Novel approaches to assessing the signs of atherosclerotic plaque instability in the carotid arteries

Cover Page

Cite item

Full Text


Introduction. Application of contrast agents in vascular untrasonography has become a new direction in noninvasive assessment of signs of atherosclerotic plaque (ASP) instability; the type of plaque neovascularization being the major sign. However, questions regarding the accuracy of the methods for quantitative evaluation of plaque neovascularization are still to be answered.

Objective. To evaluate signs of ASP instability in the carotid arteries according to the contrast-enhanced duplex scanning data and to elaborate our own approach to quantitative evaluation of neovascularization.

Materials and methods. Twenty-six patients with carotid atherosclerosis who had been subjected to carotid endarterectomy (n=27) followed by morphological plaque verification were enrolled in this study. All patients underwent standard duplex scanning and scanning using contrast agent SonoVue.

Results. Neovascularization was revealed in all 27 patients with ASP according to the pathomorphological and contrast-enhanced ultrasonography data. The total number of vessels per cm2 of plaque was 6–51 [21±14/cm2] according to the ultrasonography data and 19–1224 [236±249/cm2] according to the pathomorphological examination. According to the ultrasonography data, the absolute values were close to the density of plaque vessels ≥ 30 μm in diameter determined during pathomorphological examination and did not differ significantly from this value (p = 0.67). The morphology data show that vessels <20 μm in diameter, which constituted up to 96% of all microvessels in ASP, cannot be detected by ultrasonography. In one case, ulceration of the ASP surface was detected only by contrast medium injection. Calcified plaques with different degrees of calcination imposed the greatest difficulties when performing ultrasonic assessment of neovascularization.

Conclusions. Contrast-enhanced untrasonography can be used as an informative method to noninvasively detect signs of ASP instability enabling rather accurate assessment of neovascularization at microvessel diameter ≥30 μm. Calcification of ASPs may significantly affect the study results.

About the authors

Andrey O. Chechetkin

Research Center of Neurology

Author for correspondence.
ORCID iD: 0000-0002-8726-8928

D. Sci. (Med.), Head, Ultrasound diagnostic laboratory

Russian Federation, Moscow

Lyudmila D. Druina

Research Center of Neurology

Russian Federation, Moscow

Anna N. Evdokimenko

Research Center of Neurology

Russian Federation, Moscow

Tat'yana S. Gulevskaya

Research Center of Neurology

Russian Federation, Moscow

Sergey I. Skrylev

Research Center of Neurology

Russian Federation, Moscow

Marine M. Tanashyan

Research Center of Neurology

ORCID iD: 0000-0002-5883-8119

D. Sci. (Med.), Prof., Corresponding member of RAS, Deputy Director for science, Head, 1st Neurological department

Russian Federation, Moscow


  1. Tanashyan М.М., Lagoda O.V., Gulevskaya Т.S. et al. [Progressive cerebral atherosclerosis: clinical, biochemical and morphological aspects]. Annals of Clinical and Experimental Neurology. 2013; 7 (4): 4–9. (In Russ.)
  2. Tanashyan М.М., Lagoda O.V. [Carotid atherosclerosis and ischaemic cerebrovascular accidents]. Klinicheskaya farmakologiya i terapiya. 2011; 20 (5): 79–82. (In Russ.)
  3. [National guidelines for management of patients with diseases of carotid arteries]. Angiology and Vascular Surgery. 2013; 19 (2). (In Russ.)
  4. Tanashyan М.М., Suslina Z.A., Ionov V.G. et al. [Status of endothelial function in patients with ischemic stroke with atherosclerosis of the carotid arteries of varying degrees]. Nerologichesky vestnik. Zhurnal im. V.M. Bekhtereva. 2007; XXXIX (1): 12–16. (In Russ.)
  5. Alonso A., Artemis D., Hennerici M. Molecular Imaging of Carotid Plaque Vulnerability. Cerebrovasc Dis. 2015; 39 (1): 5–12. doi: 10.1159/000369123. PMID: 25547782.
  6. Doyle B., Caplice N. Plaque neovascularization and antiangiogenic therapy for atherosclerosis. J Am Coll Cardiol. 2007; 49 (21): 2073–80. DOI: 10.1016/j. jacc.2007.01.089. PMID: 17531655.
  7. Dunmore B., McCarthy M., Naylor A. et al. Carotid plaque instability and ischemic symptoms are linked to immaturity of microvessels within plaques. J Vasc Surg 2007; 45(1): 155–9. doi: 10.1016/j.jvs.2006.08.072. PMID: 17210401.
  8. Mofidi R., Crotty T., McCarthy P. et al. Association between plaque instability, angiogenesis and symptomatic carotid occlusive disease. Br J Surg. 2001; 88 (7): 945–50. doi: 10.1046/j.0007-1323.2001.01823.x. PMID: 11442525.
  9. Hellings W., Peeters W., Moll F. et al. Composition of carotid atherosclerotic plaque is associated with cardiovascular outcome: a prognostic study. Circulation. 2010; 121 (17):1941–50. doi: 10.1161/CIRCULATIONAHA.109.887497. PMID: 20404256.
  10. Howard D., van Lammeren G., Rothwell P. et al. Symptomatic carotid atherosclerotic disease: correlations between plaque composition and ipsilateral stroke risk. Stroke 2015; 46 (1):182–9. doi: 10.1161/STROKEAHA.114.007221 PMID: 25477221.
  11. [SonoVue. The dynamic contrast enhancement in real time]. Scientific monograph. 2013; 6–40. (In Russ.)
  12. Feinstein S. The powerful microbubble: from bench to bedside, from intravascular indicator to therapeutic delivery system, and beyond. Am J Physiol Heart Circ Physiol 2004; 287(2): H450–7. doi: 10.1152/ajpheart.00134.2004. PMID: 15277188.
  13. Saha S., Gourineni V., Feinstein S. The Use of Contrast-enhanced Ultrasonography for Imaging of Carotid Atherosclerotic Plaques: Current Evidence, Future Directions. Neuroimaging Clin N Am. 2016; 26 (1): 81–96. DOI: 10.1016/j. nic.2015.09.007. PMID: 26610662.
  14. Filis K., Toufektzian L., Galyfos G. et al. Assessment of the vulnerable carotid atherosclerotic plaque using contrast-enhanced ultrasonography. Vascular. 2016. doi: 10.1177/1708538116665734. PMID: 27580821.
  15. Gray-Weale A., Graham J., Burnett J. et al. Carotid artery atheroma: comparison of preoperative B-mode ultrasound appearance with carotid endarterectomy specimen pathology. J Cardiovasc Surg (Torino). 1988; 29(6): 676–81. PMID: 3062007.
  16. Kaspar M., Partovi S., Aschwanden M. et al. Assessment of microcirculation by contrast-enhanced ultrasound: a new approach in vascular medicine. Swiss Med Wkly 2015; 145: w14047. doi: 10.4414/smw.2015.14047. PMID: 25588141
  17. Müller H., Viaccoz A., Kuzmanovic I. et al. Contrast-enhanced ultrasound imaging of carotid plaque neo-vascularization: accuracy of visual analysis. Ultrasound Med Biol. 2014; 40(1): 18–24. doi: 10.1016/j.ultrasmedbio.2013.08.012.
  18. Hjelmgren O., Johansson L., Prahl U. et al. A study of plaque vascularization and inflammation using quantitative contrast-enhanced US and PET/CT. Eur J Radiol 2014; 83 (7): 1184–9. doi: 10.1016/j.ejrad.2014.03.021. PMID: 24767629.
  19. Hoogi A., Adam D., Hoffman A. et al. Carotid Plaque Vulnerability: Quantification of Neovascularization on Contrast-Enhanced Ultrasound With Histopathologic Correlation. American Journal of Roentgenology. 2011; 196: 431–436. doi: 10.2214/AJR.10.4522. PMID: 21257897.
  20. Saito K., Nagatsuka K., Ishibashi-Ueda H. et al. Contrast-enhanced ultrasound for the evaluation of neovascularization in atherosclerotic carotid artery plaques. Stroke 2014; 45 (10): 3073–5. doi: 10.1161/STROKEAHA. 114.006483. PMID: 25158775.
  21. Xiong L., Deng Y.B., Zhu Y. et al. Correlation of carotid plaque neovascularization detected by using contrast-enhanced US with clinical symptoms. Radiology. 2009; 251 (2): 583–9. doi: 10.1148/radiol.2512081829. PMID: 19304920.
  22. Giannoni M., Vicenzini E., Citone M. et al. Contrast carotid ultrasound for the detection of unstable plaques with neoangiogenesis: a pilot study. Eur J Vasc Endovasc Surg 2009; 37 (6): 722–7. doi: 10.1016/j.ejvs.2008.12.028. PMID: 19328729.
  23. Staub D., Partovi S., Schinkel A. et al. Correlation of carotid artery atherosclerotic lesion echogenicity and severity at standard US with intraplaque neovascularization detected at contrast-enhanced US. Radiology. 2011; 258 (2): 618–26. doi: 10.1148/radiol.10101008. PMID: 20971776.
  24. ten Kate G., Sijbrands E., Staub D. et al. Noninvasive imaging of the vulnerable atherosclerotic plaque. Curr Probl Cardiol 2010; 35: 556–591. doi: 10.1016/j.cpcardiol.2010.09.002. PMID: 20974314.

Supplementary files

Supplementary Files

Copyright (c) 2017 Chechetkin A.O., Druina L.D., Evdokimenko A.N., Gulevskaya T.S., Skrylev S.I., Tanashyan M.M.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77-83204 от 12.05.2022.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies