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Review

Non-invasive ultrasound-based imaging of atherosclerosis

Published Online:https://doi.org/10.1024/0301-1526/a000747

Abstract. Early detection of vascular damage in atherosclerosis and accurate assessment of cardiovascular risk factors are the basis for appropriate treatment strategies in cardiovascular medicine. The current review focuses on non-invasive ultrasound-based methods for imaging of atherosclerosis. Endothelial dysfunction is an accepted early manifestation of atherosclerosis. The most widely used technique to study endothelial function is non-invasive, flow-mediated dilation of the brachial artery under high-resolution ultrasound imaging. Although an increased intima-media thickness value is associated with future cardiovascular events in several large population studies, systematic use is not recommended in clinical practice for risk assessment of individual persons. Carotid plaque analysis with grey-scale median, 3-D ultrasound or contrast-enhanced ultrasound are promising techniques for further scientific work in prevention and therapy of generalized atherosclerosis.

Literature

  • Cattaneo M, Wyttenbach R, Corti R, Staub D & Gallino A. The Growing Field of Imaging of Atherosclerosis in Peripheral Arteries. Angiology. 2018:3319718776122. First citation in articleMedlineGoogle Scholar

  • Xu Y, Arora RC, Hiebert BM, Lerner B, Szwajcer A & McDonald K, et al. Non-invasive endothelial function testing and the risk of adverse outcomes: a systematic review and meta-analysis. Eur Heart J Cardiovasc Imaging. 2014;15(7):736–46. First citation in articleCrossref MedlineGoogle Scholar

  • Greyling A, van Mil AC, Zock PL, Green DJ, Ghiadoni L & Thijssen DH, et al. Adherence to guidelines strongly improves reproducibility of brachial artery flow-mediated dilation. Atherosclerosis. 2016;248:196–202. First citation in articleCrossref MedlineGoogle Scholar

  • Anderson TJ & Phillips SA. Assessment and prognosis of peripheral artery measures of vascular function. Progress in cardiovascular diseases. 2015;57(5):497–509. First citation in articleCrossref MedlineGoogle Scholar

  • Touboul PJ, Hennerici MG, Meairs S, Adams H, Amarenco P & Bornstein N, et al. Mannheim carotid intima-media thickness and plaque consensus (2004–2006–2011). An update on behalf of the advisory board of the 3rd, 4th and 5th watching the risk symposia, at the 13th, 15th and 20th European Stroke Conferences, Mannheim, Germany, 2004, Brussels, Belgium, 2006, and Hamburg, Germany, 2011. Cerebrovasc Dis. 2012;34(4):290–6. First citation in articleMedlineGoogle Scholar

  • Rueb K, Mynard J, Liu R, Wake M, Vuillermin P & Ponsonby AL, et al. Changes in carotid artery intima-media thickness during the cardiac cycle – a comparative study in early childhood, mid-childhood, and adulthood. Vasa. 2017;46(4):275–81. First citation in articleLinkGoogle Scholar

  • Lorenz MW, Markus HS, Bots ML, Rosvall M & Sitzer M. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation. 2007;115(4):459–67. First citation in articleCrossref MedlineGoogle Scholar

  • Huang Y, Li W, Dong L, Li R & Wu Y. Effect of statin therapy on the progression of common carotid artery intima-media thickness: an updated systematic review and meta-analysis of randomized controlled trials. J Atheroscler Thromb. 2013;20(1): 108–21. First citation in articleCrossref MedlineGoogle Scholar

  • Gebauer K & Reinecke H. PCSK9 inhibition for LDL lowering and beyond – implications for patients with peripheral artery disease. Vasa. 2018;47(3):165–76. First citation in articleLinkGoogle Scholar

  • Lorenz MW, Polak JF, Kavousi M, Mathiesen EB, Volzke H & Tuomainen TP, et al. Carotid intima-media thickness progression to predict cardiovascular events in the general population (the PROG-IMT collaborative project): a meta-analysis of individual participant data. Lancet. 2012;379(9831):2053–62. First citation in articleCrossref MedlineGoogle Scholar

  • Lorenz MW, Gao L, Ziegelbauer K, Norata GD, Empana JP & Schmidtmann I, et al. Predictive value for cardiovascular events of common carotid intima media thickness and its rate of change in individuals at high cardiovascular risk – Results from the PROG-IMT collaboration. PLoS One. 2018;13(4):e0191172. First citation in articleCrossref MedlineGoogle Scholar

  • Aschwanden M, Kesten F, Stern M, Thalhammer C, Walker UA & Tyndall A, et al. Vascular involvement in patients with giant cell arteritis determined by duplex sonography of 2x11 arterial regions. Ann Rheum Dis. 2010;69(7):1356–9. First citation in articleCrossref MedlineGoogle Scholar

  • Wohlin M, Sundstrom J, Andren B, Larsson A & Lind L. An echolucent carotid artery intima-media complex is a new and independent predictor of mortality in an elderly male cohort. Atherosclerosis. 2009;205(2):486–91. First citation in articleCrossref MedlineGoogle Scholar

  • Eikendal AL, Groenewegen KA, Bots ML, Peters SA, Uiterwaal CS & den Ruijter HM. Relation Between Adolescent Cardiovascular Risk Factors and Carotid Intima-Media Echogenicity in Healthy Young Adults: The Atherosclerosis Risk in Young Adults (ARYA) Study. J Am Heart Assoc. 2016;5(5). doi: 10.1161/JAHA.115.002941. First citation in articleCrossref MedlineGoogle Scholar

  • Andersson J, Sundstrom J, Gustavsson T, Hulthe J, Elmgren A & Zilmer K, et al. 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):612–8. First citation in articleCrossref MedlineGoogle Scholar

  • Vlachopoulos C, Aznaouridis K & Stefanadis C. Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J Am Coll Cardiol. 2010;55(13):1318–27. First citation in articleCrossref MedlineGoogle Scholar

  • Boesen ME, Singh D, Menon BK & Frayne R. A systematic literature review of the effect of carotid atherosclerosis on local vessel stiffness and elasticity. Atherosclerosis. 2015;243(1): 211–22. First citation in articleCrossref MedlineGoogle Scholar

  • Podgorski M, Grzelak P, Kaczmarska M, Polguj M, Lukaszewski M & Stefanczyk L. Feasibility of two-dimensional speckle tracking in evaluation of arterial stiffness: Comparison with pulse wave velocity and conventional sonographic markers of atherosclerosis. Vascular. 2018;26(1):63–9. First citation in articleCrossref MedlineGoogle Scholar

  • Kim CH, Wang S, Park JB, Jung KH, Yoon YE & Lee SP, et al. Assessing Impact of High-Dose Pitavastatin on Carotid Artery Elasticity with Speckle-Tracking Strain Imaging. J Atheroscler Thromb. 2018. doi: 10.5551/jat.42861. First citation in articleCrossrefGoogle Scholar

  • Schiele F, Navarese EP, Visona A & Ray K. What imaging techniques should be used in primary versus secondary prevention for further risk stratification? Atherosclerosis Supplements. 2017;26:36–44. First citation in articleCrossref MedlineGoogle Scholar

  • Piepoli MF, Hoes AW, Agewall S, Albus C, Brotons C & Catapano AL, et al. 2016 European Guidelines on cardiovascular disease prevention in clinical practice: The Sixth Joint Task Force of the European Society of Cardiology and Other Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of 10 societies and by invited experts)Developed with the special contribution of the European Association for Cardiovascular Prevention & Rehabilitation (EACPR). Eur Heart J. 2016;37(29):2315–81. First citation in articleMedlineGoogle Scholar

  • Inaba Y, Chen JA & Bergmann SR. Carotid plaque, compared with carotid intima-media thickness, more accurately predicts coronary artery disease events: a meta-analysis. Atherosclerosis. 2012;220(1):128–33. First citation in articleCrossref MedlineGoogle Scholar

  • Pelz JO, Weinreich A, Fritzsch D & Saur D. Quantification of Internal Carotid Artery Stenosis with 3D Ultrasound Angiography. Ultraschall Med. 2015;36(5):487–93. First citation in articleCrossref MedlineGoogle Scholar

  • Pelz JO, Weinreich A, Karlas T & Saur D. Evaluation of Freehand B-Mode and Power-Mode 3D Ultrasound for Visualisation and Grading of Internal Carotid Artery Stenosis. PLoS One. 2017; 12(1):e0167500. First citation in articleCrossref MedlineGoogle Scholar

  • Ball S, Rogers S, Kanesalingam K, Taylor R, Katsogridakis E & McCollum C. Carotid plaque volume in patients undergoing carotid endarterectomy. Br J Surg. 2018;105(3):262–9. First citation in articleCrossref MedlineGoogle Scholar

  • Sandholt BV, Collet-Billon A, Entrekin R & Sillesen HH. Inter-Scan Reproducibility of Carotid Plaque Volume Measurements by 3-D Ultrasound. Ultrasound Med Biol. 2018;44(3):670–6. First citation in articleCrossref MedlineGoogle Scholar

  • Jashari F, Ibrahimi P, Bajraktari G, Gronlund C, Wester P & Henein MY. Carotid plaque echogenicity predicts cerebrovascular symptoms: a systematic review and meta-analysis. Eur J Neurol. 2016;23(7):1241–7. First citation in articleCrossref MedlineGoogle Scholar

  • Kaspar M, Partovi S, Aschwanden M, Imfeld S, Baldi T & Uthoff H, et al. Assessment of microcirculation by contrast-enhanced ultrasound: a new approach in vascular medicine. Swiss Med Wkly. 2015;145:w14047. First citation in articleMedlineGoogle Scholar

  • Staub D, Partovi S, Imfeld S, Uthoff H, Baldi T & Aschwanden M, et al. Novel applications of contrast-enhanced ultrasound imaging in vascular medicine. Vasa. 2013;42(1):17–31. First citation in articleLinkGoogle Scholar

  • Schinkel AF, Kaspar M & Staub D. Contrast-enhanced ultrasound: clinical applications in patients with atherosclerosis. The international journal of cardiovascular imaging. 2016;32(1): 35–48. First citation in articleCrossref MedlineGoogle Scholar

  • Partovi S, Loebe M, Aschwanden M, Baldi T, Jager KA & Feinstein SB, et al. Contrast-enhanced ultrasound for assessing carotid atherosclerotic plaque lesions. AJR Am J Roentgenol. 2012; 198(1):W13–9. First citation in articleCrossref MedlineGoogle Scholar

  • Sluimer JC & Daemen MJ. Novel concepts in atherogenesis: angiogenesis and hypoxia in atherosclerosis. The Journal of pathology. 2009;218(1):7–29. First citation in articleCrossref MedlineGoogle Scholar

  • Hellings WE, Peeters W, Moll FL, Piers SR, van Setten J & Van der Spek PJ, et al. Composition of carotid atherosclerotic plaque is associated with cardiovascular outcome: a prognostic study. Circulation. 2010;121(17):1941–50. First citation in articleCrossref MedlineGoogle Scholar

  • Coli S, Magnoni M, Sangiorgi G, Marrocco-Trischitta MM, Melisurgo G & Mauriello A, et al. Contrast-enhanced ultrasound imaging of intraplaque neovascularization in carotid arteries: correlation with histology and plaque echogenicity. J Am Coll Cardiol. 2008;52(3):223–30. First citation in articleCrossref MedlineGoogle Scholar

  • Staub D, Partovi S, Schinkel AF, Coll B, Uthoff H & Aschwanden M, 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. First citation in articleCrossref MedlineGoogle Scholar

  • Staub D, Patel MB, Tibrewala A, Ludden D, Johnson M & Espinosa P, et al. Vasa vasorum and plaque neovascularization on contrast-enhanced carotid ultrasound imaging correlates with cardiovascular disease and past cardiovascular events. Stroke. 2010;41(1):41–7. First citation in articleCrossref MedlineGoogle Scholar

  • van den Oord SC, Akkus Z, Bosch JG, Hoogi A, ten Kate GL & Renaud G, et al. Quantitative contrast-enhanced ultrasound of intraplaque neovascularization in patients with carotid atherosclerosis. Ultraschall Med. 2015;36(2):154–61. First citation in articleMedlineGoogle Scholar

  • Li C, He W, Guo D, Chen L, Jin X & Wang W, et al. Quantification of carotid plaque neovascularization using contrast-enhanced ultrasound with histopathologic validation. Ultrasound Med Biol. 2014;40(8):1827–33. First citation in articleCrossref MedlineGoogle Scholar

  • Sidhu PS, Cantisani V, Dietrich CF, Gilja OH, Saftoiu A & Bartels E, et al. The EFSUMB Guidelines and Recommendations for the Clinical Practice of Contrast-Enhanced Ultrasound (CEUS) in Non-Hepatic Applications: Update 2017 (Short Version). Ultraschall Med. 2018;39(2):154–80. First citation in articleCrossref MedlineGoogle Scholar

  • Xu B, Xing J, Wu W, Zhang WJ, Zhu QQ & Zhang D, 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. First citation in articleMedlineGoogle Scholar

  • Catapano AL, Graham I, De Backer G, Wiklund O, Chapman MJ & Drexel H, et al. 2016 ESC/EAS Guidelines for the Management of Dyslipidaemias. Eur Heart J. 2016;37(39):2999–3058. First citation in articleCrossref MedlineGoogle Scholar