Assessing endothelium resistance to thrombus formation as a potential risk factor causing recurrent cardiovascular events in young patients after cardiac infarction
I.A. Novikova, L.A. Nekrutenko, T.M. Lebedeva, A.V. Khachatryan
Perm State Medical University named after Academician E.A. Wagner, 26 Petropavlovskaya Str., Perm, 614000, Russian Federation
Cardiac infarction is considered a disease more common for elderly people; despite that, up to 10% of all cardiac infarctions occur at a young age. Cardiac infarction has grave consequences both for mental health and future working capability of patients who had it. Approximately 15% patients who have had cardiac infarction have to face a recurrent cardiovascular event based on thrombus formation in spite of therapy. Our research goal was to assess endothelium homeostasis in patients after cardiac infarction being treated with double anti-thrombocyte therapy during out-patient rehabilitation and to reveal potential risks that could cause recurrent cardiovascular diseases. Overall, we examined 25 people aged from 18 to 45 who had cardiac infarction and were treated with invasive therapy aimed at eliminating ischemic heart disease. The therapy was emergency percutaneous coronary intervention and coronary artery stenting performed at Perm Clinical Cardiologic Clinic during a period from September 2018 to March 2019. Endothelial homeostasis was examined in 12 months after cardiac infarction.
We detected that, together with conventional risk factors, young patients after cardiac infarction had apparent changes in coagulation homeostasis (shorter activated partial thromboplastin time, shorter prothrombin time, an increase in fibrinogen concentration; greater aggregative activity of thrombocytes with adenosine-diphosphate; depressed Hageman-factor-dependent fibrinolysis. Nevertheless, there was no significant difference in aggregative activity of thrombosytes with ristocetin between the test and control groups. Therefore, in 12 months after cardiac infarction, young patients still ran high risks of recurrent cardiovascular events; those risks were caused both by significant prevalence of conventional risk factors and by high thrombogenic risk that persisted in spite of relevant anti-thrombus therapy.
- Mathers C.D., Loncar D. Projections of global mortality and burden of disease from 2002 to 2030. PLoS Med, 2006, vol. 3, no. 11, pp. 2011–2030. DOI: 10.1371/journal.pmed.0030442
- Doughty M., Mehta R., Bruckman D., Das S., Karavite D., Tsai T., Eagle K. Acute myocardial infarction in the young – the University of Michigan experience. Am. Heart J., 2002, no. 143, pp. 56–62. DOI: 10.1067/mhj.2002.120300
- Imazio M., Bobbio M., Bergerone S., Barlera S., Maggioni A.P. Clinical and epidemiological characteristics of juvenile myocardial infarction in Italy: the GISSI experience. G. Ital. Cardiol, 1998, no. 28, pp. 505–512.
- Risgaard B., Nielsen J.B., Jabbari R., Haunsø S., Gaarsdal Holst A., Winkel B.G., Tfelt-Hansen J. Prior myocardial infarction in the young: predisposes to a high relative risk but low absolute risk of a sudden cardiac death. Europace, 2013, 15, pp. 48–54. DOI: 10.1093/europace/eus190
- Cardiovascular diseases (CVDs). World Health Organization, 2017. Available at: http://www.who.int/mediacentre/factsheets/fs317/en/ (26.11.2019).
- Giustino G., Mehran R., Dangas G.D., Kirtane A.J., Redfors B., Généreux P., Brener S.J., Prats J. [et al.]. Characterization of the average daily ischemic and bleeding risk after primary PCI for STEMI. J. Am. Coll. Cardiol, 2017, no. 70, pp. 1846–1857. DOI: 10.1016/j.jacc.2017.08.018
- Okafor O., Gorog D. Endogenous fibrinolysis: an important mediator of thrombus formation and cardiovascular risk. J. Am. Coll. Cardiol, 2015, no. 65, pp. 1683–1699.DOI: 10.1016/j.jacc.2015.02.040
- Leander K., Blomback M., Walle´n H., He S. Impaired fibrinolytic capacity and increased fibrin formation associate with myocardial infarction. Thromb. Haemost, 2012, no. 107, pp. 1092–1099. DOI: 10.1160/TH11-11-0760
- Davignon J., Ganz P. Role of endothelial dysfunction in atherosclerosis. Circulation, 2004, no. 109, pp. 327–332. DOI: 10.1161/01.CIR.0000131515.03336.f8
- Borissoff J.I., Spronk H.M., ten Cate H. The hemostatic system as a modulator of atherosclerosis. N. Engl. J. Med., 2011, vol. 364, no. 18, pp. 1746–1760. DOI: 10.1056/NEJMra1011670
- Van Gils J.M., Zwaginga J.J., Hordijk P.L. Molecular and functional interactions among monocytes, platelets, and endothelial cells and their relevance for cardiovascular diseases. J. Leukoc. Biol., 2009, vol. 85, no. 2, pp. 195–204. DOI: 10.1189/jlb.0708400
- Jin R.C., Voetsch B., Loscalzo J. Endogenous mechanisms of inhibition of platelet function. Microcirculation, 2005, vol. 12, no. 3, pp. 247–258. DOI: 10.1080/10739680590925493
- Yago T., Lou J., Wu T., Yang J., Miner J.J., Coburn L., López J.A., Cruz M.A. [et al.]. Platelet glycoprotein Ibalpha forms catch bonds with human WT vWF but not with type 2B von Willebrand disease vWF. J. Clin. Invest, 2008, vol. 118, no. 9, pp. 3195–3207. DOI: 10.1172/JCI35754
- Ruggeri Z.M. Von Willebrand factor, platelets and endothelial cell interactions. J. Thromb. Haemost, 2003, vol. 1, no. 7, pp. 1335–1342. DOI: 10.1046/j.1538-7836.2003.00260.x
- Kanaji S., Fahs S.A., Shi Q., Haberichter S.L., Montgomery R.R. Contribution of platelet vs. endothelial VWF to platelet adhesion and hemostasis. J. Thromb. Haemost, 2012, no. 10, pp. 1646–1652. DOI: 10.1111/j.1538-7836.2012.04797.x
- Yee A., Kretz C.A. Von Willebrand factor: form for function. Semin. Thromb. Hemost, 2014, no. 40, pp. 17–27. DOI: 10.1055/s-0033-1363155
- Boos C.J., Jaumdally R.J., MacFadyen R.J., Varma C., Lip G.Y.H. Circulating endothelial cells and von Willebrand factor as indices of endothelial damage/dysfunction in coronary artery disease: a comparison of central vs. peripheral levels and effects of coronary angioplasty. J. Thromb. Haemost, 2007, no. 5, pp. 630–632. DOI: 10.1111/j.1538-7836.2007.02341.x
- Pinsky D.J., Naka Y., Liao H., Oz M.C., Wagner D.D., Mayadas T.N., Johnson R.C., Hynes R.O. [et al.]. Hypoxia-induced exocytosis of endothelial cell Weibel-Palade bodies. A mechanism for rapid neutrophil recruitment after cardiac preservation. J. Clin. Invest, 1996, no. 97, pp. 493–500. DOI: 10.1172/JCI118440
- Zezos P., Papaioannou G., Nikolaidis N., Vasiliadis T., Giouleme O., Evgenidis N. Elevated plasma von Willebrand factor levels in patients with active ulcerative colitis reflect endothelial perturbation due to systemic inflammation. World J. Gastroenterol, 2005, no. 11, pp. 7639–7645. DOI: 10.3748/wjg.v11.i48.7639
- Lenting P.J., Christophe O.D., Denis C.V. Von Willebrand factor biosynthesis, secretion, and clearance: connecting the far ends. Blood, 2015, vol. 125, no. 13, pp. 2019–2028. DOI: 10.1182/blood-2014-06-528406
- Li Z., Delaney M.K., O'Brien K.A., Du X. Signaling during platelet adhesion and activation. Arterioscler. Thromb. Vasc. Biol., 2010, vol. 30, no. 12, pp. 2341–2349. DOI: 10.1161/ATVBAHA.110.207522
- Collet J.P., Allali Y., Lesty C., Tanguy M.L., Silvain J., Ankri A., Blanchet B., Dumaine R. [et al.]. Altered fibrin architecture is associated with hypofibrinolysis and premature coronary atherothrombosis. Arterioscler. Thromb. Vasc. Biol., 2006, vol. 26, pp. 2567–2573. DOI: 10.1161/01.ATV.0000241589.52950.4c
- McMullen B.A., Fujikawa K. Amino acid sequence of the heavy chain of human a-factor XIIa (activated Hageman factor). J. Biol. Chem, 1985, no. 260, pp. 5328–5341.
- Binnema D.J., Dooijewaard G., Turion P.N.C. An analysis of the activators of single-chain urokinase-type plasminogen activator (scu-PA) in the dextran sulphateeuglobulin fraction of normal plasma and of plasmas deficient in factor XII and prekallikrein. Thromb. Haemost, 1991, no. 65, pp. 144–148. DOI: 10.1055/s-0038-1647473
- Fuhrer G., Gallimore M.J., Heller W., Hoffmeister H.E. FXII. Blut, 1990, no. 61, pp. 258–266. DOI: 10.1007/BF01732874
- Ganyukov V.I., Shilov A.A., Bokhan N.S., Moiseenkov G.V., Barbarash L.S. Prichiny trombozov stentov koronarnykh arterii [Reasons for thrombosis in coronary artery stents]. Mezhdunarodnyi Zhurnal interventsionnoi kardioangiologii, 2012, no. 28, pp. 29–34 (in Russian).
- Kukes V.G. Klinicheskaya farmakologiya [Clinical pharmacology]. Moscow, GEOTAR-Media Publ., 2008, pp. 392–395 (in Russian).
- Thygesen K., Alpert J.S., Jaffe A.S., Chaitman B.R., Bax J.J., Morrow D.A., White H.D. [et al.]. Fourth universal definition of myocardial infarction. European Heart Journal, 2018, vol. 13, no. 138 (20), pp. e618–e651. DOI: 10.1161/CIR.0000000000000617
- Kurtul A., Yarlioglues M., Murat S.N., Duran M., Oksuz F., Koseoglu C., Celik I.E., Kilic A. [et al.]. The association of plasma fibrinogen with the extent and complexity of coronary lesions in patients with acute coronary syndromes. Kardiol. Pol., 2016, no. 74, pp. 338–345. DOI: 10.5603/KP.a2015.0196
- Lupi A., Secco G.G., Rognoni A., Rossi L., Lazzero M., Nardi F., Rolla R., Bellomo G. [et al.]. Plasma fibrinogen levels and restenosis after primary percutaneous coronary intervention. J. Thromb. Thrombolysis, 2012, no. 33, pp. 308–317. DOI: 10.1007/s11239-011-0628-z
- Mahmud E., Behnamfar O., Lin F., Reeves R., Patel M., Ang L. [et al.]. Elevated serum fibrinogen is associated with 12-month major adverse cardiovascular events following percutaneous coronary intervention. J. Am. Coll. Cardiol, 2016, no. 67, pp. 2556–2557. DOI: 10.1016/j.jacc.2016.03.540
- Trip M.D., Cats V.M., Van Capelle F.J., Vreeken J. Platelet hyperreactivity and prognosis in survivors of myocardial infarction. N. Engl. J. Med., 1990, no. 322, pp. 1549–1554. DOI: 10.1056/NEJM199005313222201
- Gurbel P.A., Becker R.C., Mann K.G., Steinhubl S.R., Michelson A.D. Platelet function monitoring in patients with coronary artery disease. J. Am. Coll. Cardiol., 2007, no. 50, pp. 1822–1834. DOI: 10.1016/j.jacc.2007.07.051
- Wiviott S.D., Braunwald E., McCabe C.H., Montalescot G., Ruzyllo W., Gottlieb S., Neumann F.-J., Ardissino D. [et al.]. TRITON-TIMI 38 Investigators. Prasugel versus clopidogrel in patients with acute coronary syndromes. N. Engl. J. Med., 2007, no. 357, pp. 2001–2015. DOI: 10.1056/NEJMoa0706482
- Wallentin L., Becker R.C., Budaj A., Cannon C.P., Emanuelsson H., Held C., Horrow J., Husted S. [et al.]. Ticagrelor versus clopidogrel in patients with acute coronary syndromes. N. Engl. J. Med., 2009, no. 361, pp. 1045–1057. DOI: 10.1056/NEJMoa0904327
- Stuckey T.D., Kirtane A.J., Brodie B.R.,Witzenbichler B., Litherland C., Weisz G., Rinaldi M.J., Neumann F.-J. [et al.]. Impact of aspirin and clopidogrel hypo responsiveness in patients treated with drug-eluting stents: 2-year results of a prospective, multicenter registry study. JACC Cardiovasc. Interv., 2017, no. 10, pp. 1607–1617. DOI: 10.1016/j.jcin.2017.05.059
- Wang X., Zhao J., Zhang Y., Xue X., Yin J., Liao L., Xu C., Hou Y. [et al.]. Kinetics of plasma von Willebrand factor in acute myocardial infarction patients: a meta-analysis. Oncotarget, 2017, vol. 8, no. 52, pp. 90371–90379. DOI: 10.18632/oncotarget.20091
- Sambola A., García Del Blanco B., Ruiz-Meana M., Francisco J., Barrabés J.A., Figueras J., Bañeras J., Otaegui I. [et al.]. Increased von Willebrand factor, P-selectin and fibrin content in occlusive thrombus resistant to lytic therapy. Thromb. Haemost, 2016, vol. 115, no. 6, pp. 1129–1137. DOI: 10.1160/TH15-12-0985
- Ozawa K., Packwood W., Varlamov O., Qi Y., Xie A., Wu M.D., Ruggeri Z., López J. [et al.]. Molecular Imaging of VWF (von Willebrand Factor) and Platelet Adhesion in Postischemic Impaired Microvascular Reflow. Circ. Cardiovasc. Imaging, 2018, vol. 11, no. 11, pp. 1–9. DOI: 10.1161/CIRCIMAGING.118.007913
- Saraf S., Christopoulos C., Salha I.B., Stott D.J., Gorog D.A. Impaired endogenous thrombolysis in acute coronary syndrome patients predicts cardiovascular death and nonfatal myocardial infarction. J. Am Coll. Cardiol, 2010, vol. 55, no. 19, pp. 2107–2115.DOI: 10.1016/j.jacc.2010.01.033
- Christopoulos C., Farag M., Sullivan K., Wellsted D., Gorog D.A. Impaired thrombolytic status predicts adverse cardiac events in patients undergoing primary percutaneous coronary intervention. Thromb. Haemost, 2017, vol. 117, no. 3, pp. 457–470. DOI: 10.1160/TH16-09-0712
- Farag М., Spinthakis N., Gue Y.X., Srinivasan M., Sullivan K., Wellsted D., Gorog D.A. Impaired endogenous fibrinolysis in ST-segment elevation myocardial infarction patients undergoing primary percutaneous coronary intervention is a predictor of recurrent cardiovascular events: the RISK PPCI study. European Heart Journal, 2019, vol. 40, no. 3, pp. 295–305. DOI: 10.1093/eurheartj/ehy656
- Ryamzina I.N, Glebova S.A. Pokazateli gemostaza i lipidnogo profilya kak prediktory serdechno-sosudistoi smerti u bol'nykh, perenesshikh infarct miokarda [Parameters of homeostasis and lipid profile as predictors of cardiovascular death among patients who have had cardiac infarction]. Permskii meditsinskii zhurnal, 2003, vol. 20, no. 2, pp. 73–77 (in Russian).