Contrast-enhanced carotid ultrasound: current status
https://doi.org/10.15829/1560-4071-2019-12-114-123
Abstract
Unstable atherosclerotic plaques (ASP) are the cause of acute ischemia in the carotid and coronary systems. Numerous studies have shown a relationship between plaque instability, manifestations, echogenicity, histological findings and its neovascularization. The presence and extent of ASP neovascularization in the carotid arteries can be detected for the first time using contrast-enhanced carotid ultrasound. Contrast-enhanced carotid ultrasound does not have nephrotoxic effect; it also improves the accuracy of plaque ulceration detecting and determining the severity of stenosis. The article presents the opinions of the authors and international experts on contrast ultrasound of peripheral arteries. An analysis of the literature data and our own observations is presented. Significant parameters such as the doses, procedure onset time and duration, methods for the qualitative and quantitative assessment of plaque neovascularization are analyzed. The difficulties of contrast-enhanced ultrasound are described.
About the Authors
O. A. PogorelovaRussian Federation
Moscow
M. I. Tripoten
Russian Federation
Moscow
T. V. Balakhonova
Russian Federation
Moscow
References
1. Kakkos SK, Griffin MB, Nicolaides AN, et al. The size of juxtaluminal hypoechoic area in ultrasound images of asymptomatic carotid plaques predicts the occurrence of stroke. J. Vasc. Surg. 2013;57(3):609-18. doi:10.1016/j.jvs.2012.09.045.
2. Picano E, Paterni M. Ultrasound tissue characterization of vulnerable atherosclerotic plaque. Int J Mol Sci. 2015;16:10121-33. doi:10.3390/ijms160510121.
3. Coli S, Magnoni M, Sangiorgi G, et al. Contrast-enhanced ultrasound imaging of intraplaque neovascularization in carotid arteries: correlation with histology and plaque echogenicity. J Am Coll Cardiol. 2008;52:223-30. doi:10.1016/j.jacc.2008.02.082.
4. Giannoni MF, 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;37:722-7. doi:10.1016/j.ejvs.2008.12.028.
5. Zhang Q, Li C, Han H, et al. Spatiotemporal quantification of carotid plaque neovascularization on contrast enhanced ultrasound: correlation with visual grading and histopathology. Eur J Vasc Endovas Surg. 2015;50:289-96. doi:10.1016/j. ejvs.2015.06.077.
6. Li C, He W, Guo D, et al. Quantification of carotid plaque neovascularization using contrastehanced ultrasound with histopathologic validation. Ultrasound Med Biol. 2014;40:182733. doi:10.1016/j.ultrasmedbio.2014.02.010.
7. Vavuranakis M, Sigala F, Vrachatis DA, et al. Quantitative analysis of carotid plaque vasa vasorum by CEUS and correlation with histology after endarterectomy. VASA.2013;42:18495. doi:10.1024/0301-1526/a000267.
8. Xiong L, Deng YB, Zhu Y, et al. Correlation of carotid plaque neovascularization detected by using contrast-enhanced us with clinical symptoms. Radiology. 2009;251:583-9. doi:10.1148/radiol.2512081829.
9. Staub D, Partovi S, Schinkel AF, et al. Correlation of carotid artery atherosclerotic lesion echogenicity and severity at standard US with intraplaque neovascularization detected at contrast-enhanced US. Radiology. 2011;258:618-26. doi:10.1148/radiol.10101008.
10. Owen DR, Shalhoub J, Miller S, et al. Inflammation within carotid atherosclerotic plaque: assessment with late-phase contrast-enhanced US. Radiology. 2010;255:638-44. doi:10.1148/radiol.10091365.
11. Shalhoub J, Monaco C, Owen DR, et al. Late-phase contrast-enhanced ultrasound reflects biological features of instability in human carotid atherosclerosis. Stroke.2011;42:3634-6. doi:10.1161/STROKEAHA.111.631200.
12. Nakamura J, Nakamura T, Deyama J, et al. Assessment of carotid plaque neovascularization using quantitative analysis of contrast-enhanced ultrasound imaging is useful for risk stratification in patients with coronary artery disease. Int J Cardiol. 2015;195:113-9. doi:10.1016/j.ijcard.2015.05.107.
13. Deyama J, Nakamura T, Takishima I, et al. Contrast-enhanced ultrasound imaging of carotid plaque neovascularization is useful for identifying high-risk patients with coronary artery disease. Circ J. 2013;77:1499-507. doi:10.1253/circj.cj-12-1529.
14. Sidhu PS, Cantisani V, Dietrich CF, et al. The EFSUMB guidelines and recommendations for the clinical practice of Contrast-Enhanced Ultrasound (CEUS) in non-hepatic applications: update 2017 (long version) Ultraschall Med. 2018;39(2):e2-e44. doi:10.1055/a-0586-1107.
15. Stein JH, Korcarz CE, Hurst RT, et al. Use of carotid ultrasound to identify subclinical vascular disease and evaluate cardiovascular disease risk: a consensus statement from the American Society of Echocardiography Carotid Intima-Media Thickness Task Force endorsed by the society for vascular medicine. J Am Soc Echocardiogr. 2008;21(2):93111;189-90. doi:10.1016/j.echo.2007.11.011.
16. Touboul P-J, Hennerici MG, Meairs S, et al. Mannheim Carotid Intima-Media Thickness and Plaque Consensus (2004-2006-2011). Cerebrovasc Dis. 2012;34:290-6. doi:10.1159/000343145.
17. European Carotid Surgery Trialists’ Collaborative Group. MRC European Carotid Surgery Trial: interim results for symptomatic patients with severe (70-99%) or with mild (0-29%) carotid stenosis. Lancet. 1991;337:1235-43.
18. Hjelmgren O, Johansson L, Prahl U, et al A study of plaque vascularization and inflammation usingquantitative contrast-enhanced US and PET/CT. Eur J Radiol. 2014;83(7):1184-9. doi:10.1016/j.ejrad.2014.03.021.
19. Hoogi A, Adam D, Hoffman A, et al. Carotid plaque vulnerability: quantification of neovascularization on contrast-enhanced ultrasound with histopathologic correlation. AJR. 2011;196(2):431-6. doi:10.2214/AJR.10.4522.
20. Van den Oord SC, Akkus Z, Bosch JG, et al. Quantitative contrast-enhanced ultrasound of intraplaque neovascularization in patients with carotid atherosclerosis. Ultraschall Med. 2015;36(2):154-61. doi:10.1055/s-0034-1366410.
21. Ten Kate GL, van den Oord SC, Sijbrands EJ, et al. Current status and future developments of contrast-enhanced ultrasound of carotid atherosclerosis. J Vasc Surg. 2013;57:539-46. doi:10.1016/j.jvs.2012.07.028.
22. Piscaglia F, Nolsøe C, Dietrich CF, et al. The EFSUMB Guidelines and recommendations on the clinical practice of Contrast Enhanced Ultrasound (CEUS): update 2011 on non-hepatic applications. Ultraschall Med. 2012;33(1):33-59. doi:10.1055/s-0031-1281676.
23. Chechetkin AO, Druina LD, Evdokimenko AN, et al. Novel approaches to assessing the signs of atherosclerotic plaque instability in the carotid arteries. Annals of Clinical and Experimental Neurology. 2017;11(1):47-54. (In Russ.)
24. Timina IE, Askerova NN, Karmazanovsky GG, et al. Contrast-enhanced ultrasonographic study in patients with lower limb arterial lesions. Angiology and Vascular Surgery. 2018;24(2).41-8. (In Russ.)
25. Staub D, Partovi S, Imfeld S, et al. Novel applications of contrast-enhanced ultrasound imaging in vascular medicine. Vasa. 2013;42:17-31. doi:10.1024/0301-1526/a000244.
26. 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.
27. Dietrich CF, Averkiou MA, Correas J-M, et al. An EFSUMB introduction into Dynamic ContrastEnhanced Ultrasound (DCE-US) for quantification of tumour perfusion. Ultraschall in Med. 2012;33:344-51. doi:10.1055/s-0032-1313026.
28. Kern R, Szabo K, Hennerici M, et al. Characterization of carotid artery plaques using real-time compound B-mode ultrasound. Stroke. 2004;35:870-5. doi:10.1161/01. STR.0000120728.72958.4A.
29. Staub D, Patel MB, Tibrewala A, et al. Vasa vasorum and plaque neovascularization on contrastenhanced carotid ultrasound imaging correlates with cardiovascular disease and past cardiovascular events. Stroke. 2010;41(1):41-7. doi:10.1161/STROKEAHA.109.560342.
30. Saha SA, Gourineni V, Feinstein SB. The use of contrast-enhanced ultrasonography for imaging of carotid atherosclerotic plaques current evidence, future directions. Neuroimag Clin N Am. 2016;26:81-96. doi:10.1016/j.nic.2015.09.007.
31. Shah F, Balan P, Weinberg M, et al. Contrast-enhanced ultrasound imaging of atherosclerotic carotid plaque neovascularization: a new surrogate marker of atherosclerosis? Vasc Med. 2007;12(4):291-7. doi:10.1177/1358863X07083363.
32. Huang XZ, Wang ZY, Dai XH, et al. Velocity vector imaging of longitudinal mechanical properties of upstream and downstream shoulders and fibrous cap tops of human carotid atherosclerotic plaque. Echocardiography. 2013;30(2):211-8. doi:10.1111/echo.12005.
33. Dirksen MT, van der Wal AC, van den Berg FM, et al. Distribution of inflammatory cells in atherosclerotic plaques relates to the direction of flow. Circulation. 1998;98:2000-3. doi:10.1161/01.cir.98.19.2000.
34. Huang PT, Huang FG, Zou CP, et al. Contrast-enhanced sonographic characteristics of neovascularization in carotid atherosclerotic plaques. J Clin Ultrasound. 2008;36:346-51. doi:10.1002/jcu.20448.
35. Seidel G, Meairs S. Ultrasound contrast agents in ischemic stroke. Cerebrovasc Dis. 2009;27(2):25-39. doi:10.1159/000203124.
36. Hoogi A, Akkus Z, van den Oord SCH, et al. Quantitative analysis of ultrasound contrast flow behavior in carotid plaque neovasculature. Ultrasound Med Biol. 2012;38:2072-83. doi:10.1016/j.ultrasmedbio.2012.08.002.
37. Akkus Z, Renaud G, van den Oord SCH, et al. New quantification methods for carotid intra-plaque neovascularization using contrast-enhanced ultrasound. Ultrasound in Med Biol. 2014;40(1):25-36. doi:10.1016/j.ultrasmedbio.2013.09.010.
38. Xu B, Xing J, Wu W, et al. Improved plaque neovascularization following 2-year atorvastatin therapy based on contrast-enhanced ultrasonography: A pilot study. Experimental and therapeutic medicine. 2018;15(5):4491-7. doi:10.3892/etm.2018.5926.
Review
For citations:
Pogorelova O.A., Tripoten M.I., Balakhonova T.V. Contrast-enhanced carotid ultrasound: current status. Russian Journal of Cardiology. 2019;(12):114-123. (In Russ.) https://doi.org/10.15829/1560-4071-2019-12-114-123