Platelet-derived microvesicles in cardiovascular diseases
DOI:
https://doi.org/10.52692/1857-0011.2024.1-78.17Keywords:
platelet-derived extracellular vesicles, ndothelial dysfunction, inflammation, thrombosisAbstract
Extracellular vesicles (EVs) are a family of particles/vesicles present in blood and body fluids, bounded by a lipid dual- layer and non-replicable. They do not contain a functional core and carry a variety of molecules important in mediating cellular communication, thereby modulating crucial cellular processes such as homeostasis, induction/attenuation of inflammation, and support of cellular repair.Their existence, initially suspected in 1946 and confirmed in 1967, led to a sudden increase in the number of scientific publications, given their potential significance in understanding the mechanisms underlying various diseases, such as cancer, cardiovascular, metabolic, neurological diseases and infectious. These researches revealed a role for EVs as promising candidate biomarkers for diagnosis, prognosis, and even therapeutic purposes.The population of platelet-derived vesicles (pEVs) is the largest among other types of circulating EVs.Cell membrane physical characteristics and biological burden define the pivotal role of platelet-derived vesicles in the pathogenesis of cardiovascular (CV) diseases.Platelet-derived EVs are, therefore, key players in mediating inflammatory and coagulation reactions involving endotheliocytes, platelets, smooth muscle cells and inflammatory cells and thus contribute to the development ofatherosclerosis and angiogenesis, dysregulation of the coronary microcirculation in contiguity with endothelial dysfunction. In addition, EVs play an essential role in tissue repair, angiogenesis, and neovascularization through intracellular signaling cascades. In fact, EVs mediate autocrine and paracrine signals that are able to rebuild the homeostatic microenvironment in the heart and vessels.This review aims to provide a brief overview of the biogenesis, characteristics of platelet micro-particles with a special focus on their involvement in cardiovascular disease, but especially on the link between thrombosis, endothelial dysfunction and inflammation.In addition, here we review early experiments, summarize key findings that propelled the field, describe the growth of an organized EV community, and discuss the current state of the field.
References
E. Bazzan et al., “Critical Review of the Evolution of Extracellular Vesicles’ Knowledge: From 1946 to Today,” Int. J. Mol. Sci., vol. 22, no. 12, Jun. 2021, doi: 10.3390/IJMS22126417.
M. Mabrouk, F. Guessous, A. Naya, Y. Merhi, and Y. Zaid, “The Pathophysiological Role of Platelet-Derived Extracellular Vesicles,” Semin. Thromb. Hemost., vol.49, no. 3, pp. 279–283, Apr. 2023, doi: 10.1055/S-0042-1756705/ID/JR03047-14/BIB.
S. Fu, Y. Zhang, Y. Li, L. Luo, Y. Zhao, and Y. Yao, “Extracellular vesicles in cardiovascular diseases,” Cell Death Discov. 2020 61, vol. 6, no. 1, pp. 1–9, Jul. 2020, doi: 10.1038/s41420-020-00305-y.
A. Hafiane and S. S. Daskalopoulou, “Extracellular vesicles characteristics and emerging roles in atherosclerotic cardiovascular disease,” Metabolism, vol. 85, pp. 213–222, Aug. 2018, doi: 10.1016/J.METABOL.2018.04.008.
S. Palazzolo, V. Canzonieri, and F. Rizzolio, “The history of small extracellular vesicles and their implication in cancer drug resistance,” Front. Oncol., vol. 12, p. 948843, Aug. 2022, doi: 10.3389/FONC.2022.948843/ BIBTEX.
P. Wolf, “The nature and significance of platelet products in human plasma,” Br. J. Haematol., vol. 13, no. 3, pp. 269–288, 1967, doi: 10.1111/J.1365-2141.1967. TB08741.X.
S. Saheera, V. P. Jani, K. W. Witwer, and S. Kutty, “Extracellular vesicle interplay in cardiovascular pathophysiology,” Am. J. Physiol. - Hear. Circ. Physiol., vol. 320, no. 5, pp. H1749–H1761, May 2021, doi: 10.1152/AJPHEART.00925.2020/ASSET/IMAGES/ LARGE/AJPHEART.00925.2020_F003.JPEG.
Y. Couch et al., “A brief history of nearly EV‐ erything – The rise and rise of extracellular vesicles,” J. Extracell. Vesicles, vol. 10, no. 14, Dec. 2021, doi: 10.1002/JEV2.12144.
Y. J. Lee et al., “Elevated platelet microparticles in transient ischemic attacks, lacunar infarcts, and multiinfarct dementias,” Thromb. Res., vol. 72, no. 4, pp. 295–304, Nov. 1993, doi: 10.1016/0049-3848(93)90138-E.
“Elevated platelet-derived microparticle levels during unstable angina - PubMed.” https://pubmed.ncbi.nlm.nih.gov/8542543/ (accessed Apr. 07, 2024).
J. J. Powell, R. S. J. Harvey, and R. P. H. Thompson, “Microparticles in Crohn’s disease--has the dust settled?,” Gut, vol. 39, no. 2, p. 340, 1996, doi: 10.1136/GUT.39.2.340.“Membrane vesiculation protects erythrocytes from destruction by complement - PubMed.” https://pubmed.ncbi.nlm.nih.gov/1918984/ (accessed Apr. 07, 2024).
O. Fourcade et al., “Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells,” Cell, vol. 80, no. 6, pp. 919–927, Mar. 1995, doi: 10.1016/0092- 8674(95)90295-3.
G. Raposo et al., “B lymphocytes secrete antigen- presenting vesicles,” J. Exp. Med., vol. 183, no. 3, pp. 1161–1172, Mar. 1996, doi: 10.1084/JEM.183.3.1161.
R. Wubbolts et al., “Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation,” J. Biol. Chem., vol. 278, no. 13, pp. 10963– 10972, Mar. 2003, doi: 10.1074/JBC.M207550200.
C. Subra, K. Laulagnier, B. Perret, and M. Record, “Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies,” Biochimie, vol. 89, no. 2, pp. 205–212, Feb. 2007, doi: 10.1016/J.BIOCHI.2006.10.014.
G. Van Niel et al., “Intestinal epithelial exosomes carry MHC class II/peptides able to inform the immune system in mice,” Gut, vol. 52, no. 12, pp. 1690–1697, Dec. 2003, doi: 10.1136/GUT.52.12.1690.
N. Chaput, N. E. C. Schartz, F. Andre, and L. Zitvogel, “Exosomes for immunotherapy of cancer,” Adv. Exp. Med. Biol., vol. 532, pp. 215–221, 2003, doi: 10.1007/978-1-4615-0081-0_17.
H. Valadi, K. Ekström, A. Bossios, M. Sjöstrand,J. J. Lee, and J. O. Lötvall, “Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells,” Nat. Cell Biol., vol. 9, no. 6, pp. 654–659, Jun. 2007, doi: 10.1038/NCB1596.
S. Bruno et al., “Mesenchymal stem cell-derived microvesicles protect against acute tubular injury,” J. Am. Soc. Nephrol., vol. 20, no. 5, pp. 1053–1067, May 2009, doi: 10.1681/ASN.2008070798.
C. Théry et al., “Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines,” J. Extracell. Vesicles, vol. 7, no. 1, p. 1535750, Dec. 2018, doi: 10.1080/20013078.2018.1535750.
S. I. Ohno, G. P. C. Drummen, and M. Kuroda, “Focus on Extracellular Vesicles: Development of Extracellular Vesicle-Based Therapeutic Systems,” Int. J. Mol. Sci. 2016, Vol. 17, Page 172, vol. 17, no. 2, p. 172, Feb. 2016, doi: 10.3390/IJMS17020172.
J. F. Nabhan, R. Hu, R. S. Oh, S. N. Cohen, and Q. Lu, “Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein,” Proc. Natl. Acad. Sci. U. S. A., vol. 109, no. 11, pp. 4146–4151, Mar. 2012, doi: 10.1073/PNAS.1200448109.
Q. Wang, J. Yu, T. Kadungure, J. Beyene, H. Zhang, and Q. Lu, “ARMMs as a versatile platform for intracellular delivery of macromolecules,” Nat. Commun., vol. 9, no. 1, Dec. 2018, doi: 10.1038/S41467-018- 03390-X.
D. Burger, S. Schock, C. S. Thompson, A. C. Montezano,A. M. Hakim, and R. M. Touyz, “Microparticles: biomarkers and beyond,” Clin. Sci. (Lond)., vol. 124, no. 7, pp. 423–441, Apr. 2013, doi: 10.1042/CS20120309.
D. K. Jeppesen et al., “Reassessment of Exosome Composition,” Cell, vol. 177, no. 2, pp. 428-445.e18, Apr. 2019, doi: 10.1016/J.CELL.2019.02.029.
E. Petrovčíková, K. Vičíková, and V. Leksa, “Extracellular vesicles – biogenesis, composition, function, uptake and therapeutic applications,” Biol. 2018 734, vol. 73, no. 4, pp. 437–448, May 2018, doi: 10.2478/S11756- 018-0047-0.
L. Badimon, R. Suades, E. Fuentes, I. Palomo, and T. Padró, “Role of Platelet-Derived Microvesicles As Crosstalk Mediators in Atherothrombosis and Future Pharmacology Targets: A Link between Inflammation, Atherosclerosis, and Thrombosis,” Front. Pharmacol., vol. 7, no. AUG, Aug. 2016, doi: 10.3389/FPHAR.2016.00293.
L. M. Lugo-Gavidia et al., “Role of Microparticles in Cardiovascular Disease: Implications for Endothelial Dysfunction, Thrombosis, and Inflammation,” Hypertension, vol. 77, no. 6, pp. 1825–1844, Jun. 2021, doi: 10.1161/HYPERTENSIONAHA.121.16975.
L. A. Mulcahy, R. C. Pink, and D. R. F. Carter, “Routes and mechanisms of extracellular vesicle uptake,” J. Extracell. vesicles, vol. 3, no. 1, 2014, doi: 10.3402/JEV. V3.24641.
S. Nomura and M. Shimizu, “Clinical significance of procoagulant microparticles,” J. Intensive Care, vol. 3, no. 1, Jan. 2015, doi: 10.1186/S40560-014-0066-Z.
B. Chyrchel, A. Drożdż, D. Długosz, E. Stȩpień, and A. Surdacki, “Platelet Reactivity And Circulating Platelet-Derived Microvesicles Are Differently Affected By P2Y12 Receptor Antagonists,” Int. J. Med. Sci., vol. 16, no. 2, pp. 264–275, 2019, doi: 10.7150/IJMS.28580.
A. Blann, E. Shantsila, and A. Shantsila, “Microparticles and arterial disease,” Semin. Thromb. Hemost., vol. 35, no. 5, pp. 488–496, 2009, doi: 10.1055/S- 0029-1234144.
J. D. Allbritton-King and G. García-Cardeña, “Endothelial cell dysfunction in cardiac disease: driver or consequence?,” Front. Cell Dev. Biol., vol. 11, 2023, doi: 10.3389/FCELL.2023.1278166.
A. E. Berezin and A. A. Berezin, “Extracellular Endothelial Cell-Derived Vesicles: Emerging Role in Cardiac and Vascular Remodeling in Heart Failure,” Front. Cardiovasc. Med., vol. 7, p. 519297, Apr. 2020, doi: 10.3389/FCVM.2020.00047/BIBTEX.
L. Bernal-Mizrachi et al., “Endothelial microparticles correlate with high-risk angiographic lesions in acute coronary syndromes,” Int. J. Cardiol., vol. 97, no. 3, pp. 439–446, Dec. 2004, doi: 10.1016/j. ijcard.2003.10.029.
D. J. Medina-Leyte, O. Zepeda-García, M. Domínguez-Pérez, A. González-Garrido, T. Villarreal- Molina, and L. Jacobo-Albavera, “Endothelial Dysfunction, Inflammation and Coronary Artery Disease: Potential Biomarkers and Promising Therapeutical Approaches,” Int. J. Mol. Sci. 2021, Vol. 22, Page 3850, vol. 22, no. 8, p. 3850, Apr. 2021, doi: 10.3390/IJMS22083850.
J. D. Allbritton-King and G. García-Cardeña, “Endothelial cell dysfunction in cardiac disease: driver or consequence?,” Front. Cell Dev. Biol., vol. 11, 2023, doi: 10.3389/FCELL.2023.1278166.
Y. Cui et al., “Circulating microparticles in patients with coronary heart disease and its correlation with interleukin-6 and C-reactive protein,” Mol. Biol. Rep., vol. 40, no. 11, pp. 6437–6442, Nov. 2013, doi: 10.1007/ S11033-013-2758-1.
L. M. Lugo-Gavidia et al., “Association of Circulating Platelet Extracellular Vesicles and Pulse Wave Velocity with Cardiovascular Risk Estimation,” Int. J. Mol. Sci., vol. 23, no. 18, p. 10524, Sep. 2022, doi: 10.3390/ IJMS231810524/S1.
D. J. Medina-Leyte, O. Zepeda-García, M. Domínguez-Pérez, A. González-Garrido, T. Villarreal- Molina, and L. Jacobo-Albavera, “Endothelial Dysfunction, Inflammation and Coronary Artery Disease: Potential Biomarkers and Promising Therapeutical Approaches,” Int. J. Mol. Sci. 2021, Vol. 22, Page 3850, vol. 22, no. 8, p.3850, Apr. 2021, doi: 10.3390/IJMS22083850.
C. Christersson, Å. Thulin, and A. Siegbahn, “Microparticles during long-term follow-up after acute myocardial infarction,” Thromb. Haemost., vol. 117, no. 08, pp. 1571–1581, 2017, doi: 10.1160/th16-11-0837.
F. Zeiger, S. Stephan, G. Hoheisel, D. Pfeiffer, C. Ruehlmann, and M. Koksch, “P-Selectin expression, platelet aggregates, and platelet-derived microparticle formation are increased in peripheral arterial disease,” Blood Coagul. Fibrinolysis, vol. 11, no. 8, pp. 723–728, 2000, doi: 10.1097/00001721-200012000-00005.
T. Nozaki et al., “Prognostic value of endothelial microparticles in patients with heart failure,” Eur. J. Heart Fail., vol. 12, no. 11, pp. 1223–1228, Nov. 2010, doi: 10.1093/EURJHF/HFQ145.
R. R. Koenen et al., “Platelet-Derived Microvesicles in Cardiovascular Diseases,” vol. 4, 2017, doi: 10.3389/fcvm.2017.00074.
J. Mörtberg, K. Lundwall, F. Mobarrez, H. Wallén, S. H. Jacobson, and J. Spaak, “Increased concentrations of platelet- and endothelial-derived microparticles in patients with myocardial infarction and reduced renal function- a descriptive study,” BMC Nephrol., vol. 20, no. 1, Mar. 2019, doi: 10.1186/S12882-019-1261-X.
E. Zacharia et al., “Cell-Derived Microparticles and Acute Coronary Syndromes: Is there a Predictive Role for Microparticles?,” Curr. Med. Chem., vol. 27, no. 27, pp. 4440–4468, Dec. 2020, doi: 10.2174/0929867327666 191213104841.
C. Jung, P. Sörensson, N. Saleh, H. Arheden, L. Rydén, and J. Pernow, “Circulating endothelial and platelet derived microparticles reflect the size of myocardium at risk in patients with ST-elevation myocardial infarction,” Atherosclerosis, vol. 221, no. 1, pp. 226–231, Mar. 2012, doi: 10.1016/J.ATHEROSCLEROSIS.2011.12.025.
D. Braig et al., “Transitional changes in the CRP structure lead to the exposure of proinflammatory binding sites,” Nat. Commun., vol. 8, Jan. 2017, doi: 10.1038/ NCOMMS14188.
M. Brambilla et al., “Different Contribution of Monocyte- and Platelet-Derived Microvesicles to Endothelial Behavior,” Int. J. Mol. Sci., vol. 23, no. 9, May 2022, doi: 10.3390/IJMS23094811.
Q. Leng et al., “Insights Into Platelet-Derived MicroRNAs in Cardiovascular and Oncologic Diseases: Potential Predictor and Therapeutic Target,” Front. Cardiovasc. Med., vol. 9, p. 879351, Jun. 2022, doi: 10.3389/FCVM.2022.879351/BIBTEX.
C. A. Mavroudis et al., “Microparticles in acute coronary syndrome,” Thromb. Res., vol. 156, pp. 109–116, Aug. 2017, doi: 10.1016/J.THROMRES.2017.06.003.
S. Koganti, D. Eleftheriou, R. Gurung, Y. Hong,P. Brogan, and R. D. Rakhit, “Persistent circulating platelet and endothelial derived microparticle signature may explain on-going pro-thrombogenicity after acute coronary syndrome,” Thromb. Res., vol. 206, pp. 60–65, Oct. 2021, doi: 10.1016/J.THROMRES.2021.07.018.
A. H. Bryk-Wiązania and A. Undas, “Hypofibrinolysis in type 2 diabetes and its clinical implications: from mechanisms to pharmacological modulation,” Cardiovasc. Diabetol. 2021 201, vol. 20, no. 1, pp. 1–16, Sep. 2021, doi: 10.1186/S12933-021- 01372-W.
A. B. Hartopo, I. Puspitawati, P. P. R. Gharini, and B. Y. Setianto, “Platelet microparticle number is associated with the extent of myocardial damage in acute myocardial infarction,” Arch. Med. Sci., vol. 12, no. 3, pp. 529–537, 2016, doi: 10.5114/AOMS.2016.59926.
C. Sun, W. B. Zhao, Y. Chen, and H. Y. Hu, “Higher Plasma Concentrations of Platelet Microparticles in Patients With Acute Coronary Syndrome: A Systematic Review and Meta-analysis,” Can. J. Cardiol., vol. 32, no. 11, p. 1325.e1, Nov. 2016, doi: 10.1016/J.CJCA.2016.02.052.
K. Supriami, I. Puspitawati, D. S. Mayasari, and A. B. Hartopo, “Increased Platelet-derived Microparticles Counts is Correlated with Elevated Blood LDL Cholesterol in Acute Myocardial Infarction,” Indones. Biomed. J., vol. 14, no. 3, pp. 261–8, Sep. 2022, doi: 10.18585/INABJ. V14I3.1892.
E. Zacharia et al., “Plasma signature of apoptotic microvesicles is associated with endothelial dysfunction and plaque rupture in acute coronary syndromes,” J. Mol. Cell. Cardiol., vol. 138, pp. 110–114, Jan. 2020, doi: 10.1016/J.YJMCC.2019.11.153.
A. Awad, I. Ahmed, M. Abdul-Fattah, I. Shalaby, M. Abd El-Hameed, and M. S. Mohamed, “MICROPARTICLES AS A PREDICTIVE BIOMARKER IN ACUTE MYOCARDIAL INFARCTION,” Al-Azhar Med. J., vol. 50, no. 3, pp. 2185–2200, Jul. 2021, doi: 10.21608/AMJ.2021.178680.
S. Godo and H. Shimokawa, “Endothelial Functions,” Arterioscler. Thromb. Vasc. Biol., vol. 37, no. 9, pp. e108–e114, Sep. 2017, doi: 10.1161/ ATVBAHA.117.309813.
P. Collins, A. Maas, M. Prasad, L. Schierbeck, and A. Lerman, “Endothelial Vascular Function as a Surrogate of Vascular Risk and Aging in Women,” Mayo Clin. Proc., vol. 95, no. 3, pp. 541–553, 2020, doi: 10.1016/j. mayocp.2019.07.001.
T. Toya et al., “Prognostic impact and clinical outcomes of coronary flow reserve and hyperaemic microvascular resistance: CFR, HMR, and MACE,” EuroIntervention, vol. 17, no. 7, p. 569, Sep. 2021, doi: 10.4244/EIJ-D-20-00853.
K. Taguchi, M. Hida, H. Narimatsu, T. Matsumoto, and T. Kobayashi, “Glucose and angiotensin II-derived endothelial extracellular vesicles regulate endothelial dysfunction via ERK1/2 activation,” Pflugers Arch., vol. 469, no. 2, pp. 293–302, Feb. 2017, doi: 10.1007/S00424- 016-1926-2.
A. Osman et al., “Endoplasmic Reticulum (ER) Stress-Generated Extracellular Vesicles (Microparticles) Self-Perpetuate ER Stress and Mediate Endothelial Cell Dysfunction Independently of Cell Survival,” Front.
Cardiovasc. Med., vol. 7, Dec. 2020, doi: 10.3389/ FCVM.2020.584791.
F. Buffolo, S. Monticone, G. Camussi, and E. Aikawa, “Role of Extracellular Vesicles in the Pathogenesis of VascularDamage,” Hypertens. (Dallas, Tex. 1979), vol. 79, no. 5, p. 863, May 2022, doi: 10.1161/ HYPERTENSIONAHA.121.17957.
C. M. Boulanger, “Microparticles, vascular function and hypertension,” Curr. Opin. Nephrol. Hypertens., vol. 19, no. 2, pp. 177–180, Mar. 2010, doi: 10.1097/MNH.0B013E32833640FD.
R. A. Preston et al., “Effects of Severe Hypertension on Endothelial and Platelet Microparticles,” Hypertension, vol. 41, no. 2, pp. 211–217, Feb. 2003, doi: 10.1161/01.HYP.0000049760.15764.2D.
T. Helbing, C. Olivier, C. Bode, M. Moser, and P. Diehl, “Role of microparticles in endothelial dysfunction and arterial hypertension,” World J. Cardiol., vol. 6, no. 11, p. 1135, Nov. 2014, doi: 10.4330/WJC.V6.I11.1135.
M. T. K. Zaldivia et al., “Successful renal denervation decreases the platelet activation status in hypertensive patients,” Cardiovasc. Res., vol. 116, no. 1, pp. 202–210, Jan. 2020, doi: 10.1093/CVR/CVZ033.
J. N. Barnes et al., “Cerebrovascular Reactivity and Vascular Activation in Postmenopausal Women With Histories of Preeclampsia,” Hypertens. (Dallas, Tex. 1979), vol. 71, no. 1, pp. 110–117, Jan. 2018, doi: 10.1161/ HYPERTENSIONAHA.117.10248.
S. I. Gilani, T. L. Weissgerber, V. D. Garovic, and M. Jayachandran, “Preeclampsia and Extracellular Vesicles,” Curr. Hypertens. Rep., vol. 18, no. 9, Sep. 2016, doi: 10.1007/S11906-016-0678-X.
N. C. Bacha et al., “Treprostinil treatment decreases circulating platelet microvesicles and their procoagulant activity in pediatric pulmonary hypertension,” Pediatr. Pulmonol., vol. 54, no. 1, pp. 66–72, Jan. 2019, doi: 10.1002/PPUL.24190.
J. Rosińska, M. Łukasik, and W. Kozubski, “The Impact of Vascular Disease Treatment on Platelet-Derived Microvesicles,” Cardiovasc. drugs Ther., vol. 31, no. 5–6, pp. 627–644, Dec. 2017, doi: 10.1007/S10557-017-6757-7.
F. Santilli, M. Marchisio, P. Lanuti, A. Boccatonda,S. Miscia, and G. Davl, “Microparticles as new markers of cardiovascular risk in diabetes and beyond,” Thromb. Haemost., vol. 116, no. 2, pp. 220–234, Aug. 2016, doi: 10.1160/TH16-03-0176.
A. Extracellular Vesicles, T. in Atrial, A. E. Berezin, and A. A. Berezin, “Extracellular Vesicles and Thrombogenicity in Atrial Fibrillation,” Int. J. Mol. Sci. 2022, Vol. 23, Page 1774, vol. 23, no. 3, p. 1774, Feb. 2022, doi: 10.3390/IJMS23031774.
H. Wang et al., “The microvesicle/CD36 complex triggers a prothrombotic phenotype in patients with non‐ valvular atrial fibrillation,” J. Cell. Mol. Med., vol. 24, no. 13, p. 7331, Jul. 2020, doi: 10.1111/JCMM.15311.
D. Patel et al., “Biomarkers of Thrombo- Inflammatory Responses in Pulmonary Embolism Patients With Pre-Existing Versus New-Onset Atrial Fibrillation,” Clin. Appl. Thromb. Hemost., vol. 27, 2021, doi: 10.1177/10760296211014964.
B. Ibanez et al., “2017 ESC Guidelines for the management of acute myocardial infarction in patients presenting with ST-segment elevation: The Task Force for the management of acute myocardial infarction in patients presenting with ST-segment elevation of the European Society of Cardiology (ESC),” Eur. Heart J., vol. 39, no. 2, pp. 119– 177, Jan. 2018, doi: 10.1093/EURHEARTJ/EHX393.
A. Lenart-Migdalska, L. Drabik, M. Kaźnica- Wiatr, L. Tomkiewicz-Pająk, P. Podolec, and M. Olszowska, “Flow Cytometric Assessment of Endothelial and Platelet Microparticles in Patients With Atrial Fibrillation Treated With Dabigatran,” Clin. Appl. Thromb., vol. 26, Nov. 2020, doi: 10.1177/1076029620972467/ASSET/IMAGES/ LARGE/10.1177_1076029620972467-FIG2.JPEG.
R. C. F. Duarte et al., “Thrombin Generation and other hemostatic parameters in patients with atrial fibrillation in use of warfarin or rivaroxaban,” J. Thromb. Thrombolysis, vol. 51, no. 1, pp. 47–57, Jan. 2021, doi: 10.1007/S11239-020-02126-3/METRICS.
L. Weiss et al., “Nonvalvular atrial fibrillation patients anticoagulated with rivaroxaban compared with warfarin exhibit reduced circulating extracellular vesicles with attenuated pro‐inflammatory protein signatures,” J. Thromb. Haemost., vol. 19, no. 10, pp. 2583–2595, Oct. 2021, doi: 10.1111/JTH.15434.
H. Azzam and M. Zagloul, “Elevated platelet microparticle levels in valvular atrial fibrillation,” Hematology, vol. 14, no. 6, pp. 357–360, Dec. 2009, doi: 10.1179/102453309X12473408860460.
C. Herrera Sikldy et al., “Cellular damage, platelet activation, and inflammatory response after pulmonary vein isolation: A randomized study comparing radiofrequency ablation with cryoablation,” Hear. Rhythm, vol. 9, no. 2, pp. 189–196, Feb. 2012, doi: 10.1016/J.HRTHM.2011.09.017.
L. Jesel et al., “Do Atrial Differences in Endothelial Damage, Leukocyte and Platelet Activation, or Tissue Factor Activity Contribute to Chamber-Specific Thrombogenic Status in Patients with Atrial Fibrillation?,” J. Cardiovasc. Electrophysiol., vol. 25, no. 3, pp. 266–270, Mar. 2014, doi: 10.1111/JCE.12312.
X.-Z. Zhang et al., “CD62P and GP IIb/IIIa in hypercoagulation after RFCA,” 2016.
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