Rader DJ, Cannon RO. Oestrogen and inhibition of oxidation of low-density lipoproteins in postmenopausal women. Lancet. 1994;343:269–70.CrossRefPubMed Sack MN, Rader DJ, Cannon RO. Oestrogen and inhibition of oxidation of low-density lipoproteins in postmenopausal women. Lancet. 1994;343:269–70.CrossRefPubMed
55.
go back to reference Mikkola TS, Clarkson TB. Estrogen replacement therapy, atherosclerosis, and vascular function. Cardiovasc Res. 2002;53:605–19.CrossRefPubMed Mikkola TS, Clarkson TB. Estrogen replacement therapy, atherosclerosis, and vascular function. Cardiovasc Res. 2002;53:605–19.CrossRefPubMed
56.
go back to reference Piro M, Bona RD, Abbate A, Biasucci IM, Crea F. Sex-related differences in myocardial remodeling. J Am Coll Cardiol. 2010;55:1057–65.CrossRefPubMed Piro M, Bona RD, Abbate A, Biasucci IM, Crea F. Sex-related differences in myocardial remodeling. J Am Coll Cardiol. 2010;55:1057–65.CrossRefPubMed
57.
go back to reference Selvin E, Feinleib M, Zhang L, et al. Androgens and diabetes in men: results from the Third National Health and Nutrition Examination Survey (NHANES III). Diabetes Care. 2007;30(2):234–8.CrossRefPubMed Selvin E, Feinleib M, Zhang L, et al. Androgens and diabetes in men: results from the Third National Health and Nutrition Examination Survey (NHANES III). Diabetes Care. 2007;30(2):234–8.CrossRefPubMed
58.
go back to reference Hak AE, Witteman JC, de Jong FH, Geerlings MI, Hofman A, Pols HA. Low levels of endogenous androgens increase the risk of atherosclerosis in elderly men: the Rotterdam study. J Clin Endocrinol Metab. 2002;87(8):3632–9.CrossRefPubMed Hak AE, Witteman JC, de Jong FH, Geerlings MI, Hofman A, Pols HA. Low levels of endogenous androgens increase the risk of atherosclerosis in elderly men: the Rotterdam study. J Clin Endocrinol Metab. 2002;87(8):3632–9.CrossRefPubMed
59.
go back to reference Kaushik M, Sontineni SP, Hunter C. Cardiovascular disease and androgens: a review. Int J Cardiol. 2010;142(1):8–14.CrossRefPubMed Kaushik M, Sontineni SP, Hunter C. Cardiovascular disease and androgens: a review. Int J Cardiol. 2010;142(1):8–14.CrossRefPubMed
60.
go back to reference Jensen-Urstad K, Johansson J. Gender difference in age-related changes in vascular function. J Intern Med. 2001;250(1):29–36.CrossRefPubMed Jensen-Urstad K, Johansson J. Gender difference in age-related changes in vascular function. J Intern Med. 2001;250(1):29–36.CrossRefPubMed
61.
go back to reference Anuurad E, Boffa MB, Koschinsky ML, Berglund L. Lipoprotein(a): a unique risk factor for cardiovascular disease. Clin Lab Med. 2006;26(4):751–72.CrossRefPubMed Anuurad E, Boffa MB, Koschinsky ML, Berglund L. Lipoprotein(a): a unique risk factor for cardiovascular disease. Clin Lab Med. 2006;26(4):751–72.CrossRefPubMed
62.
go back to reference Qasim AN, Martin SS, Mehta NN, Wolfe ML, Park J, Schwartz S, et al. Lipoprotein(a) is strongly associated with coronary artery calcification in type-2 diabetic women. Int J Cardiol. 2011;150(1):17–21.PubMedCentralCrossRefPubMed Qasim AN, Martin SS, Mehta NN, Wolfe ML, Park J, Schwartz S, et al. Lipoprotein(a) is strongly associated with coronary artery calcification in type-2 diabetic women. Int J Cardiol. 2011;150(1):17–21.PubMedCentralCrossRefPubMed
63.
go back to reference Gremmel T, Kopp CW, Eichelberger B, Koppensteiner R, Panzer S. Sex differences of leukocyte-platelet interactions and on-treatment platelet reactivity in patients with atherosclerosis. Atherosclerosis. 2014;237(2):692–5.CrossRefPubMed Gremmel T, Kopp CW, Eichelberger B, Koppensteiner R, Panzer S. Sex differences of leukocyte-platelet interactions and on-treatment platelet reactivity in patients with atherosclerosis. Atherosclerosis. 2014;237(2):692–5.CrossRefPubMed
64.
go back to reference Koupenova M, Mick E, Mikhalev E, Benjamin EJ, Tanriverdi K, Freedman JE. Sex differences in platelet toll-like receptors and their association with cardiovascular risk factors. Arterioscler Thromb Vasc Biol. 2015;35(4):1030–7.CrossRefPubMed Koupenova M, Mick E, Mikhalev E, Benjamin EJ, Tanriverdi K, Freedman JE. Sex differences in platelet toll-like receptors and their association with cardiovascular risk factors. Arterioscler Thromb Vasc Biol. 2015;35(4):1030–7.CrossRefPubMed
65.
go back to reference Edfeldt K, Bennet AM, Eriksson P, Frostegård J, et al. Association of hypo-responsive toll- like receptor 4 variants with risk of myocardial infarction. Eur Heart J. 2004;25:1447–53.CrossRefPubMed Edfeldt K, Bennet AM, Eriksson P, Frostegård J, et al. Association of hypo-responsive toll- like receptor 4 variants with risk of myocardial infarction. Eur Heart J. 2004;25:1447–53.CrossRefPubMed
Metadata
Title
Gender-Related Differences in Atherosclerosis
Authors
Pankaj Mathur
Bohuslav Ostadal
Francesco Romeo
Jawahar L. Mehta
Publication date
01-08-2015
Publisher
Springer US
Published in
Cardiovascular Drugs and Therapy / Issue 4/2015
Print ISSN: 0920-3206
Electronic ISSN: 1573-7241
DOI
https://doi.org/10.1007/s10557-015-6596-3

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