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A Meta-Analysis of Circulating Microvesicles in Patients with Myocardial Infarction

Abstract

Background:

Cell-derived microvesicles (MVs) are vesicles released from activated or apoptotic cells. However, the levels of MVs in myocardial infarction have been found inconsistent in researches.

Objective:

To assess the association between MVs and myocardial infarction by conducting a meta-analysis.

Methods:

A systematic literature search on PubMed, Embase, Cochran, Google Scholar electronic database was conducted. Comparison of the MVs levels between myocardial infarction patients and healthy persons were included in our study. Standard Mean Difference (SMD) and 95% confidence interval (CI) in groups were calculated and meta-analyzed.

Results:

11 studies with a total of 436 participants were included. Compared with the health persons, AMVs [SMD = 3.65, 95% CI (1.03, 6.27)], PMVs [SMD = 2.88, 95% CI (1.82, 3.93),] and EMVs [SMD = 2.73, 95% CI (1.13, 4.34)], levels were higher in patients with myocardial infarction. However, LMVs levels [SMD = 0.73, 95% CI (-0.57, 2.03)] were not changed significantly in patients with myocardial infarction.

Conclusions:

AMVs, PMVs and EMVs might be potential biomarkers for myocardial infarction.

Keywords:
Myocardiaol Infarction; Biomarkers; Cell-Derived Microparticles; Annexion A5; Blood Platelets; Leukocytes; Endothelium

Resumo

Fundamentos:

As microvesículas derivadas de células (MVs) são vesículas liberadas de células ativadas ou apoptóticas. No entanto, os níveis de MVs no infarto do miocárdio foram encontrados inconsistentes nas pesquisas.

Objetivo:

Avaliar a associação entre MV e infarto do miocárdio por meio de uma meta-análise.

Métodos:

Foi realizada uma pesquisa sistemática na literatura em PubMed, Embase, Cochran e no banco de dados eletrônico do Google Scholar. Uma comparação dos níveis de MV entre pacientes com infarto do miocárdio e pessoas saudáveis foi incluída no nosso estudo. A Diferença Média Padrão (DMP) e o intervalo de confiança (IC) de 95% nos grupos foram calculadas e meta-analisadas.

Resultados:

Foram incluídos 11 estudos com um total de 436 participantes. Em comparação com as pessoas saudáveis, as MVA [DMP = 3,65, IC 95% (1,03, 6,27)], MVPs [DMP = 2,88, IC 95% (1,82, 3,93)] e MVEs [DMP = 2,73, IC 95% (1,13, 4.34)], foram maiores em pacientes com infarto do miocárdio. No entanto, os níveis de MVL [DMP = 0,73, IC 95% (-0,57, 2,03)] não foram alterados significativamente em pacientes com infarto do miocárdio.

Conclusões:

MVAs, MVPs e MVEs podem ser biomarcadores potenciais para o infarto do miocárdio.

Palavras-chave:
Infarto do Miocárdio; Micropartículas Derivadas de Células; Anexina A5; Plaquetas; Leucócitos; Endotélio

Introduction

Ischemic Heart Disease (IHD) is one of the cardiovascular diseases, which impairs human health.11 Dahlof B. Cardiovascular disease risk factors: epidemiology and risk assessment. Am J Cardiol. 2010;105(1 Suppl):3A-9A. Atherothrombosis, endothelial dysfunction and cell apoptosis are on the pathologic basis in these diseases. The relevant studies in this area have suggested that cell-derived microvesicles (MVs) are related with platelet activation, endothelial damage and inflammation associated with the existence of cardiovascular risk factors.22 Mastronardi ML, Mostefai HA, Meziani F, Martinez MC, Asfar P, Andriantsitohaina R. Circulating microparticles from septic shock patients exert differential tissue expression of enzymes related to inflammation and oxidative stress. Crit Care Med 2011;39(7):1739-48.

3 Boulanger CM, Scoazec A, Ebrahimian T, Henry P, Mathieu E, Tedgui A, et al. Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction. Circulation. 2001;104(22):2649-52.
-44 Mezentsev A, Merks RM, O'Riordan E, Chen J, Mendelev N, Goligorsky MS, et al. Endothelial microparticles affect angiogenesis in vitro: role of oxidative stress. Am J Physiol Heart Circ Physiol. 2005;289(3):H1106-14. Since they are involved in the pathophysiologic process of diseases, attention has being focused on the relationship between MVs and myocardial infarction (MI).55 Bernal-Mizrachi L, Jy W, Jimenez JJ, Pastor J, Mauro LM, Horstman LL, et al. High levels of circulating endothelial microparticles in patients with acute coronary syndromes. Am Heart J. 2003;145(6):962-70.

6 Bulut D, Maier K, Bulut-Streich N, Borgel J, Hanefeld C, Mugge A. Circulating endothelial microparticles correlate inversely with endothelial function in patients with ischemic left ventricular dysfunction. J Card Fail. 2008;14(4):336-40.

7 Zielinska M, Koniarek W, Goch JH, Cebula B, Tybura M, Robak T, Smolewski P. Circulating endothelial microparticles in patients with acute myocardial infarction. Kardiol Pol. 2005;62(6):531-42.
-88 van der Zee PM, Biro E, Ko Y, de Winter RJ, Hack CE, Sturk A, Nieuwland R. P-selectin- and CD63-exposing platelet microparticles reflect platelet activation in peripheral arterial disease and myocardial infarction. Clin Chem. 2006;52(4):657-64. Increasing evidences imply that MVs might be considered as novel biomarkers or mediators helpful in understanding the mechanisms of cardiovascular diseases.

MVs are used to describe a population of sub-cellular vesicles released from plasma membrane during cell activation or apoptosis and identified by size range from 100 nm to 1.0 µm in diameter. MVs constitute a heterogeneous population, different in cellular origin, numbers, size, antigenic composition, and functional properties. Alterations in the amounts of different cell-derived MVs may provide information on the pathophysiologic changes. Although many studies have shown that myocardial infarction is associated with MVs, the information obtained shows heterogeneous result, with a high variation regarding MVs size, MVs type, MVs levels, inclusion criteria and methods. Thus, we performed a meta-analysis of the changes of Annexin V positive MVs (AMVs), platelet MVs (PMVs), endothelial MVs (EMVs) and leukocytes MVs (LMVs) in patients with myocardial infarction and healthy persons.

Methods

Data Sources and Searches

We searched the databases of MEDLINE (pubmed), Embase, Cochrane and Google Scholar electronic database for articles from 2000 to 2013. All searches were applied with the following medical subject headings: “myocardial infarction”, “primary percutaneous coronary intervention”, “stenting”, “balloon angioplasty”, “acute coronary syndrome” or “coronary ischemia”, “microparticles”, “cell-derived microparticles”, “circulating microparticles”, “microvesicles”. These searches were restricted to publications limited to research on humans. A manual search for references cited in the published studies and relevant review articles was also performed to identify additionally suitable investigations for our purpose. For unpublished and published studies that were not exhaustively disclosed, the attempt through e-mail was made to contact principal investigators in order to retrieve missing data. Finally, well-known experts in this area were contacted to ensure that all relevant data were captured.

Study Selection

Two of us performed the identification of relevant abstracts and the selection of studies based on the criteria described below independently, and a third investigator resolved any discrepancy. We selected studies comparing the levels of diverse MVs: total, platelet-, endothelial-, leukocyte-derived between healthy persons and patients with myocardial infarction.

Studies were included if they met the following criteria: (i) Study entitled circulating MVs correlated with MI; (ii) Design of study was case-control study or cohort study; (iii) The MI as a research subgroup independently extract relevant information MI. We excluded the following: (i) Review; (ii) Not full text, only a summary; (iii) Animal testing.

Data Extraction and Synthesis

We extracted information including study and population characteristics, sample size, study design, and outcomes relevant to this study. Means and standard deviations of MVs levels were extracted. When an article complied with the inclusion criteria but lacked information on parameters for analysis, or when outcomes were reported but not related to myocardial infarction, we contacted the authors to obtain raw data. The quality of studies was assessed using the Downs and Black checklist.

Statistical Analysis

The data was analyzed using RevMan 5.0 statistical software provided by the Cochrane Collaboration analyzed. SMD and 95% CI were used as summary estimates. The presence of heterogeneity between studies was tested with the χ² test for heterogeneity and the I² statistic. Heterogeneity was significant when p< 0.05 or I² was more than 50%. A random-effects model was used in all analyses to test the stability of the results to the choice of the statistical model. If significant heterogeneity, results of the random-effects model are used. We defined a priori sensitivity analysis of high-quality studies for each clinical outcome. The potential for publication bias was evaluated using the funnel plot approach.

Results

Search Results

172 articles identified from MEDLINE (pubmed), Embase, Cochrane and Google Scholar electronic database were analyzed; and then, 140 were excluded based on title and abstract. After detailed evaluation of potential eligibility, 11 studies met all the inclusion criteria and were retrieved for meta-analysis.99 Cui Y, Zheng L, Jiang M, Jia R, Zhang X, Quan Q, et al. Circulating microparticles in patients with coronary heart disease and its correlation with interleukin-6 and C-reactive protein. Mol Biol Rep. 2013;40(11):6437-42.

10 Min PK, Kim JY, Chung KH, Lee BK, Cho M, Lee DL, et al. Local increase in microparticles from the aspirate of culprit coronary arteries in patients with ST-segment elevation myocardial infarction. Atherosclerosis. 2013;227(2):323-8.

11 Skeppholm M, Mobarrez F, Malmqvist K, Wallen H. Platelet-derived microparticles during and after acute coronary syndrome. Thromb Haemost. 2012;107(6):1122-9.

12 Stepien E, Stankiewicz E, Zalewski J, Godlewski J, Zmudka K, Wybranska I. Number of microparticles generated during acute myocardial infarction and stable angina correlates with platelet activation. Arch Med Res. 2012;43(1):31-5.

13 Leong HS, Podor TJ, Manocha B, Lewis JD. Validation of flow cytometric detection of platelet microparticles and liposomes by atomic force microscopy. J Thromb Haemost. 2011;9(12):2466-76.

14 Del Turco S, Basta G, Lazzerini G, Evangelista M, Rainaldi G, Tanganelli P, et al. Effect of the administration of n-3 polyunsaturated fatty acids on circulating levels of microparticles in patients with a previous myocardial infarction. Haematologica. 2008;93(6):892-9.

15 Morel O, Jesel L, Freyssinet JM, Toti F. Elevated levels of procoagulant microparticles in a patient with myocardial infarction, antiphospholipid antibodies and multifocal cardiac thrombosis. Thromb J. 2005;3:15.

16 Tan KT, Tayebjee MH, Macfadyen RJ, Lip GY, Blann AD. Elevated platelet microparticles in stable coronary artery disease are unrelated to disease severity or to indices of inflammation. Platelets. 2005;16(6):368-71.

17 Morel O, Hugel B, Jesel L, Mallat Z, Lanza F, Douchet MP, et al. Circulating procoagulant microparticles and soluble GPV in myocardial infarction treated by primary percutaneous transluminal coronary angioplasty: a possible role for GPIIb-IIIa antagonists. J Thromb Haemost. 2004;2(7):1118-26.

18 Matsumoto N, Nomura S, Kamihata H, Kimura Y, Iwasaka T. Increased level of oxidized LDL-dependent monocyte-derived microparticles in acute coronary syndrome. Thromb Haemost. 2004;91(1):146-54.
-1919 Michelsen AE, Brodin E, Brosstad F, Hansen JB. Increased level of platelet microparticles in survivors of myocardial infarction. Scand J Clin Lab Invest. 2008;68(5):386-92. The trial flowchart is summarized in Figure 1.

Figure 1
Flow diagram of search strategy and study selection.

Baseline Characteristics of the studies

The characteristics of all included studies are presented in Table 1. These studies were published from 2004 to 2013. Sample size ranged from 5 to 61. A total of 436 participants (186 healthy controls and 250 MI patients) were included. Among these studies, the results of MVs were expressed differently. Six reports were expressed as numbers of MVs in plasma per microliter, milliliter and liter. Three reports were expressed as PS eq (phosphatidylserine equivalents), one report was expressed as numbers of MVs in platelet count, and one report was expressed as plasma concentrations of MVs. There were four reports only report the median, range and the size of the trial. In order to estimate the mean and the variance in these articles, we used the number of sample and elementary inequalities.2020 Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005;5:13.

Table 1
Characteristic of included studies

Quality Index

The majority of studies scored highly on reporting of the interventions used and outcome measures. Only one report scored lowly on the small sample size. The average score of all studies was 15.8 (Table 2).

Table 2
Quality Index of included studies

Annexin V+ microvesicles in health control and patients with myocardial infarction

Four of the eleven studies showed changes in AMVs levels between patients with myocardial infarction and healthy controls. In three of these reports, AMVs levels in patients with myocardial infarction were higher than healthy controls. Only in one study, patients with myocardial infarction did not differ from healthy controls concerning AMVs levels. When results of all studies were combined, there was a significant difference between groups with higher AMVs levels in patients with a myocardial infarction [SMD = 3.65, 95% CI (1.03, 6.27), Z = 2.73 (p < 0.00001; Figure 2A)]. Furthermore, there was significant statistical heterogeneity across studies (χ2= 95.64, df = 3, p < 0.00001, I2= 97%). As shown in Figure 2B, no publication bias was found.

Figure 2
The forest plot (A) and funnel plot (B) of meta-analysis of Annexin V+ microvesicles in myocardial infarction.

Platelet microvesicles in health control and patients with myocardial infarction

All of eleven studies found PMVs levels varied between myocardial infarction patients and healthy controls. Nine studies reported that level of PMVs were higher in MI patients, whereas the other studies showed no difference in groups. Combining the results of all studies, it was significantly increased in myocardial infarction patients [SMD = 2.88, 95% CI (1.82, 3.93), Z = 5.35 (p < 0.00001; Figure 3A)]. There was also significant statistical heterogeneity across studies (χ2= 235.02, df = 10, p < 0.00001, I2= 96%). As shown in Figure 3B, a little publication bias was found.

Figure 3
The forest plot (A) and funnel plot (B) meta-analysis of platelet microvesicles in myocardial infarction.

Endothelial microvesicles in health control and patients with myocardial infarction

Six of the eleven studies reported alternation in EMVs levels between the two groups. Four reports concluded that a proportion of MI patients have elevated EMVs levels. But the other studies showed no significant difference. Combining all results of those studies, MI patients had a higher level of EMVs. [SMD = 2.73, 95% CI (1.13, 4.34), Z = 3.33 (p = 0.0009; Figure 4A)]. The statistical heterogeneity was significant across studies (χ2= 155.28, df = 6, p < 0.00001, I2= 96%). As shown in Figure 4B, no publication bias was found.

Figure 4
The forest plot (A) and funnel plot (B) meta-analysis of endothelial microvesicles in myocardial infarction.

Leukocyte microvesicles in health control and patients with myocardial infarction

Five of the eleven studies exhibited differences in LMVs levels between myocardial infarction patients and health controls. Four reports showed that LMVs levels in myocardial infarction patients were higher than health controls. The finding of one report was, however, in the opposite direction, with patients having significantly lower LMVs levels than controls. When results of all studies were combined, there was no significant difference between the two groups [SMD = 0.73, 95% CI (-0.57, 2.03), Z = 1.11 (p = 0.27; Figure 5A)]. There was also significant statistical heterogeneity across studies (χ2= 90.69, df = 4, p < 0.00001, I2= 96%). As shown in Figure 5B, no publication bias was found.

Figure 5
The forest plot (A) and funnel plot (B) meta-analysis of leukocyte microvesicles in myocardial infarction.

Discussion

We conducted an exhaustive search to identify studies related to our question and gave the most comprehensive overview of MVs in MI to date. Systematic methods were applied to reduce bias in the identification of studies, data extraction and synthesis, and appraisal of study quality. This meta-analysis showed that higher level of AMVs, PMVs and EMVs in peripheral blood might be associated with patients with MI, indicating that these MVs may be helpful in the diagnosis of MI. However, the result of LMVs was negative.

Microvesicles (MVS) or microparticles (MPS) have relationship not only with inflamatory and thrombotic processes but with tissue regenerative process and angiogenesis, which can be a protective function. In addition, MVS can be a signaler of homeostasis balancing cell stimulus and apoptosis. Diabetic patients have increased release of MVS and this can be a biomarker of diabetic progression by retinopathy. Pharmacologic approach is helpful because of endothelial dysfunction. Renin-angiotensin system blocker and calcium channel blocker may be good options in type 2 diabetes mellitus.2121 França CN, Izar MC, Amaral JB, Tegani DM, Fonseca FA. Microparticles as potential biomarkers of cardiovascular disease. Arq Bras Cardiol. 2015;104(2):169-74. Pinheiro et al.2222 Pinheiro LF, França CN, Izar MC, Barbosa SP, Bianco HT, Kasmas SH, et al. Pharmacokinetic interactions between clopidogrel and rosuvastatin: effects on vascular protection in subjects with coronary heart disease. Int J Cardiol. 2012;158(1):125-9. have assessed the effect of the antiplatelet drug clopidogrel in association or not with rosuvastatin (40 mg) on the levels of EMP and PMP in patients with stable coronary disease on statins for at least three months. Those authors have identified an increase in the levels of PMP after suspension of rosuvastatina and maintenance of only clopidogrel for four weeks and a tendency towards greater release of EMP in those patients. They have suggested that an increase in the apoptosis of platelets occurred, and that rosuvastatin might have a protective effect on the endothelium when associated with clopidogrel.2222 Pinheiro LF, França CN, Izar MC, Barbosa SP, Bianco HT, Kasmas SH, et al. Pharmacokinetic interactions between clopidogrel and rosuvastatin: effects on vascular protection in subjects with coronary heart disease. Int J Cardiol. 2012;158(1):125-9. In a similar study, França et al.2323 França CN, Pinheiro LF, Izar MC, Brunialti MK, Salomão R, Bianco HT, et al. Endothelial progenitor cell mobilization and platelet microparticle release are influenced by clopidogrel plasma levels in stable coronary artery disease. Circ J. 2012;76(3):729-36. have assessed the influence of atorvastatin (80 mg) in association or not with clopidogrel in patients with stable coronary disease. Those authors have suggested higher vascular stability promoted by atorvastatin after identifying an inverse relationship between the plasma concentration of atorvastatin and the levels of PMP.2323 França CN, Pinheiro LF, Izar MC, Brunialti MK, Salomão R, Bianco HT, et al. Endothelial progenitor cell mobilization and platelet microparticle release are influenced by clopidogrel plasma levels in stable coronary artery disease. Circ J. 2012;76(3):729-36.

MVs have a bilayered phospholipid membrane.2424 Morel O, Jesel L, Freyssinet JM, Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol. 2011;31(1):15-26. The presence of externalized PS on MVs surfaces indicates an altered phospholipid distribution profile compared to the plasma membrane of a resting mammalian cell. Additionally, the molecules present in the outer surface, once defined, provide accessible markers for detecting and characterizing MVs using molecular probes.2525 Gyorgy B, Szabo TG, Pasztoi M, Pal Z, Misjak P, Aradi B, et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci. 2011;68(16):2667-88. AMVs express phosphatidylserine (PS) in their surface and are currently defined as apoptotic MVs. It is shown that AMVs levels were significantly higher in patients with MI than healthy controls. It is likely due to the myocardial ischemia and hypoxia which make cell apoptosis, thereby releasing large amounts of AMVs. In each case, the variation in AMVs levels shows that cell apoptosis occurs. A in vitro study uncovered that MVs extracted from the circulating blood of a patient with myocardial infarction and applied to the isolated aortic rings of a rat, led to severely damage of endothelial function.2626 Boulanger CM, Scoazec A, Ebrahimian T, Henry P, Mathieu E, Tedgui A, et al. Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction. Circulation. 2001;104(22):2649-52. Thus, the high level of AMVs and their effect may be the cause the further progression of myocardial infarction.

PMVs are defined as membranous vesicles derived from the platelet which are defined and identified by surface molecules CD62P and CD63.2727 Zwicker JI, Lacroix R, Dignat-George F, Furie BC, Furie B. Measurement of platelet microparticles. Methods Mol Biol. 2012;788:127-39. With the ability to bind coagulation factors VIII, Va, and IX, PMVs not only reflect platelet activation but also contribute to the activation of the coagulation pathway and thrombogenesis.2828 Morel O, Morel N, Freyssinet JM, Toti F. Platelet microparticles and vascular cells interactions: a checkpoint between the haemostatic and thrombotic responses. Platelets. 2008;19(1):9-23.-2929 Sinauridze EI, Kireev DA, Popenko NY, Pichugin AV, Panteleev MA, Krymskaya OV, et al. Platelet microparticle membranes have 50- to 100-fold higher specific procoagulant activity than activated platelets. Thromb Haemost. 2007;97(3):425-34. It was found that there was high level of PMVs in the peripheral blood of the MI patients. The main cause may be the change of blood flow shear force induced by pathological changes in the blood vessels of the MI patients. These changes promote the aggregation and activation of platelets, thereby leading to the generation of a large number of PMVs. This suggests that increased PMVs may be further expanded by the coagulation reaction of the blood vessels in the MI patients.

The dysfunction of endothelial cells plays an important role in the MI. EMVs are sub-cellular membrane vesicles released from endothelial cell during activation or apoptosis.3030 Dignat-George F, Boulanger CM. The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol. 2011;31(1):27-33. EMVs carry specific markers which originate from the maternal cells, including CD31, CD51, CD54, CD62E, CD105, CD144 or CD146. It is found that EMVs were significantly higher in the MI group. His could be because of the dysfunction of endothelial cells, which release lots of EMVs into the blood. When the EMVs were incubated with human umbilical vein endothelial cells (HUVECs), endothelial cells proliferation decreased and their apoptosis increased, then the capacity of angiogenesis went down dramatically.3131 Mezentsev A, Merks RM, O'Riordan E, Chen J, Mendelev N, Goligorsky MS, et al. Endothelial microparticles affect angiogenesis in vitro: role of oxidative stress. Am J Physiol Heart Circ Physiol. 2005;289(3):H1106-14. The high level of EMVs is considered as a cause to worsen the condition by inducing endothelial dysfunction on the MI states.

Unlike the single source of EMVs or PMVs, LMVs may originate from neutrophils, monocytes/macrophages, and lymphocytes.3232 Angelillo-Scherrer A. Leukocyte-derived microparticles in vascular homeostasis. Circ Res. 2012;110(2):356-69. They also express markers from their parental cells. Various antibodies were used to capture LMVs, including CD4, CD14, CD11a and so on. Combined with the clinical results, this meta-analysis found that there was no significant variation in LMVs’ level between the health controls and patients with MI. But the studies that used CD4 and CD14 antibodies, shown LMVs’ level was higher in patients with MI. When CD11a antibody was used, a muddle of contradictory results was found. Therefore, additional studies are needed to further investigate the level of LMVs in MI. Meanwhile, LMVs measurement still requires elaborate techniques because of its lack of standardization.

Limitations of this meta-analysis must be considered. First, the quality of individual studies was not always optimal, as shown by the general lack of information on some studies. So we used simple and elementary inequalities in order to estimate the mean and the variance for such studies. But it is not exactly enough. Second, there is heterogeneity of SMD across studies, corresponding in part to heterogeneity in study definitions. Third, although the quality of included studies was judged overall to be adequate, the findings in the present study need to be interpreted with caution, given that not all studies reported on potential confounding variables and their adjustment in analyses. Finally, meta-analytic data also need to be cautiously interpreted, given the substantial heterogeneity among studies.

Conclusion

This meta-analysis showed that higher level of AMVs, PMVs and EMVs in peripheral blood may be associated with patients with MI, indicating that these MVs may be helpful in the diagnosis of MI. However, the result of LMVs was negative.

  • Sources of Funding
    This study was funded by National Natural Science Foundation of China through grant n°. 81602496; Science and Technology Foundation of Administration of Traditional Chinese Medicine of Tianjin, China, nos 2015022 and 13047; Science and Technology Foundation of Tianjin Municipal Commission of Health and Family planning, n°. 2013KZ054.
  • Study Association
    This study is not associated with any thesis or dissertation work.

References

  • 1
    Dahlof B. Cardiovascular disease risk factors: epidemiology and risk assessment. Am J Cardiol. 2010;105(1 Suppl):3A-9A.
  • 2
    Mastronardi ML, Mostefai HA, Meziani F, Martinez MC, Asfar P, Andriantsitohaina R. Circulating microparticles from septic shock patients exert differential tissue expression of enzymes related to inflammation and oxidative stress. Crit Care Med 2011;39(7):1739-48.
  • 3
    Boulanger CM, Scoazec A, Ebrahimian T, Henry P, Mathieu E, Tedgui A, et al. Circulating microparticles from patients with myocardial infarction cause endothelial dysfunction. Circulation. 2001;104(22):2649-52.
  • 4
    Mezentsev A, Merks RM, O'Riordan E, Chen J, Mendelev N, Goligorsky MS, et al. Endothelial microparticles affect angiogenesis in vitro: role of oxidative stress. Am J Physiol Heart Circ Physiol. 2005;289(3):H1106-14.
  • 5
    Bernal-Mizrachi L, Jy W, Jimenez JJ, Pastor J, Mauro LM, Horstman LL, et al. High levels of circulating endothelial microparticles in patients with acute coronary syndromes. Am Heart J. 2003;145(6):962-70.
  • 6
    Bulut D, Maier K, Bulut-Streich N, Borgel J, Hanefeld C, Mugge A. Circulating endothelial microparticles correlate inversely with endothelial function in patients with ischemic left ventricular dysfunction. J Card Fail. 2008;14(4):336-40.
  • 7
    Zielinska M, Koniarek W, Goch JH, Cebula B, Tybura M, Robak T, Smolewski P. Circulating endothelial microparticles in patients with acute myocardial infarction. Kardiol Pol. 2005;62(6):531-42.
  • 8
    van der Zee PM, Biro E, Ko Y, de Winter RJ, Hack CE, Sturk A, Nieuwland R. P-selectin- and CD63-exposing platelet microparticles reflect platelet activation in peripheral arterial disease and myocardial infarction. Clin Chem. 2006;52(4):657-64.
  • 9
    Cui Y, Zheng L, Jiang M, Jia R, Zhang X, Quan Q, et al. Circulating microparticles in patients with coronary heart disease and its correlation with interleukin-6 and C-reactive protein. Mol Biol Rep. 2013;40(11):6437-42.
  • 10
    Min PK, Kim JY, Chung KH, Lee BK, Cho M, Lee DL, et al. Local increase in microparticles from the aspirate of culprit coronary arteries in patients with ST-segment elevation myocardial infarction. Atherosclerosis. 2013;227(2):323-8.
  • 11
    Skeppholm M, Mobarrez F, Malmqvist K, Wallen H. Platelet-derived microparticles during and after acute coronary syndrome. Thromb Haemost. 2012;107(6):1122-9.
  • 12
    Stepien E, Stankiewicz E, Zalewski J, Godlewski J, Zmudka K, Wybranska I. Number of microparticles generated during acute myocardial infarction and stable angina correlates with platelet activation. Arch Med Res. 2012;43(1):31-5.
  • 13
    Leong HS, Podor TJ, Manocha B, Lewis JD. Validation of flow cytometric detection of platelet microparticles and liposomes by atomic force microscopy. J Thromb Haemost. 2011;9(12):2466-76.
  • 14
    Del Turco S, Basta G, Lazzerini G, Evangelista M, Rainaldi G, Tanganelli P, et al. Effect of the administration of n-3 polyunsaturated fatty acids on circulating levels of microparticles in patients with a previous myocardial infarction. Haematologica. 2008;93(6):892-9.
  • 15
    Morel O, Jesel L, Freyssinet JM, Toti F. Elevated levels of procoagulant microparticles in a patient with myocardial infarction, antiphospholipid antibodies and multifocal cardiac thrombosis. Thromb J. 2005;3:15.
  • 16
    Tan KT, Tayebjee MH, Macfadyen RJ, Lip GY, Blann AD. Elevated platelet microparticles in stable coronary artery disease are unrelated to disease severity or to indices of inflammation. Platelets. 2005;16(6):368-71.
  • 17
    Morel O, Hugel B, Jesel L, Mallat Z, Lanza F, Douchet MP, et al. Circulating procoagulant microparticles and soluble GPV in myocardial infarction treated by primary percutaneous transluminal coronary angioplasty: a possible role for GPIIb-IIIa antagonists. J Thromb Haemost. 2004;2(7):1118-26.
  • 18
    Matsumoto N, Nomura S, Kamihata H, Kimura Y, Iwasaka T. Increased level of oxidized LDL-dependent monocyte-derived microparticles in acute coronary syndrome. Thromb Haemost. 2004;91(1):146-54.
  • 19
    Michelsen AE, Brodin E, Brosstad F, Hansen JB. Increased level of platelet microparticles in survivors of myocardial infarction. Scand J Clin Lab Invest. 2008;68(5):386-92.
  • 20
    Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005;5:13.
  • 21
    França CN, Izar MC, Amaral JB, Tegani DM, Fonseca FA. Microparticles as potential biomarkers of cardiovascular disease. Arq Bras Cardiol. 2015;104(2):169-74.
  • 22
    Pinheiro LF, França CN, Izar MC, Barbosa SP, Bianco HT, Kasmas SH, et al. Pharmacokinetic interactions between clopidogrel and rosuvastatin: effects on vascular protection in subjects with coronary heart disease. Int J Cardiol. 2012;158(1):125-9.
  • 23
    França CN, Pinheiro LF, Izar MC, Brunialti MK, Salomão R, Bianco HT, et al. Endothelial progenitor cell mobilization and platelet microparticle release are influenced by clopidogrel plasma levels in stable coronary artery disease. Circ J. 2012;76(3):729-36.
  • 24
    Morel O, Jesel L, Freyssinet JM, Toti F. Cellular mechanisms underlying the formation of circulating microparticles. Arterioscler Thromb Vasc Biol. 2011;31(1):15-26.
  • 25
    Gyorgy B, Szabo TG, Pasztoi M, Pal Z, Misjak P, Aradi B, et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci. 2011;68(16):2667-88.
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Publication Dates

  • Publication in this collection
    10 July 2017
  • Date of issue
    Jul-Aug 2017

History

  • Received
    20 Jan 2017
  • Accepted
    15 Mar 2017
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