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Cardiovascular & Hematological Agents in Medicinal Chemistry

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ISSN (Print): 1871-5257
ISSN (Online): 1875-6182

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Review Article

Biomarkers in Unstable Carotid Plaque: Physiopathology and Prediction

Author(s): Antonio Siniscalchi*, Sean Murphy, Cleona Gray, Giovambattista De Sarro and Luca Gallelli

Volume 20, Issue 1, 2022

Published on: 01 September, 2021

Page: [13 - 19] Pages: 7

DOI: 10.2174/1871525719666210901131509

Price: $65

Abstract

Aims: To study the role of cytokines and vascular inflammatory biomarkers in unstable carotid plaque.

Background: Clinical studies showed that not only the degree of stenosis but also the type of carotid plaque can be responsible for ipsilateral ischemic stroke.

Objective: The objective of this study is to suggest a role for vulnerable carotid atherosclerotic disease in the occurrence of ischemic stroke.

Methods: PubMed, Embase, Cochrane library, and reference lists have been used to evaluate articles published until February 15, 2021.

Results: Several factors may be involved in unstable plaque. Clinical studies support the involvement of brain inflammatory biomarkers as well as cytokines in the unstable carotid plaque.

Conclusions: Biomarkers could help to stratify patients with a vulnerable carotid plaque and to personalize the drug treatment. In this review, we briefly discuss the characteristics of vulnerable plaque and the role of biomarkers in the vulnerable carotid plaque.

Keywords: Brain inflammation, carotid artery disease, cytokines, stroke, vascular inflammatory biomarker, atherosclerosis.

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[1]
Anticoli, S.; Bravi, M.C.; Perillo, G.; Siniscalchi, A.; Pozzessere, C.; Pezzella, F.R.; Tanzi, P.; Gallelli, L.; Cartoni, D. Effect of cardioembolic etiology on intravenous thrombolysis efficacy for acute ischemic stroke. Curr. Neurovasc. Res., 2016, 13(3), 193-198.
[http://dx.doi.org/10.2174/1567202613666160506125426] [PMID: 27149937]
[2]
Siniscalchi, A.; Bonci, A.; Mercuri, N.B.; De Siena, A.; De Sarro, G.; Malferrari, G.; Diana, M.; Gallelli, L. Cocaine dependence and stroke: pathogenesis and management. Curr. Neurovasc. Res., 2015, 12(2), 163-172.
[http://dx.doi.org/10.2174/1567202612666150305110144] [PMID: 25742568]
[3]
Ooi, Y.C.; Gonzalez, N.R. Management of extracranial carotid artery disease. Cardiol. Clin., 2015, 33(1), 1-35.
[http://dx.doi.org/10.1016/j.ccl.2014.09.001] [PMID: 25439328]
[4]
Gaba, K.; Ringleb, P.A.; Halliday, A. Asymptomatic carotid stenosis: Intervention or best medical therapy? Curr. Neurol. Neurosci. Rep., 2018, 18(11), 80.
[http://dx.doi.org/10.1007/s11910-018-0888-5] [PMID: 30251204]
[5]
Kernan, W.N.; Ovbiagele, B.; Black, H.R.; Bravata, D.M.; Chimowitz, M.I.; Ezekowitz, M.D.; Fang, M.C.; Fisher, M.; Furie, K.L.; Heck, D.V.; Johnston, S.C.; Kasner, S.E.; Kittner, S.J.; Mitchell, P.H.; Rich, M.W.; Richardson, D.; Schwamm, L.H.; Wilson, J.A. Guidelines for the prevention of stroke in patients with stroke and transient ischemic attack: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke, 2014, 45(7), 2160-2236.
[http://dx.doi.org/10.1161/STR.0000000000000024] [PMID: 24788967]
[6]
Naylor, A.R.; Ricco, J.B.; de Borst, G.J.; Debus, S.; de Haro, J.; Halliday, A.; Hamilton, G.; Kakisis, J.; Kakkos, S.; Lepidi, S.; Markus, H.S.; McCabe, D.J.; Roy, J.; Sillesen, H.; van den Berg, J.C.; Vermassen, F.; Kolh, P.; Chakfe, N.; Hinchliffe, R.J.; Koncar, I.; Lindholt, J.S.; Vega de Ceniga, M.; Verzini, F.; Archie, J.; Bellmunt, S.; Chaudhuri, A.; Koelemay, M.; Lindahl, A.K.; Padberg, F.; Venermo, M. Editor’s choice - Management of atherosclerotic carotid and vertebral artery disease: 2017 clinical practice guidelines of the European Society for Vascular Surgery (ESVS). Eur. J. Vasc. Endovasc. Surg., 2018, 55(1), 3-81.
[http://dx.doi.org/10.1016/j.ejvs.2017.06.021] [PMID: 28851594]
[7]
Yamada, K.; Kawasaki, M.; Yoshimura, S.; Shirakawa, M.; Uchida, K.; Shindo, S.; Nishida, S.; Iwamoto, Y.; Nakahara, S.; Sato, Y. High-intensity signal in carotid plaque on routine 3d-tof-mra is a risk factor of ischemic stroke. Cerebrovasc. Dis., 2016, 41(1-2), 13-18.
[http://dx.doi.org/10.1159/000441094] [PMID: 26580667]
[8]
Higgins, J.P.T.; Green, S. 2011.http://handbook-5-1.cochrane.org
[9]
Hosseini, A.A.; Kandiyil, N.; Macsweeney, S.T.; Altaf, N.; Auer, D.P. Carotid plaque hemorrhage on magnetic resonance imaging strongly predicts recurrent ischemia and stroke. Ann. Neurol., 2013, 73(6), 774-784.
[http://dx.doi.org/10.1002/ana.23876] [PMID: 23463579]
[10]
Selwaness, M.; Bos, D.; van den Bouwhuijsen, Q.; Portegies, M.L.; Ikram, M.A.; Hofman, A.; Franco, O.H.; van der Lugt, A.; Wentzel, J.J.; Vernooij, M.W. Carotid atherosclerotic plaque characteristics on magnetic resonance imaging relate with history of stroke and coronary heart disease. Stroke, 2016, 47(6), 1542-1547.
[http://dx.doi.org/10.1161/STROKEAHA.116.012923] [PMID: 27165952]
[11]
Saam, T.; Hetterich, H.; Hoffmann, V.; Yuan, C.; Dichgans, M.; Poppert, H.; Koeppel, T.; Hoffmann, U.; Reiser, M.F.; Bamberg, F. Meta-analysis and systematic review of the predictive value of carotid plaque hemorrhage on cerebrovascular events by magnetic resonance imaging. J. Am. Coll. Cardiol., 2013, 62(12), 1081-1091.
[http://dx.doi.org/10.1016/j.jacc.2013.06.015] [PMID: 23850912]
[12]
Singh, N.; Moody, A.R.; Panzov, V.; Gladstone, D.J. Carotid intraplaque hemorrhage in patients with embolic stroke of undetermined source. J. Stroke Cerebrovasc. Dis., 2018, 27(7), 1956-1959.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2018.02.042] [PMID: 29571754]
[13]
Xu, D.; Hippe, D.S.; Underhill, H.R.; Oikawa-Wakayama, M.; Dong, L.; Yamada, K.; Yuan, C.; Hatsukami, T.S. Prediction of high-risk plaque development and plaque progression with the carotid atherosclerosis score. JACC Cardiovasc. Imaging, 2014, 7(4), 366-373.
[http://dx.doi.org/10.1016/j.jcmg.2013.09.022] [PMID: 24631510]
[14]
Yuan, C.; Zhang, S.X.; Polissar, N.L.; Echelard, D.; Ortiz, G.; Davis, J.W.; Ellington, E.; Ferguson, M.S.; Hatsukami, T.S. Identification of fibrous cap rupture with magnetic resonance imaging is highly associated with recent transient ischemic attack or stroke. Circulation, 2002, 105(2), 181-185.
[http://dx.doi.org/10.1161/hc0202.102121] [PMID: 11790698]
[15]
van Dijk, A.C.; Truijman, M.T.; Hussain, B.; Zadi, T.; Saiedie, G.; de Rotte, A.A.; Liem, M.I.; van der Steen, A.F.; Daemen, M.J.; Koudstaal, P.J.; Nederkoorn, P.J.; Hendrikse, J.; Kooi, M.E.; van der Lugt, A. Intraplaque hemorrhage and the plaque surface in carotid atherosclerosis: The Plaque At RISK study (PARISK). AJNR Am. J. Neuroradiol., 2015, 36(11), 2127-2133.
[http://dx.doi.org/10.3174/ajnr.A4414] [PMID: 26251429]
[16]
Barnett, H.J.; Taylor, D.W.; Eliasziw, M.; Fox, A.J.; Ferguson, G.G.; Haynes, R.B.; Rankin, R.N.; Clagett, G.P.; Hachinski, V.C.; Sackett, D.L.; Thorpe, K.E.; Meldrum, H.E.; Spence, J.D. Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. N. Engl. J. Med., 1998, 339(20), 1415-1425.
[http://dx.doi.org/10.1056/NEJM199811123392002] [PMID: 9811916]
[17]
van Gils, M.J.; Homburg, P.J.; Rozie, S.; de Weert, T.T.; Dippel, D.W.; van der Lugt, A. Evolution of atherosclerotic carotid plaque morphology: do ulcerated plaques heal? A serial multidetector CT angiography study. Cerebrovasc. Dis., 2011, 31(3), 263-270.
[http://dx.doi.org/10.1159/000322152] [PMID: 21178351]
[18]
Saba, L.; Raz, E.; Grassi, R.; Di Paolo, P.L.; Iacomino, A.; Montisci, R.; Piga, M. Association between the volume of carotid artery plaque and its subcomponents and the volume of white matter lesions in patients selected for endarterectomy. AJR Am. J. Roentgenol., 2013, 201(5), W747-52.
[http://dx.doi.org/10.2214/AJR.12.10217] [PMID: 24147504]
[19]
Lu, M.; Peng, P.; Cui, Y.; Qiao, H.; Li, D.; Cai, J.; Zhao, X. Association of progression of carotid artery wall volume and recurrent transient ischemic attack or stroke: a magnetic resonance imaging study. Stroke, 2018, 49(3), 614-620.
[http://dx.doi.org/10.1161/STROKEAHA.117.019422] [PMID: 29382804]
[20]
Qiao, Y.; Etesami, M.; Astor, B.C.; Zeiler, S.R.; Trout, H.H., III; Wasserman, B.A. Carotid plaque neovascularization and hemorrhage detected by MR imaging are associated with recent cerebrovascular ischemic events. AJNR Am. J. Neuroradiol., 2012, 33(4), 755-760.
[http://dx.doi.org/10.3174/ajnr.A2863] [PMID: 22194363]
[21]
Saba, L.; Saam, T.; Jäger, H.R.; Yuan, C.; Hatsukami, T.S.; Saloner, D.; Wasserman, B.A.; Bonati, L.H.; Wintermark, M. Imaging biomarkers of vulnerable carotid plaques for stroke risk prediction and their potential clinical implications. Lancet Neurol., 2019, 18(6), 559-572.
[http://dx.doi.org/10.1016/S1474-4422(19)30035-3] [PMID: 30954372]
[22]
Kakkos, S.K.; Griffin, M.B.; Nicolaides, A.N.; Kyriacou, E.; Sabetai, M.M.; Tegos, T.; Makris, G.C.; Thomas, D.J.; Geroulakos, G. The size of juxtaluminal hypoechoic area in ultrasound images of asymptomatic carotid plaques predicts the occurrence of stroke. J. Vasc. Surg., 2013, 57(3), 609-618.e1.
[http://dx.doi.org/10.1016/j.jvs.2012.09.045] [PMID: 23337294]
[23]
Underhill, H.R.; Hatsukami, T.S.; Cai, J.; Yu, W.; DeMarco, J.K.; Polissar, N.L.; Ota, H.; Zhao, X.; Dong, L.; Oikawa, M.; Yuan, C. A noninvasive imaging approach to assess plaque severity: the carotid atherosclerosis score. AJNR Am. J. Neuroradiol., 2010, 31(6), 1068-1075.
[http://dx.doi.org/10.3174/ajnr.A2007] [PMID: 20093315]
[24]
Ritter, M.A.; Theismann, K.; Schmiedel, M.; Ringelstein, E.B.; Dittrich, R. Vascularization of carotid plaque in recently symptomatic patients is associated with the occurrence of transcranial microembolic signals. Eur. J. Neurol., 2013, 20(8), 1218-1221.
[http://dx.doi.org/10.1111/ene.12030] [PMID: 23163829]
[25]
Nicoll, R.; Henein, M.Y. Arterial calcification: friend or foe? Int J. Control, 2013, 167(2), 322-327.
[http://dx.doi.org/10.1016/j.ijcard.2012.06.110]
[26]
Ibrahimi, P.; Jashari, F.; Nicoll, R.; Bajraktari, G.; Wester, P.; Henein, M.Y. Coronary and carotid atherosclerosis: how useful is the imaging? Atherosclerosis, 2013, 231(2), 323-333.
[http://dx.doi.org/10.1016/j.atherosclerosis.2013.09.035] [PMID: 24267246]
[27]
Shi, X.; Han, Y.; Li, M.; Yin, Q.; Liu, R.; Wang, F.; Xu, X.; Xiong, Y.; Ye, R.; Liu, X. Superficial calcification with rotund shape is associated with carotid plaque rupture: an optical coherence tomography study. Front. Neurol., 2020, 11, 563334.
[http://dx.doi.org/10.3389/fneur.2020.563334] [PMID: 33071946]
[28]
Kadoglou, N.P.; Gerasimidis, T.; Golemati, S.; Kapelouzou, A.; Karayannacos, P.E.; Liapis, C.D. Intensive lipid-lowering therapy ameliorates novel calcification markers and GSM score in patients with carotid stenosis. J. Vasc. Surg., 2008, 47(1), 55-56.
[http://dx.doi.org/10.1016/j.jvs.2007.09.058] [PMID: 18178454]
[29]
Siniscalchi, A.; Gallelli, L.; Malferrari, G.; Pirritano, D.; Serra, R.; Santangelo, E.; De Sarro, G. Cerebral stroke injury: the role of cytokines and brain inflammation. J. Basic Clin. Physiol. Pharmacol., 2014, 25(2), 131-137.
[http://dx.doi.org/10.1515/jbcpp-2013-0121] [PMID: 24515999]
[30]
Siniscalchi, A.; Iannacchero, R.; Anticoli, S.; Pezzella, F.R.; De Sarro, G.; Gallelli, L. Anti-inflammatory strategies in stroke: a potential therapeutic target. Curr. Vasc. Pharmacol., 2016, 14(1), 98-105.
[http://dx.doi.org/10.2174/1570161113666150923111329] [PMID: 26411421]
[31]
Tedgui, A.; Mallat, Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol. Rev., 2006, 86(2), 515-581.
[http://dx.doi.org/10.1152/physrev.00024.2005] [PMID: 16601268]
[32]
Tzoulaki, I.; Murray, G.D.; Lee, A.J.; Rumley, A.; Lowe, G.D.; Fowkes, F.G. Relative value of inflammatory, hemostatic, and rheological factors for incident myocardial infarction and stroke: the Edinburgh Artery Study. Circulation, 2007, 115(16), 2119-2127.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.635029] [PMID: 17404162]
[33]
Avgerinos, E.D.; Kadoglou, N.P.; Moulakakis, K.G.; Giannakopoulos, T.G.; Liapis, C.D. Current role of biomarkers in carotid disease: a systematic review. Int. J. Stroke, 2011, 6(4), 337-345.
[http://dx.doi.org/10.1111/j.1747-4949.2011.00623.x] [PMID: 21745345]
[34]
Martinez, E.; Martorell, J.; Riambau, V. Review of serum biomarkers in carotid atherosclerosis. J. Vasc. Surg., 2020, 71(1), 329-341.
[http://dx.doi.org/10.1016/j.jvs.2019.04.488] [PMID: 31327598]
[35]
Biscetti, F.; Straface, G.; Bertoletti, G.; Vincenzoni, C.; Snider, F.; Arena, V.; Landolfi, R.; Flex, A. Identification of a potential proinflammatory genetic profile influencing carotid plaque vulnerability. J. Vasc. Surg., 2015, 61(2), 374-381.
[http://dx.doi.org/10.1016/j.jvs.2014.08.113] [PMID: 25441669]
[36]
Profumo, E.; Buttari, B.; Tosti, M.E.; Siracusano, A.; Ortona, E.; Margutti, P.; Capoano, R.; Salvati, B.; Riganò, R. Association of intracellular pro- and anti-inflammatory cytokines in peripheral blood with the clinical or ultrasound indications for carotid endarterectomy in patients with carotid atherosclerosis. Clin. Exp. Immunol., 2008, 152(1), 120-126.
[http://dx.doi.org/10.1111/j.1365-2249.2008.03604.x] [PMID: 18307518]
[37]
Koutouzis, M.; Rallidis, L.S.; Peros, G.; Nomikos, A.; Tzavara, V.; Barbatis, C.; Andrikopoulos, V.; Vassiliou, J.; Kyriakides, Z.S. Serum interleukin-6 is elevated in symptomatic carotid bifurcation disease. Acta Neurol. Scand., 2009, 119(2), 119-125.
[http://dx.doi.org/10.1111/j.1600-0404.2008.01068.x] [PMID: 18638042]
[38]
Bountouris, I.; Paraskevas, K.I.; Koutouzis, M.; Tzavara, V.; Nikolaou, N.; Nomikos, A.; Barbatis, C.; Andrikopoulos, V.; Mikhailidis, D.P.; Andrikopoulou, M.; Kyriakides, Z.S.; Georgopoulos, S.; Michail, P.O.; Bastounis, E. Serum leptin levels in patients undergoing carotid endarterectomy: a pilot study. Angiology, 2009, 60(6), 698-704.
[http://dx.doi.org/10.1177/0003319709350133] [PMID: 19825871]
[39]
Debing, E.; Peeters, E.; Demanet, C.; De Waele, M.; Van den Brande, P. Markers of inflammation in patients with symptomatic and asymptomatic carotid artery stenosis: a case-control study. Vasc. Endovascular Surg., 2008, 42(2), 122-127.
[http://dx.doi.org/10.1177/1538574407307406] [PMID: 18421029]
[40]
Eltoft, A.; Arntzen, K.A.; Wilsgaard, T.; Mathiesen, E.B.; Johnsen, S.H. Interleukin-6 is an independent predictor of progressive atherosclerosis in the carotid artery: The Tromsø Study. Atherosclerosis, 2018, 271, 1-8.
[http://dx.doi.org/10.1016/j.atherosclerosis.2018.02.005] [PMID: 29453087]
[41]
Stankovic, M.; Ljujic, B.; Babic, S.; Maravic-Stojkovic, V.; Mitrovic, S.; Arsenijevic, N.; Radak, D.; Pejnovic, N.; Lukic, M.L. IL-33/IL-33R in various types of carotid artery atherosclerotic lesions. Cytokine, 2019, 120, 242-250.
[http://dx.doi.org/10.1016/j.cyto.2019.05.010] [PMID: 31132589]
[42]
Andersson, J.; Sundström, J.; Gustavsson, T.; Hulthe, J.; Elmgren, A.; Zilmer, K.; Zilmer, M.; Lind, L. Echogenecity of the carotid intima-media complex is related to cardiovascular risk factors, dyslipidemia, oxidative stress and inflammation: the Prospective Investigation of the Vasculature in Uppsala Seniors (PIVUS) study. Atherosclerosis, 2009, 204(2), 612-618.
[http://dx.doi.org/10.1016/j.atherosclerosis.2008.10.038] [PMID: 19200993]
[43]
Mallat, Z.; Corbaz, A.; Scoazec, A.; Besnard, S.; Lesèche, G.; Chvatchko, Y.; Tedgui, A. Expression of interleukin-18 in human atherosclerotic plaques and relation to plaque instability. Circulation, 2001, 104(14), 1598-1603.
[http://dx.doi.org/10.1161/hc3901.096721] [PMID: 11581135]
[44]
Mallat, Z.; Corbaz, A.; Scoazec, A.; Graber, P.; Alouani, S.; Esposito, B.; Humbert, Y.; Chvatchko, Y.; Tedgui, A. Interleukin-18/interleukin-18 binding protein signaling modulates atherosclerotic lesion development and stability. Circ. Res., 2001, 89(7), E41-E45.
[http://dx.doi.org/10.1161/hh1901.098735] [PMID: 11577031]
[45]
Elhage, R.; Jawien, J.; Rudling, M.; Ljunggren, H.G.; Takeda, K.; Akira, S.; Bayard, F.; Hansson, G.K. Reduced atherosclerosis in interleukin-18 deficient apolipoprotein E-knockout mice. Cardiovasc. Res., 2003, 59(1), 234-240.
[http://dx.doi.org/10.1016/S0008-6363(03)00343-2] [PMID: 12829194]
[46]
Siniscalchi, A.; Gallelli, L. Could COVID-19 represent a negative prognostic factor in patients with stroke? Infect. Control Hosp. Epidemiol., 2020, 41(9), 1115-1116.
[http://dx.doi.org/10.1017/ice.2020.146] [PMID: 32307025]
[47]
Mohamud, A.Y.; Griffith, B.; Rehman, M.; Miller, D.; Chebl, A.; Patel, S.C.; Howell, B.; Kole, M.; Marin, H. Intraluminal carotid artery thrombus in covid-19: another danger of cytokine storm? AJNR Am. J. Neuroradiol., 2020, 41(9), 1677-1682.
[PMID: 32616585]
[48]
Chou, C.Y.; Kuo, H.L.; Lin, H.H.; Liu, J.S.; Liu, Y.L.; Huang, C.C. C-reactive protein predicts ischaemic stroke in haemodialysis patients. Int. J. Clin. Pract., 2009, 63(2), 243-248.
[http://dx.doi.org/10.1111/j.1742-1241.2007.01333.x] [PMID: 17973918]
[49]
Anan, F.; Shimomura, T.; Kaku, T.; Kaneda, K.; Imagawa, M.; Tsukagawa, H.; Masaki, T.; Nawata, T.; Yonemochi, H.; Eshima, N.; Saikawa, T.; Yoshimatsu, H. High-sensitivity C-reactive protein level is a significant risk factor for silent cerebral infarction in patients on hemodialysis. Metabolism, 2008, 57(1), 66-70.
[http://dx.doi.org/10.1016/j.metabol.2007.08.007] [PMID: 18078860]
[50]
Chuang, S.Y.; Bai, C.H.; Chen, W.H.; Lien, L.M.; Pan, W.H. Fibrinogen independently predicts the development of ischemic stroke in a Taiwanese population: CVDFACTS study. Stroke, 2009, 40(5), 1578-1584.
[http://dx.doi.org/10.1161/STROKEAHA.108.540492] [PMID: 19286580]
[51]
Shindo, A.; Tanemura, H.; Yata, K.; Hamada, K.; Shibata, M.; Umeda, Y.; Asakura, F.; Toma, N.; Sakaida, H.; Fujisawa, T.; Taki, W.; Tomimoto, H. Inflammatory biomarkers in atherosclerosis: pentraxin 3 can become a novel marker of plaque vulnerability. PLoS One, 2014, 9(6), e100045.
[http://dx.doi.org/10.1371/journal.pone.0100045] [PMID: 24936646]
[52]
Pini, R.; Faggioli, G.; Fittipaldi, S.; Pasquinelli, G.; Tonon, C.; Beltrandi, E.; Mauro, R.; Stella, A. Inflammatory mediators and cerebral embolism in carotid stenting: new markers of risk. J. Endovasc. Ther., 2013, 20(5), 684-694.
[http://dx.doi.org/10.1583/13-4354R.1] [PMID: 24093322]
[53]
Duivenvoorden, R.; Mani, V.; Woodward, M.; Kallend, D.; Suchankova, G.; Fuster, V.; Rudd, J.H.F.; Tawakol, A.; Farkouh, M.E.; Fayad, Z.A. Relationship of serum inflammatory biomarkers with plaque inflammation assessed by FDG PET/CT: the dal- PLAQUE study. JACC Cardiovasc. Imaging, 2013, 6(10), 1087-1094.
[http://dx.doi.org/10.1016/j.jcmg.2013.03.009] [PMID: 24135322]
[54]
Wang, A.; Huang, X.; Liu, X.; Su, Z.; Wu, J.; Chen, S.; Liu, X.; Ruan, C.; Guo, X.; Wu, S.; Zhao, X. No association between high-sensitivity c-reactive protein and carotid intima-media progression: the apac study. J. Stroke Cerebrovasc. Dis., 2017, 26(2), 252-259.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2016.09.013] [PMID: 27742537]
[55]
Grosse, G.M.; Schulz-Schaeffer, W.J.; Teebken, O.E.; Schuppner, R.; Dirks, M.; Worthmann, H.; Lichtinghagen, R.; Maye, G.; Limbourg, F.P.; Weissenborn, K. Monocyte subsets and related chemokines in carotid artery stenosis and ischemic stroke. Int. J. Mol. Sci., 2016, 17(4), 433.
[http://dx.doi.org/10.3390/ijms17040433] [PMID: 27023515]
[56]
Samman Tahhan, A.; Hayek, S.S.; Sandesara, P.; Hajjari, J.; Hammadah, M.; O’Neal, W.T.; Kelli, H.M.; Alkhoder, A.; Ghasemzadeh, N.; Ko, Y.A.; Aida, H.; Gafeer, M.M.; Abdelhadi, N.; Mohammed, K.H.; Patel, K.; Arya, S.; Reiser, J.; Vaccarino, V.; Sperling, L.; Quyyumi, A. Circulating soluble urokinase plasminogen activator receptor levels and peripheral arterial disease outcomes. Atherosclerosis, 2017, 264, 108-114.
[http://dx.doi.org/10.1016/j.atherosclerosis.2017.06.019] [PMID: 28728756]
[57]
Edsfeldt, A.; Nitulescu, M.; Grufman, H.; Grönberg, C.; Persson, A.; Nilsson, M.; Persson, M.; Björkbacka, H.; Gonçalves, I. Soluble urokinase plasminogen activator receptor is associated with inflammation in the vulnerable human atherosclerotic plaque. Stroke, 2012, 43(12), 3305-3312.
[http://dx.doi.org/10.1161/STROKEAHA.112.664094] [PMID: 23150653]
[58]
Olson, F.J.; Thurison, T.; Ryndel, M.; Høyer-Hansen, G.; Fagerberg, B. Soluble urokinase-type plasminogen activator receptor forms in plasma as markers of atherosclerotic plaque vulnerability. Clin. Biochem., 2010, 43(1-2), 124-130.
[http://dx.doi.org/10.1016/j.clinbiochem.2009.09.028] [PMID: 19822140]
[59]
Andersson, J.; Sundström, J.; Kurland, L.; Gustavsson, T.; Hulthe, J.; Elmgren, A.; Zilmer, K.; Zilmer, M.; Lind, L. The carotid artery plaque size and echogenicity are related to different cardiovascular risk factors in the elderly: the Prospective Investigation of the Vasculature in Uppsala Seniors (PIVUS) study. Lipids, 2009, 44(5), 397-403.
[http://dx.doi.org/10.1007/s11745-009-3281-y] [PMID: 19234732]
[60]
Hoke, M.; Winter, M.P.; Wagner, O.; Exner, M.; Schillinger, M.; Arnold, Z.; Mlekusch, W.; Maurer, G.; Koppensteiner, R.; Minar, E.; Goliasch, G. The impact of selectins on mortality in stable carotid atherosclerosis. Thromb. Haemost., 2015, 114(3), 632-638.
[http://dx.doi.org/10.1160/TH14-12-1014] [PMID: 25994120]
[61]
Pelisek, J.; Rudelius, M.; Zepper, P.; Poppert, H.; Reeps, C.; Schuster, T.; Eckstein, H.H. Multiple biological predictors for vulnerable carotid lesions. Cerebrovasc. Dis., 2009, 28(6), 601-610.
[http://dx.doi.org/10.1159/000247605] [PMID: 19844101]
[62]
Cheng, C.; Tempel, D.; van Haperen, R.; van Damme, L.; Algür, M.; Krams, R.; de Crom, R. Activation of MMP8 and MMP13 by angiotensin II correlates to severe intra-plaque hemorrhages and collagen breakdown in atherosclerotic lesions with a vulnerable phenotype. Atherosclerosis, 2009, 204(1), 26-33.
[http://dx.doi.org/10.1016/j.atherosclerosis.2009.01.025] [PMID: 19233360]
[63]
Badacz, R.; Podolec, J.; Przewlocki, T.; Siedlinski, M.; Jozefczuk, E.; Oleksy, H.; Baran, J.; Pieniazek, P.; Zmudka, K.; Kablak-Ziembicka, A. The role of chemokine CCL5/RANTES and metalloproteinase-9 as inflammatory modulators in symptomatic internal carotid artery stenosis. J. Physiol. Pharmacol., 2019, 70(4), 545-555.
[http://dx.doi.org/10.26402/jpp.2019.4.06] [PMID: 31642817]
[64]
Alvarez, B.; Ruiz, C.; Chacón, P.; Alvarez-Sabin, J.; Matas, M. Serum values of metalloproteinase-2 and metalloproteinase-9 as related to unstable plaque and inflammatory cells in patients with greater than 70% carotid artery stenosis. J. Vasc. Surg., 2004, 40(3), 469-475.
[http://dx.doi.org/10.1016/j.jvs.2004.06.023] [PMID: 15337875]
[65]
Gupta, A.; Baradaran, H.; Schweitzer, A.D.; Kamel, H.; Pandya, A.; Delgado, D.; Dunning, A.; Mushlin, A.I.; Sanelli, P.C. Carotid plaque MRI and stroke risk: a systematic review and meta-analysis. Stroke, 2013, 44(11), 3071-3077.
[http://dx.doi.org/10.1161/STROKEAHA.113.002551] [PMID: 23988640]
[66]
Katano, H.; Mase, M.; Nishikawa, Y.; Yamada, K. Calcified carotid plaques show double symptomatic peaks according to agatston calcium score. J. Stroke Cerebrovasc. Dis., 2015, 24(6), 1341-1350.
[http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2015.02.010] [PMID: 25804565]
[67]
Fisher, C.M.; Ojemann, R.G. A clinico-pathologic study of carotid endarterectomy plaques. Rev. Neurol. (Paris), 1986, 142(6-7), 573-589.
[PMID: 3797929]
[68]
Lennihan, L.; Kupsky, W.J.; Mohr, J.P.; Hauser, W.A.; Correll, J.W.; Quest, D.O. Lack of association between carotid plaque hematoma and ischemic cerebral symptoms. Stroke, 1987, 18(5), 879-881.
[http://dx.doi.org/10.1161/01.STR.18.5.879] [PMID: 3629646]
[69]
Mujaj, B.; Bos, D.; Selwaness, M.; Leening, M.J.G.; Kavousi, M.; Wentzel, J.J.; van der Lugt, A.; Hofman, A.; Stricker, B.H.; Vernooij, M.W.; Franco, O.H. Statin use is associated with carotid plaque composition: The Rotterdam Study. Int. J. Cardiol., 2018, 260, 213-218.
[http://dx.doi.org/10.1016/j.ijcard.2018.02.111] [PMID: 29519676]
[70]
Everett, B.M.; Glynn, R.J.; MacFadyen, J.G.; Ridker, P.M. Rosuvastatin in the prevention of stroke among men and women with elevated levels of C-reactive protein: justification for the Use of Statins in Prevention: an Intervention Trial Evaluating Rosuvastatin (JUPITER). Circulation, 2010, 121(1), 143-150.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.109.874834] [PMID: 20026779]
[71]
Qu, H.Y.; Xiao, Y.W.; Jiang, G.H.; Wang, Z.Y.; Zhang, Y.; Zhang, M. Effect of atorvastatin versus rosuvastatin on levels of serum lipids, inflammatory markers and adiponectin in patients with hypercholesterolemia. Pharm. Res., 2009, 26(4), 958-964.
[http://dx.doi.org/10.1007/s11095-008-9798-6] [PMID: 19082693]
[72]
Kunte, H.; Amberger, N.; Busch, M.A.; Rückert, R.I.; Meiners, S.; Harms, L. Markers of instability in high-risk carotid plaques are reduced by statins. J. Vasc. Surg., 2008, 47(3), 513-522.
[http://dx.doi.org/10.1016/j.jvs.2007.11.045] [PMID: 18295103]
[73]
Kadoglou, N.P.; Gerasimidis, T.; Moumtzouoglou, A.; Kapelouzou, A.; Sailer, N.; Fotiadis, G.; Vitta, I.; Katinios, A.; Kougias, P.; Bandios, S.; Voliotis, K.; Karayannacos, P.E.; Liapis, C.D. Intensive lipid-lowering therapy ameliorates novel calcification markers and GSM score in patients with carotid stenosis. Eur. J. Vasc. Endovasc. Surg., 2008, 35(6), 661-668.
[http://dx.doi.org/10.1016/j.ejvs.2007.12.011] [PMID: 18395477]
[74]
Kadoglou, N.P.; Sailer, N.; Moumtzouoglou, A.; Kapelouzou, A.; Gerasimidis, T.; Liapis, C.D. Aggressive lipid-lowering is more effective than moderate lipid-lowering treatment in carotid plaque stabilization. J. Vasc. Surg., 2010, 51(1), 114-121.
[http://dx.doi.org/10.1016/j.jvs.2009.07.119] [PMID: 19837545]
[75]
Ikonomidis, I.; Stamatelopoulos, K.; Lekakis, J.; Vamvakou, G.D.; Kremastinos, D.T. Inflammatory and non-invasive vascular markers: the multimarker approach for risk stratification in coronary artery disease. Atherosclerosis, 2008, 199(1), 3-11.
[http://dx.doi.org/10.1016/j.atherosclerosis.2008.02.019] [PMID: 18378239]
[76]
Bal Dit Sollier, C.; Crassard, I.; Simoneau, G.; Bergmann, J.F.; Bousser, M.G.; Drouet, L. Effect of the thromboxane prostaglandin receptor antagonist terutroban on arterial thrombogenesis after repeated administration in patients treated for the prevention of ischemic stroke. Cerebrovasc. Dis., 2009, 28(5), 505-513.
[http://dx.doi.org/10.1159/000236915] [PMID: 19752552]
[77]
Heider, P.; Poppert, H.; Wolf, O.; Liebig, T.; Pelisek, J.; Schuster, T.; Eckstein, H.H. Fibrinogen and high-sensitive C-reactive protein as serologic predictors for perioperative cerebral microembolic lesions after carotid endarterectomy. J. Vasc. Surg., 2007, 46(3), 449-454.
[http://dx.doi.org/10.1016/j.jvs.2007.05.035] [PMID: 17826232]
[78]
Gröschel, K.; Ernemann, U.; Larsen, J.; Knauth, M.; Schmidt, F.; Artschwager, J.; Kastrup, A. Preprocedural C-reactive protein levels predict stroke and death in patients undergoing carotid stenting. AJNR Am. J. Neuroradiol., 2007, 28(9), 1743-1746.
[http://dx.doi.org/10.3174/ajnr.A0650] [PMID: 17885237]
[79]
Abe, Y.; Sakaguchi, M.; Furukado, S.; Fujinaka, T.; Sakoda, S.; Yoshimine, T.; Kitagawa, K. Interleukin-6 release after carotid artery stenting and periprocedural new ischemic lesions. J. Cereb. Blood Flow Metab., 2010, 30(4), 857-863.
[http://dx.doi.org/10.1038/jcbfm.2009.250] [PMID: 19953100]
[80]
Aronow, H.D.; Shishehbor, M.; Davis, D.A.; Katzan, I.L.; Bhatt, D.L.; Bajzer, C.T.; Abou-Chebl, A.; Derk, K.W.; Whitlow, P.L.; Yadav, J.S. Leukocyte count predicts microembolic Doppler signals during carotid stenting: a link between inflammation and embolization. Stroke, 2005, 36(9), 1910-1914.
[http://dx.doi.org/10.1161/01.STR.0000177610.33478.65] [PMID: 16100016]
[81]
Kadoglou, N.P.; Avgerinos, E.D.; Liapis, C.D. An update on markers of carotid atherosclerosis in patients with Type 2 diabetes. Biomarkers Med., 2010, 4(4), 601-609.
[http://dx.doi.org/10.2217/bmm.10.79] [PMID: 20701448]
[82]
Zhao, G.; Tang, X.; Tang, H.; Lin, J.; Sun, W.; Fan, Z.; Fu, C.; Guo, D. Recent intraplaque hemorrhage is associated with a higher risk of ipsilateral cerebral embolism during carotid artery stenting. World Neurosurg., 2020, 137, e298-e307.
[http://dx.doi.org/10.1016/j.wneu.2020.01.181] [PMID: 32014542]

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