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Contrast-enhanced ultrasound of the carotid system: a review of the current literature

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Abstract

Carotid disease is a major current health problem accounting for a significant part of stroke patients. Ultrasound with colour Doppler and spectral analysis is the primary imaging technique used for screening and diagnostic evaluation of the extracranial part of carotid arteries offering identification and grading of carotid disease. However, inherent limitations of this technique include flow-related artefacts like Doppler angle dependence and aliasing artefact which may sometimes hinder complete assessment of a stenotic part of the vessel, potentially failing to address clinically significant differential diagnosis issues. The intravenous use of microbubbles as an US contrast agent has been introduced for the supplementation of conventional technique. The value of contrast-enhanced ultrasound (CEUS) has been investigated in the evaluation of carotid disease leading to promising results. CEUS provides improved flow visualization free of artefacts and detailed plaque surface delineation, thus being able to accurately grade stenosis, identify carotid plaque ulcerations, differentiate occlusion from highly stenotic plaques and identify carotid dissection. Furthermore, microbubbles can be used to identify and grade intraplaque neovascularization, carotid wall inflammation in patients with arteritis, follow-up patients after carotid intervention and assist interventional procedures reducing the need for nephrotoxic contrast agents. The purpose of this review is to present and discuss the current literature regarding the various uses of CEUS in carotid arteries.

Riassunto

La malattia carotidea rappresenta un grosso problema attuale di una parte significativa dei pazienti con ictus. L’ecografia con color Doppler e l’analisi spettrale è la metodica di imagine di prima istanza utilizzata per lo screening e la valutazione diagnostica della parte extracraniale delle arterie carotidee che offre l’identificazione e la classificazione della malattia carotidea. Tuttavia le limitazioni intrinseche di questa tecnica includono gli artefatti connessi al flusso, come dipendenza dall’angolo Doppler e l’artefatto aliasing che talvolta possono ostacolare la valutazione totale di una parte stenotica del vaso, avendo ad affrontare potenzialmente significativi problemi clinici di diagnosi differenziale. L’ uso endovenoso di microbolle come agente di contrasto nell’ecografia è stato introdotto per la supplementazione della tecnica convenzionale. Il valore del mezzo di contrasto nell’ ecografia (CEUS) è stato studiato per la valutazione della patologia carotidea e sta portando risultati promettenti. CEUS offre una migliore visualizzazione dettagliatta, libera da artefatti di flusso della placca e la delineazione della superficie essendo così in grado di precisare il grado di stenosi ed identificare ulzerazioni della placca carotidea, differenziare l’occlusione dalle placche altamente stenotiche e identificare la dissezione carotidea. Inoltre, le microbolle possono essere utilizzate per l’identificazione del grado di neovascolarizzazione intraplacca, l’infiammazione della parete carotidea in pazienti con l’arterite, di eseguire il follow-up dei pazienti dopo l’intervento carotideo e assistere le procedure interventistiche riducendo la necessità di mezzi di contrasto nefrotossici. Lo scopo di questa rassegna è quello di presentare e discutere la letteratura attuale per quando riguarda i vari usi di CEUS nelle arterie carotidee.

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References

  1. Grau AJ, Weimar C, Buggle F et al (2001) Risk factors, outcome, and treatment in subtypes of ischemic stroke: the German stroke data bank. Stroke 32:2559–2566. doi:10.1161/hs1101.098524

    Article  CAS  PubMed  Google Scholar 

  2. Krogias C, Kerasnoudis A (2012) Detection of microembolic signals and ultrasonic brain perfusion imaging in symptomatic carotid artery disease. Nevrologia-gr 21:36–46

    Google Scholar 

  3. Eckstein HH, Kuhnl A, Dorfler A et al (2013) The diagnosis, treatment and follow-up of extracranial carotid stenosis. Dtsch Arztebl Int 110:468–476. doi:10.3238/arztebl.2013.0468

    PubMed  PubMed Central  Google Scholar 

  4. Kernan WN, Ovbiagele B, Black HR et al (2014) 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 45:2160–2236. doi:10.1161/STR.0000000000000024

    Article  PubMed  Google Scholar 

  5. Saba L, Anzidei M, Marincola BC et al (2014) Imaging of the carotid artery vulnerable plaque. Cardiovasc Intervent Radiol 37:572–585. doi:10.1007/s00270-013-0711-2

    Article  PubMed  Google Scholar 

  6. Adams HP Jr, Bendixen BH, Kappelle LJ, Biller J, Love BB, Gordon DL, Marsh EE 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. doi:10.1161/01.STR.24.1.35

    Article  PubMed  Google Scholar 

  7. Bonati LH, Nederkoorn PJ (2016) Clinical perspective of carotid plaque imaging. Neuroimaging Clin N Am 26:175–182. doi:10.1016/j.nic.2015.09.012

    Article  PubMed  Google Scholar 

  8. (1991) MRC European Carotid Surgery Trial: interim results for symptomatic patients with severe (70–99%) or with mild (0–29%) carotid stenosis. European Carotid Surgery Trialists’ Collaborative Group. Lancet 337(8752):1235–1243

  9. North American Symptomatic Carotid Endarterectomy Trial Collaborators (1991) Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 325:445–453. doi:10.1056/NEJM199108153250701

    Article  Google Scholar 

  10. Naylor AR, Rothwell PM, Bell PR (2003) Overview of the principal results and secondary analyses from the European and North American randomised trials of endarterectomy for symptomatic carotid stenosis. Eur J Vasc Endovasc Surg 26:115–129. doi:10.1053/ejvs.2002.1946

    Article  CAS  PubMed  Google Scholar 

  11. Halliday A, Mansfield A, Marro J et al (2004) Prevention of disabling and fatal strokes by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet 363:1491–1502. doi:10.1016/S0140-6736(04)16146-1

    Article  CAS  PubMed  Google Scholar 

  12. Freilinger TM, Schindler A, Schmidt C et al (2012) Prevalence of nonstenosing, complicated atherosclerotic plaques in cryptogenic stroke. JACC Cardiovasc Imaging 5:397–405. doi:10.1016/j.jcmg.2012.01.012

    Article  PubMed  Google Scholar 

  13. Lanzino G, Rabinstein AA, Brown RD Jr (2009) Treatment of carotid artery stenosis: medical therapy, surgery, or stenting? Mayo Clin Proc 84:362–387. doi:10.1016/S0025-6196(11)60546-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Grant EG, Benson CB, Moneta GL et al (2003) Carotid artery stenosis: gray-scale and Doppler US diagnosis–Society of Radiologists in Ultrasound Consensus Conference. Radiology 229:340–346. doi:10.1148/radiol.2292030516

    Article  PubMed  Google Scholar 

  15. Cantisani V, Ricci P, Grazhdani H et al (2011) Prospective comparative analysis of colour-Doppler ultrasound, contrast-enhanced ultrasound, computed tomography and magnetic resonance in detecting endoleak after endovascular abdominal aortic aneurysm repair. Eur J Vasc Endovasc Surg 41:186–192. doi:10.1016/j.ejvs.2010.10.003

    Article  CAS  PubMed  Google Scholar 

  16. Cantisani V, David E, Mauro L, D’Ambrosio F, Clevert DA (2015) CEUS: what is its role in abdominal aortic diseases? Med Ultrason 17:419–421. doi:10.11152/mu.2013.2066.173.zsp

    PubMed  Google Scholar 

  17. Piscaglia F, Nolsoe C, Dietrich CF et al (2012) The EFSUMB Guidelines and Recommendations on the Clinical Practice of Contrast Enhanced Ultrasound (CEUS): update 2011 on non-hepatic applications. Ultraschall Med 33:33–59. doi:10.1055/s-0031-1281676

    Article  CAS  PubMed  Google Scholar 

  18. Ten Kate GL, van den Oord SC, Sijbrands EJ et al (2013) Current status and future developments of contrast-enhanced ultrasound of carotid atherosclerosis. J Vasc Surg 57:539–546. doi:10.1016/j.jvs.2012.07.028

    Article  PubMed  Google Scholar 

  19. Varetto G, Gibello L, Castagno C et al (2015) Use of contrast-enhanced ultrasound in carotid atherosclerotic disease: limits and perspectives. BioMed Res Int 2015:293163. doi:10.1155/2015/293163

    Article  PubMed  PubMed Central  Google Scholar 

  20. Schinkel AF, Kaspar M, Staub D (2016) Contrast-enhanced ultrasound: clinical applications in patients with atherosclerosis. Int J Cardiovasc Imaging 32:35–48. doi:10.1007/s10554-015-0713-z

    Article  PubMed  Google Scholar 

  21. Clevert DA, Paprottka P, Sommer WH, Helck A, Reiser MF, Zengel P (2013) The role of contrast-enhanced ultrasound in imaging carotid arterial diseases. Sem Ultrasound CT MR 34:204–212. doi:10.1053/j.sult.2012.11.011

    Article  Google Scholar 

  22. Staub D, Partovi S, Imfeld S, Uthoff H, Baldi T, Aschwanden M, Jaeger K (2013) Novel applications of contrast-enhanced ultrasound imaging in vascular medicine. Vasa 42:17–31. doi:10.1024/0301-1526/a000244

    Article  PubMed  Google Scholar 

  23. Piscaglia F, Bolondi L, Italian Society for Ultrasound in M, Biology Study Group on Ultrasound Contrast A (2006) The safety of Sonovue in abdominal applications: retrospective analysis of 23188 investigations. Ultrasound Med Biol 32:1369–1375. doi:10.1016/j.ultrasmedbio.2006.05.031

    Article  PubMed  Google Scholar 

  24. ter Haar G (2009) Safety and bio-effects of ultrasound contrast agents. Med Biol Eng Comput 47:893–900. doi:10.1007/s11517-009-0507-3

    Article  PubMed  Google Scholar 

  25. Clevert DA, Sommer WH, Zengel P, Helck A, Reiser M (2011) Imaging of carotid arterial diseases with contrast-enhanced ultrasound (CEUS). Eur J Radiol 80:68–76. doi:10.1016/j.ejrad.2010.12.103

    Article  CAS  PubMed  Google Scholar 

  26. Mozzini C, Roscia G, Casadei A, Cominacini L (2016) Searching the perfect ultrasonic classification in assessing carotid artery stenosis: comparison and remarks upon the existing ultrasound criteria. J Ultrasound 19:83–90. doi:10.1007/s40477-016-0193-6

    Article  PubMed  Google Scholar 

  27. Casadei A, Floreani M, Catalini R, Serra C, Assanti AP, Conci P (2012) Sonographic characteristics of carotid artery plaques: implications for follow-up planning? J Ultrasound 15:151–157. doi:10.1016/j.jus.2012.06.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Clevert DA, Horng A, Clevert DA, Jung EM, Sommer WH, Reiser M (2009) Contrast-enhanced ultrasound versus conventional ultrasound and MS-CT in the diagnosis of abdominal aortic dissection. Clin Hemorheol Microcirc 43:129–139. doi:10.3233/CH-2009-1227

    PubMed  Google Scholar 

  29. Furst G, Sitzer M, Hofer M, Steinmetz H, Hacklander T, Modder U (1995) Contrast-enhanced color-coded duplex ultrasound of high grade carotid stenoses. Ultraschall Med 16:140–144. doi:10.1055/s-2007-1003928

    Article  CAS  PubMed  Google Scholar 

  30. Partovi S, Loebe M, Aschwanden M, Baldi T, Jager KA, Feinstein SB, Staub D (2012) Contrast-enhanced ultrasound for assessing carotid atherosclerotic plaque lesions. AJR Am J Roentgenol 198:W13–W19. doi:10.2214/AJR.11.7312

    Article  PubMed  Google Scholar 

  31. ten Kate GL, Sijbrands EJ, Staub D, Coll B, ten Cate FJ, Feinstein SB, Schinkel AF (2010) Noninvasive imaging of the vulnerable atherosclerotic plaque. Curr Probl Cardiol 35:556–591. doi:10.1016/j.cpcardiol.2010.09.002

    Article  PubMed  Google Scholar 

  32. Sirlin CB, Lee YZ, Girard MS, Peterson TM, Steinbach GC, Baker KG, Mattrey RF (2001) Contrast-enhanced B-mode US angiography in the assessment of experimental in vivo and in vitro atherosclerotic disease. Acad Radiol 8:162–172

    Article  CAS  PubMed  Google Scholar 

  33. Kono Y, Pinnell SP, Sirlin CB, Sparks SR, Georgy B, Wong W, Mattrey RF (2004) Carotid arteries: contrast-enhanced US angiography–preliminary clinical experience. Radiology 230:561–568. doi:10.1148/radiol.2302020318

    Article  PubMed  Google Scholar 

  34. Lee KW, Park YJ, Rho YN, Kim DI, Kim YW (2011) Measurement of carotid artery stenosis: correlation analysis between B-mode ultrasonography and contrast arteriography. J Korean Surg Soc 80:348–354. doi:10.4174/jkss.2011.80.5.348

    Article  PubMed  PubMed Central  Google Scholar 

  35. Sidhu PS, Allan PL, Cattin F et al (2006) Diagnostic efficacy of SonoVue, a second generation contrast agent, in the assessment of extracranial carotid or peripheral arteries using colour and spectral Doppler ultrasound: a multicentre study. Br J Radiol 79:44–51. doi:10.1259/bjr/23954854

    Article  CAS  PubMed  Google Scholar 

  36. van den Oord SC, ten Kate GL, Akkus Z et al (2013) Assessment of subclinical atherosclerosis using contrast-enhanced ultrasound. Eur Heart J Cardiovasc Imaging 14:56–61. doi:10.1093/ehjci/jes109

    Article  PubMed  Google Scholar 

  37. ten Kate GL, van Dijk AC, van den Oord SC et al (2013) Usefulness of contrast-enhanced ultrasound for detection of carotid plaque ulceration in patients with symptomatic carotid atherosclerosis. Am J Cardiol 112:292–298. doi:10.1016/j.amjcard.2013.03.028

    Article  PubMed  Google Scholar 

  38. Eliasziw M, Streifler JY, Fox AJ, Hachinski VC, Ferguson GG, Barnett HJ (1994) Significance of plaque ulceration in symptomatic patients with high-grade carotid stenosis. North American Symptomatic Carotid Endarterectomy Trial. Stroke 25:304–308. doi:10.1161/01.STR.25.2.304

    Article  CAS  PubMed  Google Scholar 

  39. Barnett HJ, Taylor DW, Eliasziw M et al (1998) Benefit of carotid endarterectomy in patients with symptomatic moderate or severe stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators. N Engl J Med 339:1415–1425. doi:10.1056/NEJM199811123392002

    Article  CAS  PubMed  Google Scholar 

  40. Fisher M, Paganini-Hill A, Martin A, Cosgrove M, Toole JF, Barnett HJ, Norris J (2005) Carotid plaque pathology: thrombosis, ulceration, and stroke pathogenesis. Stroke 36:253–257. doi:10.1161/01.STR.0000152336.71224.21

    Article  PubMed  Google Scholar 

  41. van den Oord SC, Akkus Z, Renaud G, Bosch JG, van der Steen AF, Sijbrands EJ, Schinkel AF (2014) Assessment of carotid atherosclerosis, intraplaque neovascularization, and plaque ulceration using quantitative contrast-enhanced ultrasound in asymptomatic patients with diabetes mellitus. Eur Heart J Cardiovasc Imaging 15:1213–1218. doi:10.1093/ehjci/jeu127

    Article  PubMed  Google Scholar 

  42. Hammond CJ, McPherson SJ, Patel JV, Gough MJ (2008) Assessment of apparent internal carotid occlusion on ultrasound: prospective comparison of contrast-enhanced ultrasound, magnetic resonance angiography and digital subtraction angiography. Eur J Vasc Endovasc Surg 35:405–412. doi:10.1016/j.ejvs.2007.12.008

    Article  CAS  PubMed  Google Scholar 

  43. Clevert DA, Johnson T, Michaely H et al (2006) High-grade stenoses of the internal carotid artery: comparison of high-resolution contrast enhanced 3D MRA, duplex sonography and power Doppler imaging. Eur J Radiol 60:379–386. doi:10.1016/j.ejrad.2006.07.012

    Article  PubMed  Google Scholar 

  44. Jung EM, Kubale R, Ritter G, Gallegos MT, Jungius KP, Rupp N, Clevert DA (2007) Diagnostics and characterisation of preocclusive stenoses and occlusions of the internal carotid artery with B-flow. Eur Radiol 17:439–447. doi:10.1007/s00330-006-0285-3

    Article  CAS  PubMed  Google Scholar 

  45. Clevert DA, Johnson T, Jung EM et al (2007) Color Doppler, power Doppler and B-flow ultrasound in the assessment of ICA stenosis: comparison with 64-MD-CT angiography. Eur Radiol 17:2149–2159. doi:10.1007/s00330-006-0488-7

    Article  PubMed  Google Scholar 

  46. Leffers AM, Wagner A (2000) Neurologic complications of cerebral angiography. A retrospective study of complication rate and patient risk factors. Acta Radiol 41:204–210. doi:10.1080/028418500127345299

    Article  CAS  PubMed  Google Scholar 

  47. Neff KW, Kilian AK, Meairs S, Duber C (2005) Correlation of duplex sonographic stenosis grading by means of cross-sectional analysis and MR-tomographic blood volume flow quantification in unilateral stenosis of the internal carotid artery. Rofo 177:992–999. doi:10.1055/s-2005-858288

    Article  CAS  PubMed  Google Scholar 

  48. Hwang CS, Liao KM, Lee JH, Tegeler CH (2003) Measurement of carotid stenosis: comparisons between duplex and different angiographic grading methods. J Neuroimaging 13:133–139. doi:10.1111/j.1552-6569.2003.tb00169.x

    Article  PubMed  Google Scholar 

  49. Holden A, Hope JK, Osborne M, Moriarty M, Lee K (2000) Value of a contrast agent in equivocal carotid ultrasound studies: pictorial essay. Australas Radiol 44:253–260. doi:10.1046/j.1440-1673.2000.00809.x

    Article  CAS  PubMed  Google Scholar 

  50. Ferrer JM, Samso JJ, Serrando JR, Valenzuela VF, Montoya SB, Docampo MM (2000) Use of ultrasound contrast in the diagnosis of carotid artery occlusion. J Vasc Surg 31:736–741. doi:10.1067/mva.2000.104599

    Article  CAS  PubMed  Google Scholar 

  51. Droste DW, Jurgens R, Nabavi DG, Schuierer G, Weber S, Ringelstein EB (1999) Echocontrast-enhanced ultrasound of extracranial internal carotid artery high-grade stenosis and occlusion. Stroke 30:2302–2306. doi:10.1161/01.STR.30.11.2302

    Article  CAS  PubMed  Google Scholar 

  52. Ohm C, Bendick PJ, Monash J et al (2005) Diagnosis of total internal carotid occlusions with duplex ultrasound and ultrasound contrast. Vasc Endovasc Surg 39:237–243. doi:10.1177/153857440503900304

    Article  Google Scholar 

  53. Ventura CA, Silva ES, Cerri GG, Leao PP, Tachibana A, Chammas MC (2015) Can contrast-enhanced ultrasound with second-generation contrast agents replace computed tomography angiography for distinguishing between occlusion and pseudo-occlusion of the internal carotid artery? Clinics (Sao Paulo) 70:1–6. doi:10.6061/clinics/2015(01)01

    Article  Google Scholar 

  54. Hofstee DJ, Hoogland PH, Schimsheimer RJ, de Weerd AW (2000) Contrast enhanced color duplex for diagnosis of subtotal stenosis or occlusion of the internal carotid artery. Clin Neurol Neurosurg 102:9–12

    Article  CAS  PubMed  Google Scholar 

  55. Clevert DA, Sommer WH, Helck A, Saam T, Reiser M (2011) Improved carotid atherosclerotic plaques imaging with contrast-enhanced ultrasound (CEUS). Clin Hemorheol Microcirc 48:141–148. doi:10.3233/CH-2011-1403

    CAS  PubMed  Google Scholar 

  56. Yoshida K, Nozaki K, Kikuta K, Sadato A, Miyamoto S, Hashimoto N (2003) Contrast-enhanced carotid color-coded duplex sonography for carotid stenting follow-up assessment. AJNR Am J Neuroradiol 24:992–995

    PubMed  Google Scholar 

  57. Nammuni I, Batt P, Erlich J, Varcoe RL (2013) Adjunctive ultrasonography during carotid artery stenting to minimize iodine contrast use. J Clin Ultrasound 41:323–326. doi:10.1002/jcu.21902

    Article  PubMed  Google Scholar 

  58. Varcoe RL, Nammuni I, Lennox AF, Yang JL, Crowe P, Walsh WR (2012) Adjunctive ultrasonography to minimize iodinated contrast administration during carotid artery stenting: a randomized trial. J Endovasc Ther 19:638–647. doi:10.1583/JEVT-12-3918R.1

    Article  PubMed  Google Scholar 

  59. Saha SA, Gourineni V, Feinstein SB (2016) The use of contrast-enhanced ultrasonography for imaging of carotid atherosclerotic plaques: current evidence, future directions. Neuroimaging Clin N Am 26:81–96. doi:10.1016/j.nic.2015.09.007

    Article  PubMed  Google Scholar 

  60. Langheinrich AC, Kampschulte M, Buch T, Bohle RM (2007) Vasa vasorum and atherosclerosis—Quid novi? Thromb Haemost 97:873–879. doi:10.1160/TH06-12-0742

    CAS  PubMed  Google Scholar 

  61. Moreno PR, Purushothaman KR, Sirol M, Levy AP, Fuster V (2006) Neovascularization in human atherosclerosis. Circulation 113:2245–2252. doi:10.1161/CIRCULATIONAHA.105.578955

    Article  PubMed  Google Scholar 

  62. Granada JF, Feinstein SB (2008) Imaging of the vasa vasorum. Nat Clin Pract Cardiovasc Med. 5:S18–S25. doi:10.1038/ncpcardio1157

    Article  PubMed  Google Scholar 

  63. Leen E, Moug SJ, Horgan P (2004) Potential impact and utilization of ultrasound contrast media. Eur Radiol 14:P16–P24

    Article  PubMed  Google Scholar 

  64. Shalhoub J, Owen DR, Gauthier T, Monaco C, Leen EL, Davies AH (2010) The use of contrast enhanced ultrasound in carotid arterial disease. Eur J Vasc Endovasc Surg 39:381–387. doi:10.1016/j.ejvs.2009.12.011

    Article  CAS  PubMed  Google Scholar 

  65. Feinstein SB (2004) The powerful microbubble: from bench to bedside, from intravascular indicator to therapeutic delivery system, and beyond. Am J Physiol Heart Circ Physiol 287:H450–H457. doi:10.1152/ajpheart.00134.2004

    Article  CAS  PubMed  Google Scholar 

  66. Coli S, Magnoni M, Sangiorgi G et al (2008) Contrast-enhanced ultrasound imaging of intraplaque neovascularization in carotid arteries: correlation with histology and plaque echogenicity. J Am Coll Cardiol 52:223–230. doi:10.1016/j.jacc.2008.02.082

    Article  PubMed  Google Scholar 

  67. Giannoni MF, Vicenzini E, Citone M et al (2009) Contrast carotid ultrasound for the detection of unstable plaques with neoangiogenesis: a pilot study. Eur J Vasc Endovasc Surg 37:722–727. doi:10.1016/j.ejvs.2008.12.028

    Article  CAS  PubMed  Google Scholar 

  68. Hoogi A, Adam D, Hoffman A, Kerner H, Reisner S, Gaitini D (2011) Carotid plaque vulnerability: quantification of neovascularization on contrast-enhanced ultrasound with histopathologic correlation. AJR Am J Roentgenol 196:431–436. doi:10.2214/AJR.10.4522

    Article  PubMed  Google Scholar 

  69. Shah F, Balan P, Weinberg M et al (2007) Contrast-enhanced ultrasound imaging of atherosclerotic carotid plaque neovascularization: a new surrogate marker of atherosclerosis? Vasc Med 12:291–297. doi:10.1177/1358863X07083363

    Article  PubMed  Google Scholar 

  70. Li C, He W, Guo D et al (2014) Quantification of carotid plaque neovascularization using contrast-enhanced ultrasound with histopathologic validation. Ultrasound Med Biol 40:1827–1833. doi:10.1016/j.ultrasmedbio.2014.02.010

    Article  PubMed  Google Scholar 

  71. Xiong L, Deng YB, Zhu Y, Liu YN, Bi XJ (2009) Correlation of carotid plaque neovascularization detected by using contrast-enhanced US with clinical symptoms. Radiology 251:583–589. doi:10.1148/radiol.2512081829

    Article  PubMed  Google Scholar 

  72. van den Oord SC, Akkus Z, Bosch JG et al (2015) Quantitative contrast-enhanced ultrasound of intraplaque neovascularization in patients with carotid atherosclerosis. Ultraschall Medizin 36:154–161. doi:10.1055/s-0034-1366410

    Google Scholar 

  73. Giannoukas AD, Sfyroeras GS, Griffin M, Saleptsis V, Antoniou GA, Nicolaides AN (2009) Association of plaque echostructure and cardiovascular risk factors with symptomatic carotid artery disease. Vasa 38:357–364. doi:10.1024/0301-1526.38.4.357

    Article  CAS  PubMed  Google Scholar 

  74. Staub D, Partovi S, Schinkel AF et al (2011) Correlation of carotid artery atherosclerotic lesion echogenicity and severity at standard US with intraplaque neovascularization detected at contrast-enhanced US. Radiology 258:618–626. doi:10.1148/radiol.10101008

    Article  PubMed  Google Scholar 

  75. Vicenzini E, Giannoni MF, Puccinelli F et al (2007) Detection of carotid adventitial vasa vasorum and plaque vascularization with ultrasound cadence contrast pulse sequencing technique and echo-contrast agent. Stroke 38:2841–2843. doi:10.1161/STROKEAHA.107.487918

    Article  PubMed  Google Scholar 

  76. Faggioli GL, Pini R, Mauro R et al (2011) Identification of carotid ‘vulnerable plaque’ by contrast-enhanced ultrasonography: correlation with plaque histology, symptoms and cerebral computed tomography. Eur J Vasc Endovasc Surg 41:238–248. doi:10.1016/j.ejvs.2010.11.002

    Article  CAS  PubMed  Google Scholar 

  77. Saito K, Nagatsuka K, Ishibashi-Ueda H, Watanabe A, Kannki H, Iihara K (2014) Contrast-enhanced ultrasound for the evaluation of neovascularization in atherosclerotic carotid artery plaques. Stroke 45:3073–3075. doi:10.1161/STROKEAHA.114.006483

    Article  CAS  PubMed  Google Scholar 

  78. Zhou Y, Xing Y, Li Y et al (2013) An assessment of the vulnerability of carotid plaques: a comparative study between intraplaque neovascularization and plaque echogenicity. BMC Med Imaging 13:13. doi:10.1186/1471-2342-13-13

    Article  PubMed  PubMed Central  Google Scholar 

  79. Owen DR, Shalhoub J, Miller S, Gauthier T, Doryforou O, Davies AH, Leen EL (2010) Inflammation within carotid atherosclerotic plaque: assessment with late-phase contrast-enhanced US. Radiology 255:638–644. doi:10.1148/radiol.10091365

    Article  PubMed  Google Scholar 

  80. Tian J, Hu S, Sun Y et al (2013) Vasa vasorum and plaque progression, and responses to atorvastatin in a rabbit model of atherosclerosis: contrast-enhanced ultrasound imaging and intravascular ultrasound study. Heart 99:48–54. doi:10.1136/heartjnl-2012-302775

    Article  PubMed  Google Scholar 

  81. Eyding J, Geier B, Staub D (2011) Current strategies and possible perspectives of ultrasonic risk stratification of ischemic stroke in internal carotid artery disease. Ultraschall Med 32:267–273. doi:10.1055/s-0029-1245924

    Article  CAS  PubMed  Google Scholar 

  82. Guillon B, Bousser MG (2002) Epidemiology and pathophysiology of spontaneous cervical artery dissection. J Neuroradiol 29:241–249. doi:JNR-12-2002-29-4-0150-9861-101019-ART7

    CAS  PubMed  Google Scholar 

  83. Dziewas R, Konrad C, Drager B et al (2003) Cervical artery dissection–clinical features, risk factors, therapy and outcome in 126 patients. J Neurol 250:1179–1184. doi:10.1007/s00415-003-0174-5

    Article  PubMed  Google Scholar 

  84. Massalha K, Goyen M, Rudofsky G (1999) Stenosis-jet can cause a dissection of the superficial femoral artery. Vasa 28:131–133. doi:10.1024/0301-1526.28.2.131

    Article  CAS  PubMed  Google Scholar 

  85. Koennecke HC, Trocio SH Jr, Mast H, Mohr JP (1997) Microemboli on transcranial Doppler in patients with spontaneous carotid artery dissection. J Neuroimaging 7:217–220

    Article  CAS  PubMed  Google Scholar 

  86. Li ZJ, Luo XH, Du LF (2015) Identification of carotid artery dissection by contrast enhanced ultrasonograph. A case report. Med Ultrason 17:564–565. doi:10.11152/mu.2013.2066.174.aca

    PubMed  Google Scholar 

  87. Clevert DA, Kubisch C, Meimarakis G, Zengel P, Reiser M (2010) Improved visualization of carotid-jugular arteriovenous fistula by contrast-enhanced ultrasound. Ultraschall Medizin 31:610–612. doi:10.1055/s-0029-1245589

    Article  Google Scholar 

  88. Giannoni MF, Irace L, Vicenzini E, Massa R, Gossetti B, Benedetti-Valentini F (2009) Carotid body tumors: advantages of contrast ultrasound investigation. J Neuroimaging 19:388–390. doi:10.1111/j.1552-6569.2008.00323.x

    Article  PubMed  Google Scholar 

  89. Skountzos G, Eustathiou M, Pappas A, et al (2015) Paraganglioma of the carotid body: correlation of CEUS and MDCT findings. EURORAD. doi:10.1594/EURORAD/CASE.13147. http://www.eurorad.org/eurorad/case.php?id=13147&lang=fr. Accessed 25 July 2016

  90. Schinkel AF, van den Oord SC, van der Steen AF, van Laar JA, Sijbrands EJ (2014) Utility of contrast-enhanced ultrasound for the assessment of the carotid artery wall in patients with Takayasu or giant cell arteritis. Eur Heart J Cardiovasc Imaging 15:541–546. doi:10.1093/ehjci/jet243

    Article  PubMed  Google Scholar 

  91. Magnoni M, Dagna L, Coli S, Cianflone D, Sabbadini MG, Maseri A (2011) Assessment of Takayasu arteritis activity by carotid contrast-enhanced ultrasound. Circ Cardiovasc Imaging 4:e1–e2. doi:10.1161/CIRCIMAGING.110.960906

    Article  PubMed  Google Scholar 

  92. Giordana P, Baque-Juston MC, Jeandel PY, Mondot L, Hirlemann J, Padovani B, Raffaelli C (2011) Contrast-enhanced ultrasound of carotid artery wall in Takayasu disease: first evidence of application in diagnosis and monitoring of response to treatment. Circulation 124:245–247. doi:10.1161/CIRCULATIONAHA.110.006668

    Article  CAS  PubMed  Google Scholar 

  93. ten Kate GL, Renaud GG, Akkus Z et al (2012) Far-wall pseudoenhancement during contrast-enhanced ultrasound of the carotid arteries: clinical description and in vitro reproduction. Ultrasound Med Biol 38:593–600. doi:10.1016/j.ultrasmedbio.2011.12.019

    Article  PubMed  Google Scholar 

  94. van den Oord SC, Renaud G, Bosch JG, de Jong N, van der Steen AF, Schinkel AF (2013) Far wall pseudo-enhancement: a neglected artifact in carotid contrast-enhanced ultrasound? Atherosclerosis 229:451–452. doi:10.1016/j.atherosclerosis.2013.04.036

    Article  PubMed  Google Scholar 

  95. Kaufmann BA, Sanders JM, Davis C, Xie A, Aldred P, Sarembock IJ, Lindner JR (2007) Molecular imaging of inflammation in atherosclerosis with targeted ultrasound detection of vascular cell adhesion molecule-1. Circulation 116:276–284. doi:10.1161/CIRCULATIONAHA.106.684738

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The author VR has received a scholarship for his PhD studies on “Imaging of the carotid vulnerable plaque with contrast-enhanced ultrasound and multi-detector computed tomography angiography” from the Alexander S. Onassis Public Benefit Foundation (Grant Number G ZJ 050-2/2015-2016).

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Authors and Affiliations

  1. Department of Radiology, AHEPA University General Hospital, Aristotle University of Thessaloniki, St. Kiriakidi 1, 54636, Thessaloníki, Greece

    Vasileios Rafailidis, Afroditi Charitanti, Evangelos Destanis & Ioannis Chryssogonidis

  2. 1st Neurological Department, AHEPA University General Hospital, Aristotle University of Thessaloniki, Thessaloníki, Greece

    Thomas Tegos

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  1. Vasileios Rafailidis
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  2. Afroditi Charitanti
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Correspondence to Vasileios Rafailidis.

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Rafailidis, V., Charitanti, A., Tegos, T. et al. Contrast-enhanced ultrasound of the carotid system: a review of the current literature. J Ultrasound 20, 97–109 (2017). https://doi.org/10.1007/s40477-017-0239-4

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  • DOI: https://doi.org/10.1007/s40477-017-0239-4

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