Published by De Gruyter May 11, 2018

Circulating microparticles in patients after ischemic stroke: a systematic review and meta-analysis

Botao Wang , Wang Cai , Zhen Zhang , Hui Zhang , Ke Tang , Qi Zhang and Ximo Wang

From the journal Reviews in the Neurosciences

https://doi.org/10.1515/revneuro-2017-0105

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Abstract

Microparticles (MPs), a class of cell products with biological activities, have been found to participate in a series of vascular activities. The aim of this article is to investigate the changes in the concentrations of MPs after ischemic stroke by meta-analysis. According to pre-established criteria, a strict screening of articles was performed through the Medline and Embase databases. Subsequently, the included studies were subjected to quality assessment and data extraction. Finally, a meta-analysis was performed on seven major outcomes from 985 noncerebrovascular disease controls and 988 ischemic stroke patients. The pooled concentrations of total MPs (TMPs), endotheliocyte-derived MPs (EMPs), platelet-derived MPs (PMPs), erythrocyte-derived MPs (RMPs), leukocyte-derived MPs (LMPs), and monocyte-derived MPs (MMPs) were significantly increased in the ischemic stroke patients compared to the noncerebrovascular disease controls, with the results as follows: TMPs [standardized mean difference (SMD), 1.12; 95% confidence interval (CI), 0.26–1.97; p=0.01], EMPs (SMD, 0.90; 95% CI, 0.67–1.13; p<0.00001), PMPs (SMD, 1.15; 95% CI, 0.69–1.60; p<0.00001), RMPs (SMD, 1.14; 95% CI, 0.57–1.71; p<0.0001), LMPs (SMD, 1.42; 95% CI, 0.74–2.10; p<0.0001), and MMPs (SMD, 1.09; 95% CI, 0.59–1.60; p<0.0001). However, the pooled concentration of lymphocyte-derived MPs (LyMPs) demonstrated no significant difference between the patients and the controls (SMD, 0.22; 95% CI, −0.19 to 0.63; p=0.29). The available data indicated that the circulating MPs, except for LyMPs, play an important role in the development and prognosis of ischemic stroke.

Keywords: cell-derived microparticles; cerebrovascular disease; circulating microparticles; ischemic stroke; meta-analysis

Acknowledgments

We acknowledge Soundny (Sheng-Qi-An) Biotech (Wuhan, China). This study was funded by the National Natural Science Foundation of China (grant 81602496), the Science and Technology Foundation of Administration of Traditional Chinese Medicine of Tianjin, China (grant 2015022, 13047), and the Science and Technology Foundation of Tianjin Municipal Commission of Health and Family Planning (grant 2013KZ054).

References

Adams, H.P., Jr., Bendixen, B.H., Kappelle, L.J., Biller, J., Love, B.B., Gordon, D.L., and Marsh, E.E. 3rd. (1993). Classification of subtype of acute ischemic stroke. Definitions for use in a multicenter clinical trial. TOAST. Trial of Org 10172 in Acute Stroke Treatment. Stroke 24, 35–41.10.1161/01.STR.24.1.35Search in Google Scholar

Arderiu, G., Pena, E., and Badimon, L. (2015). Angiogenic microvascular endothelial cells release microparticles rich in tissue factor that promotes postischemic collateral vessel formation. Arterioscler. Thromb. Vasc. Biol. 35, 348–357.10.1161/ATVBAHA.114.303927Search in Google Scholar

Ayers, L., Nieuwland, R., Kohler, M., Kraenkel, N., Ferry, B., and Leeson, P. (2015). Dynamic microvesicle release and clearance within the cardiovascular system: triggers and mechanisms. Clin. Sci. (Lond.) 129, 915–931.10.1042/CS20140623Search in Google Scholar

Burger, D., Schock, S., Thompson, C.S., Montezano, A.C., Hakim, A.M., and Touyz, R.M. (2013). Microparticles: biomarkers and beyond. Clin. Sci. (Lond.) 124, 423–441.10.1042/CS20120309Search in Google Scholar

Chen, Y., Xiao, Y., Lin, Z., Xiao, X., He, C., Bihl, J. C., Zhao, B., Ma, X., and Chen, Y. (2015). The role of circulating platelets microparticles and platelet parameters in acute ischemic stroke patients. J. Stroke Cerebrovasc. Dis. 24, 2313–2320.10.1016/j.jstrokecerebrovasdis.2015.06.018Search in Google Scholar

Cherian, P., Hankey, G.J., Eikelboom, J.W., Thom, J., Baker, R.I., McQuillan, A., Staton, J., and Yi, Q. (2003). Endothelial and platelet activation in acute ischemic stroke and its etiological subtypes. Stroke 34, 2132–2137.10.1161/01.STR.0000086466.32421.F4Search in Google Scholar

Chiva-Blanch, G., Suades, R., Crespo, J., Pena, E., Padro, T., Jimenez-Xarrie, E., Marti-Fabregas, J., and Badimon, L. (2016). Microparticle shedding from neural progenitor cells and vascular compartment cells is increased in ischemic stroke. PLoS One 11, e0148176.10.1371/journal.pone.0148176Search in Google Scholar

Hankey, G.J. (2016). Stroke. Lancet 389, 641–654.10.1016/S0140-6736(16)30962-XSearch in Google Scholar

Hanscombe, K.B., Traylor, M., Hysi, P.G., Bevan, S., Dichgans, M., Rothwell, P.M., Worrall, B.B., Seshadri, S., Sudlow, C., Williams, F.M.K., et al. (2015). Genetic factors influencing coagulation factor XIII B-subunit contribute to risk of ischemic stroke. Stroke 46, 2069–2074.10.1161/STROKEAHA.115.009387Search in Google Scholar PubMed PubMed Central

Hargett, L.A. and Bauer, N.N. (2013). On the origin of microparticles: from “platelet dust” to mediators of intercellular communication. Pulm. Circ. 3, 329–340.10.4103/2045-8932.114760Search in Google Scholar PubMed PubMed Central

He, Z., Tang, Y., and Qin, C. (2017). Increased circulating leukocyte-derived microparticles in ischemic cerebrovascular disease. Thromb. Res. 154, 19–25.10.1016/j.thromres.2017.03.025Search in Google Scholar PubMed

Jansen, F., Yang, X., Hoelscher, M., Cattelan, A., Schmitz, T., Proebsting, S., Wenzel, D., Vosen, S., Franklin, B.S., Fleischmann, B.K., et al. (2013). Endothelial microparticle-mediated transfer of microRNA-126 promotes vascular endothelial cell repair via SPRED1 and is abrogated in glucose-damaged endothelial microparticles. Circulation 128, 2026–2038.10.1161/CIRCULATIONAHA.113.001720Search in Google Scholar PubMed

Jung, K.H., Chu, K., Lee, S.T., Park, H.K., Bahn, J.J., Kim, D.H., Kim, J.H., Kim, M., Kun Lee, S., and Roh, J.K. (2009). Circulating endothelial microparticles as a marker of cerebrovascular disease. Ann. Neurol. 66, 191–199.10.1002/ana.21681Search in Google Scholar PubMed

Koshiar, R.L., Somajo, S., Norstrom, E., and Dahlback, B. (2014). Erythrocyte-derived microparticles supporting activated protein C-mediated regulation of blood coagulation. PLoS One 9, e104200.10.1371/journal.pone.0104200Search in Google Scholar PubMed PubMed Central

Kuriyama, N., Nagakane, Y., Hosomi, A., Ohara, T., Kasai, T., Harada, S., Takeda, K., Yamada, K., Ozasa, K., Tokuda, T., et al. (2010). Evaluation of factors associated with elevated levels of platelet-derived microparticles in the acute phase of cerebral infarction. Clin. Appl. Thromb. Hemost. 16, 26–32.10.1177/1076029609338047Search in Google Scholar PubMed

Lavallee, P.C., Labreuche, J., Faille, D., Huisse, M.G., Nicaise-Roland, P., Dehoux, M., Gongora-Rivera, F., Jaramillo, A., Brenner, D., Deplanque, D., et al. (2013). Circulating markers of endothelial dysfunction and platelet activation in patients with severe symptomatic cerebral small vessel disease. Cerebrovasc. Dis. 36, 131–138.10.1159/000353671Search in Google Scholar PubMed

Li, P. and Qin, C. (2015). Elevated circulating VE-cadherin⁺ CD144⁺ endothelial microparticles in ischemic cerebrovascular disease. Thromb. Res. 135, 375–381.10.1016/j.thromres.2014.12.006Search in Google Scholar PubMed

Li, S., Wei, J., Zhang, C., Li, X., Meng, W., Mo, X., Zhang, Q., Liu, Q., Ren, K., Du, R., et al. (2016). Cell-derived microparticles in patients with type 2 diabetes mellitus: a systematic review and meta-analysis. Cell. Physiol. Biochem. 39, 2439–2450.10.1159/000452512Search in Google Scholar PubMed

Lovren, F. and Verma, S. (2013). Evolving role of microparticles in the pathophysiology of endothelial dysfunction. Clin. Chem. 59, 1166–1174.10.1373/clinchem.2012.199711Search in Google Scholar PubMed

Macey, M.G., Enniks, N., and Bevan, S. (2011). Flow cytometric analysis of microparticle phenotype and their role in thrombin generation. Cytometry B Clin. Cytom. 80, 57–63.10.1002/cyto.b.20551Search in Google Scholar PubMed

Margulis, A.V., Pladevall, M., Riera-Guardia, N., Varas-Lorenzo, C., Hazell, L., Berkman, N.D., Viswanathan, M., and Perez-Gutthann, S. (2014). Quality assessment of observational studies in a drug-safety systematic review, comparison of two tools: the Newcastle-Ottawa Scale and the RTI item bank. Clin. Epidemiol. 6, 359–368.10.2147/CLEP.S66677Search in Google Scholar PubMed PubMed Central

Mozaffarian, D., Benjamin, E.J., Go, A.S., Arnett, D.K., Blaha, M.J., Cushman, M., Das, S.R., de Ferranti, S., Despres, J.P., Fullerton, H.J., et al. (2016). Heart Disease and Stroke Statistics-2016 Update: a report from the American Heart Association. Circulation 133, e38–e360.10.1161/CIR.0000000000000350Search in Google Scholar PubMed

Pawelczyk, M., Baj, Z., Chmielewski, H., Kaczorowska, B., and Klimek, A. (2009). The influence of hyperlipidemia on platelet activity markers in patients after ischemic stroke. Cerebrovasc. Dis. 27, 131–137.10.1159/000177920Search in Google Scholar PubMed

Prakash, P.S., Caldwell, C.C., Lentsch, A.B., Pritts, T.A., and Robinson, B.R. (2012). Human microparticles generated during sepsis in patients with critical illness are neutrophil-derived and modulate the immune response. J. Trauma Acute Care Surg. 73, 401–406; discussion 406–407.10.1097/TA.0b013e31825a776dSearch in Google Scholar PubMed PubMed Central

Roseblade, A., Luk, F., Rawling, T., Ung, A., Grau, G.E., and Bebawy, M. (2013). Cell-derived microparticles: new targets in the therapeutic management of disease. J. Pharm. Pharm. Sci. 16, 238–253.10.18433/J3989XSearch in Google Scholar PubMed

Rubin, O., Delobel, J., Prudent, M., Lion, N., Kohl, K., Tucker, E.I., Tissot, J.D., and Angelillo-Scherrer, A. (2013). Red blood cell-derived microparticles isolated from blood units initiate and propagate thrombin generation. Transfusion 53, 1744–1754.10.1111/trf.12008Search in Google Scholar PubMed

Sahler, J., Woeller, C.F., and Phipps, R.P. (2014). Microparticles engineered to highly express peroxisome proliferator-activated receptor-γ decreased inflammatory mediator production and increased adhesion of recipient monocytes. PLoS One 9, e113189.10.1371/journal.pone.0113189Search in Google Scholar PubMed PubMed Central

Shim, R. and Wong, C.H. (2016). Ischemia, immunosuppression and infection – tackling the predicaments of post-stroke complications. Int. J. Mol. Sci. 17, 64.10.3390/ijms17010064Search in Google Scholar PubMed PubMed Central

Shirafuji, T., Hamaguchi, H., and Kanda, F. (2008). Measurement of platelet-derived microparticle levels in the chronic phase of cerebral infarction using an enzyme-linked immunosorbent assay. Kobe J. Med. Sci. 54, E55–E61.Search in Google Scholar

Simak, J., Gelderman, M.P., Yu, H., Wright, V., and Baird, A.E. (2006). Circulating endothelial microparticles in acute ischemic stroke: a link to severity, lesion volume and outcome. J. Thromb. Haemost. 4, 1296–1302.10.1111/j.1538-7836.2006.01911.xSearch in Google Scholar PubMed

Somajo, S., Koshiar, R.L., Norstrom, E., and Dahlback, B. (2014). Protein S and factor V in regulation of coagulation on platelet microparticles by activated protein C. Thromb. Res. 134, 144–152.10.1016/j.thromres.2014.04.031Search in Google Scholar PubMed

Sun, C., Zhao, W.B., Chen, Y., and Hu, H.Y. (2016). Higher plasma concentrations of platelet microparticles in patients with acute coronary syndrome: a systematic review and meta-analysis. Can. J. Cardiol. 32, 1325.e1321–1325.e1310.10.1016/j.cjca.2016.02.052Search in Google Scholar PubMed

Switonska, M., Slomka, A., Sinkiewicz, W., and Zekanowska, E. (2015). Tissue-factor-bearing microparticles (MPs-TF) in patients with acute ischaemic stroke: the influence of stroke treatment on MPs-TF generation. Eur. J. Neurol. 22, 395–401, e328–e399.10.1111/ene.12591Search in Google Scholar PubMed

Undas, A., Slowik, A., Wolkow, P., Szczudlik, A., and Tracz, W. (2010). Fibrin clot properties in acute ischemic stroke: relation to neurological deficit. Thromb Res. 125, 357–361.10.1016/j.thromres.2009.11.013Search in Google Scholar PubMed

Varon, D. and Shai, E. (2015). Platelets and their microparticles as key players in pathophysiological responses. J. Thromb. Haemost. 13, S40–S46.10.1111/jth.12976Search in Google Scholar PubMed

Vuckovic, B.A., Djeric, M.J., Ilic, T.A., Canak, V.B., Kojic-Damjanov, S., Zarkov, M.G., and Cabarkapa, V.S. (2010). Fibrinolytic parameters, lipid status and lipoprotein (a) in ischemic stroke patients. Srp. Arh. Celok. Lek. 138, 12–17.10.2298/SARH10S1012VSearch in Google Scholar

Wang, Z., Cai, W., Hu, S., Xia, Y., Wang, Y., Zhang, Q., and Chen, L. (2017). A meta-analysis of circulating microvesicles in patients with myocardial infarction. Arq. Bras. Cardiol. 109, 156–164.10.5935/abc.20170102Search in Google Scholar PubMed PubMed Central

Yao, Z., Wang, L., Wu, X., Zhao, L., Chi, C., Guo, L., Tong, D., Yang, X., Dong, Z., Deng, R., et al. (2016). Enhanced procoagulant activity on blood cells after acute ischemic stroke. Transl. Stroke Res. 8, 83–91.10.1007/s12975-016-0501-7Search in Google Scholar PubMed

Yong, P.J., Koh, C.H., and Shim, W.S. (2013). Endothelial microparticles: missing link in endothelial dysfunction? Eur. J. Prev. Cardiol. 20, 496–512.10.1177/2047487312445001Search in Google Scholar PubMed

Yun, J.W., Xiao, A., Tsunoda, I., Minagar, A., and Alexander, J.S. (2016). From trash to treasure: the untapped potential of endothelial microparticles in neurovascular diseases. Pathophysiology 23, 265–274.10.1016/j.pathophys.2016.08.004Search in Google Scholar PubMed

Zubairova, L.D., Nabiullina, R.M., Nagaswami, C., Zuev, Y.F., Mustafin, I.G., Litvinov, R.I., and Weisel, J.W. (2015). Circulating microparticles alter formation, structure, and properties of fibrin clots. Sci. Rep. 5, 17611.10.1038/srep17611Search in Google Scholar PubMed PubMed Central