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Polyhedral erythrocytes in intracoronary thrombus and their association with reperfusion in myocardial infarction

  • Jaroslaw ZalewskiEmail author
  • Lukasz Lewicki
  • Krzysztof Krawczyk
  • Michal Zabczyk
  • Radoslaw Targonski
  • Patrycja Molek
  • Jadwiga Nessler
  • Anetta Undas
Original Paper
  • 28 Downloads

Abstract

Objective

The tightly packed arrays of polyhedral erythrocytes, polyhedrocytes, formed during thrombus contraction, have been detected in some intracoronary thrombi (ICT) obtained from patients with ST-segment elevation myocardial infarction (STEMI). We sought to investigate determinants of polyhedrocyte content in ICT and its association with reperfusion in STEMI.

Methods

We assessed the composition of ICT obtained during thrombectomy within 12 h since the symptom onset in 110 STEMI patients, following 300 mg of aspirin (n = 110) and 600 mg of clopidogrel (n = 75). The predominance of fibrin, erythrocytes, polyhedrocytes or platelets was evaluated using scanning electron microscopy.

Results

Polyhedrocytes were found in 34 (30.9%) ICT, in which they covered 20–50% (median 38.8%) fields of view. Patients with polyhedrocytes in ICT had lower median minimal reference infarct-related artery (IRA) diameter by 20% (p < 0.0001) and area by 31% (p < 0.0001) versus those without polyhedrocytes. Time of ischemia showed association with the polyhedrocyte content (r = 0.26, p = 0.007). By multivariate analysis, minimal IRA diameter (β = − 0.50, p < 0.0001) and ischemia time (β = 0.20, p = 0.035) independently affected polyhedrocyte content in ICT (R2 = 0.45, p < 0.0001). Patients with ischemia time of > 3 h and polyhedrocytes present in ICT had more frequently TIMI-2/3 flow after thrombus aspiration (96% vs. 67%, p = 0.02) and final TIMI-2/3 myocardial perfusion grade (92% vs. 57%, p = 0.044) versus those without polyhedrocytes.

Conclusions

Our findings indicate that the presence of polyhedrocytes in ICT, observed in one-third of STEMI patients, is associated with smaller minimal IRA diameter, prolonged ischemia and their formation in late presenters is associated with more effective thrombus aspiration and better myocardial reperfusion.

Keywords

Polyhedrocytes Thrombus Myocardial infarction Scanning electron microscopy 

Notes

Acknowledgements

This work was supported by grants of the Jagiellonian University Medical College (K/ZDS/006441) and by National Science Centre Poland (2016/21/B/NZ5/01378).

Compliance with ethical standards

Conflict of interest

The authors have nothing to disclose in relation to this study.

Supplementary material

392_2019_1425_MOESM1_ESM.doc (535 kb)
Supplementary material 1 (DOC 535 KB)

References

  1. 1.
    Dégano IR, Salomaa V, Veronesi G, Ferriéres J, Kirchberger I, Laks T, Havulinna AS, Ruidavets JB, Ferrario MM, Meisinger C, Elosua R, Marrugat J (2015) Twenty-five-year trends in myocardial infarction attack and mortality rates, and case-fatality, in six European populations. Heart 101:1413–1421.  https://doi.org/10.1136/heartjnl-2014-307310 CrossRefGoogle Scholar
  2. 2.
    Fox KA, Dabbous OH, Goldberg RJ, Pieper KS, Eagle KA, Van de Werf F, Avezum A, Goodman SG, Flather MD, Anderson FA Jr, Granger CB (2006) Prediction of risk of death and myocardial infarction in the six months after presentation with acute coronary syndrome: prospective multinational observational study (GRACE). BMJ 333:1091.  https://doi.org/10.1136/bmj.38985.646481.55 CrossRefGoogle Scholar
  3. 3.
    Roffi M, Patrono C, Collet JP et al (2016) 2015 ESC guidelines for the management of acute coronary syndromes in patients presenting without persistent ST-segment elevation: task force for the management of acute coronary syndromes in patients presenting without persistent ST-segment elevation of the European Society of Cardiology (ESC). Eur Heart J 37:267–315.  https://doi.org/10.1093/eurheartj/ehv320 CrossRefGoogle Scholar
  4. 4.
    Nührenberg TG, Hochholzer W, Mashayekhi K, Ferenc M, Neumann FJ (2018) Efficacy and safety of bivalirudin for percutaneous coronary intervention in acute coronary syndromes: a meta-analysis of randomized-controlled trials. Clin Res Cardiol 107:807–815.  https://doi.org/10.1007/s00392-018-1251-1 CrossRefGoogle Scholar
  5. 5.
    Fournier S, Muller O, Benedetto U, Roffi M, Pilgrim T, Eberli FR, Rickli H, Radovanovic D, Erne P, Cook S, Noble S, Fesselet R, Zuffi A, Degrauwe S, Masci P, Windecker S, Eeckhout E, Iglesias JF, on behalf on the AMIS Plus Investigators (2018) Circadian dependence of manual thrombus aspiration benefit in patients with ST-segment elevation myocardial infarction undergoing primary percutaneous coronary intervention. Clin Res Cardiol 107:338–346.  https://doi.org/10.1007/s00392-017-1189-8 CrossRefGoogle Scholar
  6. 6.
    Khoury S, Carmon S, Margolis G, Keren G, Shacham Y (2017) Incidence and outcomes of early left ventricular thrombus following ST-elevation myocardial infarction treated with primary percutaneous coronary intervention. Clin Res Cardiol 106:695–701.  https://doi.org/10.1007/s00392-017-1111-4 CrossRefGoogle Scholar
  7. 7.
    Undas A, Zalewski J, Krochin M, Siudak Z, Sadowski M, Pregowski J, Dudek D, Janion M, Witkowski A, Zmudka K (2010) Altered plasma fibrin clot properties are associated with in-stent thrombosis. Arterioscler Thromb Vasc Biol 30:276–282.  https://doi.org/10.1161/ATVBAHA.109.194936 CrossRefGoogle Scholar
  8. 8.
    Henriques JP, Zijlstra F, Ottervanger JP, de Boer MJ, van ‘t Hof AW, Hoorntje JC, Suryapranata H (2002) Incidence and clinical significance of distal embolization during primary angioplasty for acute myocardial infarction. Eur Heart J 23:1112–1117.  https://doi.org/10.1053/euhj.2001.3035 CrossRefGoogle Scholar
  9. 9.
    Zalewski J, Zmudka K, Musialek P, Zajdel W, Pieniazek P, Kadzielski A, Przewlocki T (2004) Detection of microvascular injury by evaluating epicardial blood flow in early reperfusion following primary angioplasty. Int J Cardiol 96:389–396.  https://doi.org/10.1016/j.ijcard.2003.08.009 CrossRefGoogle Scholar
  10. 10.
    Zalewski J, Undas A, Godlewski J, Stepien E, Zmudka K (2007) No-reflow phenomenon after acute myocardial infarction is associated with reduced clot permeability and susceptibility to lysis. Arterioscler Thromb Vasc Biol 27:2258–2265.  https://doi.org/10.1161/ATVBAHA.107.149633 CrossRefGoogle Scholar
  11. 11.
    Stone GW, Peterson MA, Lansky AJ, Dangas G, Mehran R, Leon MB (2002) Impact of normalized myocardial perfusion after successful angioplasty in acute myocardial infarction. J Am Coll Cardiol 39:591–597.  https://doi.org/10.1016/S0735-1097(01)01779-X CrossRefGoogle Scholar
  12. 12.
    Zalewski J, Bogaerts K, Desmet W, Sinnaeve P, Berger P, Grines C, Danays T, Armstrong P, Van de Werf F (2011) Intraluminal thrombus in facilitated versus primary percutaneous coronary intervention; an angiographic substudy of the ASSENT-4 PCI (assessment of the safety and efficacy of a new treatment strategy with percutaneous coronary intervention) trial. J Am Coll Cardiol 57:1867–1873.  https://doi.org/10.1016/j.jacc.2010.10.061 CrossRefGoogle Scholar
  13. 13.
    Badimon L, Chesebro JH, Badimon JJ (1992) Thrombus formation on ruptured atherosclerotic plaques and rethrombosis on evolving thrombi. Circulation 86(6 Suppl):III74–I85Google Scholar
  14. 14.
    Furie B, Furie BC (2008) Mechanisms of thrombus formation. N Engl J Med 359:938–949.  https://doi.org/10.1056/NEJMra0801082 CrossRefGoogle Scholar
  15. 15.
    Cines DB, Lebedeva T, Nagaswami C, Hayes V, Massefski W, Litvinov RI, Rauova L, Lowery TJ, Weisel JW (2014) Clot contraction: compression of erythrocytes into tightly packed polyhedra and redistribution of platelets and fibrin. Blood 123:1596–1603.  https://doi.org/10.1182/blood-2013-08-523860 CrossRefGoogle Scholar
  16. 16.
    Tutwiler V, Litvinov RI, Lozhkin AP, Peshkova AD, Lebedeva T, Ataullakhanov FI, Spiller KL, Cines DB, Weisel JW (2016) Kinetics and mechanics of clot contraction are governed by the molecular and cellular composition of the blood. Blood 127:149–159.  https://doi.org/10.1182/blood-2015-05-647560 CrossRefGoogle Scholar
  17. 17.
    Zabczyk M, Sadowski M, Zalewski J, Undas A (2015) Polyhedrocytes in intracoronary thrombi from patients with ST-elevation myocardial infarction. Int J Cardiol 179:186–187.  https://doi.org/10.1016/j.ijcard.2014.10.004 CrossRefGoogle Scholar
  18. 18.
    Zalewski J, Bogaert J, Sadowski M, Woznicka O, Doulaptsis K, Ntoumpanaki M, Ząbczyk M, Nessler J, Undas A (2015) Plasma fibrin clot phenotype independently affects intracoronary thrombus ultrastructure in patients with acute myocardial infarction. Thromb Haemost 113:1258–1269.  https://doi.org/10.1160/TH14-09-0801 CrossRefGoogle Scholar
  19. 19.
    Litvinov RI, Weisel JW (2017) Role of red blood cells in haemostasis and thrombosis. ISBT Sci Ser 12:176–183.  https://doi.org/10.1111/voxs.12331 CrossRefGoogle Scholar
  20. 20.
    Tutwiler V, Peshkova AD, Adrianova IA, Khasanova DR, Weisel JW, Litvinov RI (2017) Contraction of blood cells is impaired in acute ischemic stroke. Arterioscler Thromb Vasc Biol 37:271–279.  https://doi.org/10.1161/ATVBAHA.116.308622 CrossRefGoogle Scholar
  21. 21.
    Silvain J, Collet JP, Nagaswami C, Beygui F, Edmondson KE, Bellemain-Appaix A, Cayla G, Pena A, Brugier D, Barthelemy O, Montalescot G, Weisel JW (2011) Composition of coronary thrombus in acute myocardial infarction. J Am Coll Cardiol 57:1359–1367.  https://doi.org/10.1016/j.jacc.2010.09.077 CrossRefGoogle Scholar
  22. 22.
    Collins TJ (2007) ImageJ for microscopy. Biotechniques 43:25–30.  https://doi.org/10.2144/000112517 CrossRefGoogle Scholar
  23. 23.
    Undas A, Szułdrzynski K, Stepien E, Zalewski J, Godlewski J, Tracz W, Pasowicz M, Zmudka K (2008) Reduced clot permeability and susceptibility to lysis in patients with acute coronary syndrome: effects of inflammation and oxidative stress. Atherosclerosis 196:551–557.  https://doi.org/10.1016/j.atherosclerosis.2007.05.028 CrossRefGoogle Scholar
  24. 24.
    Salonen EM, Vartio T, Hedman K (1984) Binding of fibronectin by the acute phase C-reactive protein. J Biol Chem 259:1496–1501Google Scholar
  25. 25.
    Ek A, Ekblom Ö, Hambraeus K, Cider Å, Kallings LV, Börjesson M (2018) Physical inactivity and smoking after myocardial infarction as predictors for readmission and survival: results from the SWEDEHEART-registry. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1360-x. [Epub ahead of print] Google Scholar
  26. 26.
    Fang XY, Spieler D, Albarqouni L, Ronel J, Ladwig KH (2018) Impact of generalized anxiety disorder (GAD) on prehospital delay of acute myocardial infarction patients. Findings from the multicenter MEDEA study. Clin Res Cardiol 107:471–478.  https://doi.org/10.1007/s00392-018-1208-4 CrossRefGoogle Scholar
  27. 27.
    Groot HE, Al Ali L, van der Horst ICC, Schurer RAJ, van der Werf HW, Lipsic E, van Veldhuisen DJ, Karper JC, van der Harst P (2018) Plasma interleukin 6 levels are associated with cardiac function after ST-elevation myocardial infarction. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1387-z. [Epub ahead of print] Google Scholar
  28. 28.
    Bodde MC, Hermans MC, Jukema MPJ, Schalij JW, Lijfering MJ, Rosendaal WM, Romijn FR, Ruhaak FPHTM, van der Laarse LR, Cobbaert A (2018) Apolipoproteins A1, B, and apoB/apoA1 ratio are associated with first ST-segment elevation myocardial infarction but not with recurrent events during long-term follow-up. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1381-5. [Epub ahead of print] Google Scholar
  29. 29.
    Ferreira JP, Barros A, Pitt B, Montalescot G, de Sa EL, Hamm CW, Flather M, Verheugt F, Shi H, Leite-Moreira A, Vincent J, Rossignol P, Zannad F (2018) Collagen biomarker bioprofiles predicting the antifibrotic response to eplerenone in myocardial infarction: findings from the REMINDER trial. Clin Res Cardiol 107:1192–1195.  https://doi.org/10.1007/s00392-018-1373-5 CrossRefGoogle Scholar
  30. 30.
    Plakht Y, Gilutz H, Shiyovich A (2018) Sodium levels during hospitalization with acute myocardial infarction are markers of in-hospital mortality: Soroka acute myocardial infarction II (SAMI-II) project. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1268-5. [Epub ahead of print] Google Scholar
  31. 31.
    Cecchi E, Parodi G, Fatucchi S, Angelotti P, Giglioli C, Gori AM, Bandinelli B, Bellandi B, Sticchi E, Romagnuolo I, Mannini L, Antoniucci D, Abbate (2016) Prevalence of thrombophilic disorders in takotsubo patients: the (ThROmbophylia in TAkotsubo cardiomyopathy) TROTA study. Clin Res Cardiol 105:717–726.  https://doi.org/10.1007/s00392-016-0977-x. [Epub ahead of print] CrossRefGoogle Scholar
  32. 32.
    Reithmann C, Fiek M, Aynur Z, Ulbrich M (2018) Electrocardiographic criteria of epicardial ventricular tachycardia with anterior origin. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1349-5. [Epub ahead of print] Google Scholar
  33. 33.
    Gassanov N, Le MT, Caglayan E, Hellmich M, Erdmann E, Er F (2018) Novel ECG-based scoring tool for prediction of takotsubo syndrome. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1314-3. [Epub ahead of print] Google Scholar
  34. 34.
    Stiermaier T, Pöss J, Eitel C, de Waha S, Fuernau G, Desch S, Thiele H, Eitel I (2018) Impact of left ventricular hypertrophy on myocardial injury in patients with ST-segment elevation myocardial infarction. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1273-8. [Epub ahead of print] Google Scholar
  35. 35.
    Khoury S, Steinvil A, Gal-Oz A, Margolis G, Hochstatd A, Topilsky Y, Keren G, Shacham Y (2018) Association between central venous pressure as assessed by echocardiography, left ventricular function and acute cardio-renal syndrome in patients with ST segment elevation myocardial infarction. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1266-7. [Epub ahead of print] Google Scholar
  36. 36.
    Abdin A, Pöss J, Fuernau G, Ouarrak T, Desch S, Eitel I, de Waha S, Zeymer U, Böhm M, Thiele H (2018) Correction to: prognostic impact of baseline glucose levels in acute myocardial infarction complicated by cardiogenic shock-a substudy of the IABP-SHOCK II-trial. Clin Res Cardiol 107:531.  https://doi.org/10.1007/s00392-018-1225-3 CrossRefGoogle Scholar
  37. 37.
    Abdin A, Pöss J, Fuernau G, Ouarrak T, Desch S, Eitel I, de Waha S, Zeymer U, Böhm M, Thiele H (2018) Revision: prognostic impact of baseline glucose levels in acute myocardial infarction complicated by cardiogenic shock-a substudy of the IABP-SHOCK II-trial. Clin Res Cardiol 107:517–523.  https://doi.org/10.1007/s00392-018-1213-7. (PMID: 29423774) CrossRefGoogle Scholar
  38. 38.
    Backhaus T, Fach A, Schmucker J, Fiehn E, Garstka D, Stehmeier J, Hambrecht R, Wienbergen H (2018) Management and predictors of outcome in unselected patients with cardiogenic shock complicating acute ST-segment elevation myocardial infarction: results from the Bremen STEMI Registry. Clin Res Cardiol 107:371–379.  https://doi.org/10.1007/s00392-017-1192-0 CrossRefGoogle Scholar
  39. 39.
    Ferenc M, Banholzer N, Hochholzer W, Mashayekhi K, Comberg T, Rothe J, Valina CM, Toma A, Löffelhardt N, Gick M, Neumann FJ, Nührenberg TG (2018) Long-term results after PCI of unprotected distal left main coronary artery stenosis: the Bifurcations Bad Krozingen (BBK)-Left Main Registry. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1337-9. [Epub ahead of print] Google Scholar
  40. 40.
    Richardt G, Maillard L, Nazzaro MS, Abdel-Wahab M, Carrié D, Iñiguez A, Garot P, Abdellaoui M, Morice MC, Foley D, Copt S, Stoll HP, Urban P (2018) Polymer-free drug-coated coronary stents in diabetic patients at high bleeding risk: a pre-specified sub-study of the LEADERS FREE trial. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1308-1. [Epub ahead of print] Google Scholar
  41. 41.
    Feistritzer HJ, Desch S, de Waha S, Jobs A, Zeymer U, Thiele H (2018) German contribution to development and innovations in the management of acute myocardial infarction and cardiogenic shock. Clin Res Cardiol.  https://doi.org/10.1007/s00392-018-1276-5. [Epub ahead of print] Google Scholar
  42. 42.
    Tripodi A, Braham S, Scimeca B, Moia M, Peyvandi F (2018) How and when to measure anticoagulant effects of direct oral anticoagulants? Practical issues. Pol Arch Intern Med 128:379–385.  https://doi.org/10.20452/pamw.4287 CrossRefGoogle Scholar
  43. 43.
    Yunoki K, Naruko T, Sugioka K, Inaba M, Iwasa Y, Komatsu R, Itoh A, Haze K, Inoue T, Yoshiyama M, Becker AE, Ueda M (2012) Erythrocyte-rich thrombus aspirated from patients with ST-elevation myocardial infarction: association with oxidative stress and its impact on myocardial reperfusion. Eur Heart J 33:1480–1490.  https://doi.org/10.1093/eurheartj/ehr486 CrossRefGoogle Scholar
  44. 44.
    Li X, Kramer MC, Damman P, van der Wal AC, Grundeken MJ, van Straalen JP, Koch KT, Henriques JP, Baan J Jr, Vis MM, Piek JJ, Fischer JC, Tijssen JG, de Winter RJ (2016) Older coronary thrombus is an independent predictor of 1-year mortality in acute myocardial infarction. Eur J Clin Invest 46:501–510.  https://doi.org/10.1111/eci.12619 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Coronary Artery DiseaseJagiellonian University Medical CollegeKrakowPoland
  2. 2.Gdansk University of TechnologyGdanskPoland
  3. 3.Pomeranian Cardiology CentersWejherowoPoland
  4. 4.Department of Experimental Cardiac Surgery, Anesthesiology and CardiologyJagiellonian University Medical CollegeKrakowPoland

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