Download PDF
Ultraschall Med 2021; 42(04): 348-366
DOI: 10.1055/a-1403-2400
Continuing Medical Education

Role of CEUS in Vascular Pathology

Stellenwert von CEUS in der Gefäßpathologie
Vito Cantisani
1   Department of Radiological, Oncological and Anatomopathological Sciences-Radiology, „Sapienza“ University of Rome, Rome, Italy, Universita degli Studi di Roma La Sapienza, Roma, Italy
,
Nicola Di Leo
1   Department of Radiological, Oncological and Anatomopathological Sciences-Radiology, „Sapienza“ University of Rome, Rome, Italy, Universita degli Studi di Roma La Sapienza, Roma, Italy
,
Emanuele David
2   Radiological Sciences, Radiology Unit, Papardo-Hospital, Messina, Italy, Messina, Italy.
,
Dirk-André Clevert
3   Department of Clinical Radiology, University of Munich-Großhadern Campus, Munich, Germany
› Author Affiliations
› Further Information
Also available at
    Permissions and Reprints

Abstract

In recent years, the implementation of contrast-enhanced ultrasound (CEUS) in clinical practice has opened new horizons in the arterial pathologies research field, since this technique is able to supply new sets of data that can be crucial in patient management. The main applications of CEUS in the arterial system are the detection, characterization, and follow-up of carotid plaques and endoleaks after EVAR. Other situations in which CEUS was demonstrated to be a useful tool are large vessel vasculitis, dissections, and untreated aneurysms. In carotid atherosclerosis CEUS is not only able to acquire quantitative data about stenosis but also to perform a qualitative assessment of the plaque. The most important plaque features that CEUS is able to depict are ulceration, neovascularization, and the presence of inflammatory infiltrates. All of these factors contribute to plaque vulnerability. Thus, CEUS is crucial in order to allow better risk stratification and management of patients. In follow-up after EVAR, CEUS shows sensitivity and specificity values similar to CTA while ensuring several advantages, such as lower cost and the absence of ionizing radiation and nephrotoxic agents. Moreover, CEUS is able to offer real-time evaluation of endoleaks and thus is a useful tool in cases that are ambiguous on CTA. Most limitations are patient-related and are the same as in all other ultrasound techniques, such as high BMI and meteorism.

Zusammenfassung

In den letzten Jahren hat der Einsatz des kontrastverstärkten Ultraschalls (CEUS) in der klinischen Praxis neue Horizonte auf dem Forschungsgebiet der arteriellen Pathologien eröffnet, da diese Technik neue Datensätze liefern kann, die von entscheidender Bedeutung für das Patientenmanagement sein können.

Die Hauptanwendungen von CEUS beim arteriellen System sind Nachweis, Charakterisierung und Verlaufskontrolle von Karotisplaques sowie von Endoleaks nach EVAR. Andere Fälle, in denen sich CEUS als nützliches Instrument erwiesen hat, betreffen die Vaskulitiden großer Gefäße, Dissektionen und nicht behandelte Aneurysmen.

Bei Arteriosklerose der A. carotis kann CEUS nicht nur quantitative Daten zur Stenose erfassen, sondern auch eine qualitative Beurteilung der Plaque durchführen. Die wichtigsten Plaque-Merkmale, die CEUS darstellen kann, sind Ulzeration, Neovaskularisation und das Vorhandensein von entzündlichen Infiltraten. Alle diese Faktoren tragen zur Vulnerabilität der Plaque bei. Daher ist CEUS von entscheidender Bedeutung, um die Risikostratifizierung und das Management der Patienten zu verbessern.

In der Nachsorge nach EVAR zeigt CEUS ähnliche Sensitivitäts- und Spezifitätswerte wie die CTA und bietet gleichzeitig mehrere Vorteile, wie z. B. geringere Kosten sowie Verzicht auf Strahlenbelastung und auf nephrotoxische Substanzen. Darüber hinaus ermöglicht CEUS die Echtzeit-Evaluierung von Endoleaks, ein wertvolles Instrument für Fälle, in denen die CTA nicht eindeutig ist. Die meisten Einschränkungen sind patientenbezogen und bei allen anderen Ultraschalltechniken gleich, wie z. B. ein hoher BMI und Meteorismus.



Publication History

Article published online:
29 April 2021

© 2021. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • Literatur

  • 1 Rübenthaler J, Reiser M, Clevert DA. Diagnostic vascular ultrasonography with the help of color Doppler and contrast-enhanced ultrasonography. Ultrasonography 2016; 35: 289-301
    CrossrefPubMedGoogle Scholar
  • 2 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 in Med 2018; 39: e2-e44
    Article in Thieme ConnectPubMedGoogle Scholar
  • 3 Di Leo N, Venturini L, de Soccio V. et al. Multiparametric ultrasound evaluation with CEUS and shear wave elastography for carotid plaque risk stratification. Journal of Ultrasound 2018; 21: 293-300
    CrossrefPubMedGoogle Scholar
  • 4 Clevert DA, Sommer WH, Helck A. et al. Improved carotid atherosclerotic plaques imaging with contrast-enhanced ultrasound (CEUS). Clin Hemorheol Microcirc 2011; 48: 141-148
    CrossrefPubMedGoogle Scholar
  • 5 Clevert DA, Paprottka P, Sommer WH. et al. The role of contrast-enhanced ultrasound in imaging carotid arterial diseases. Semin Ultrasound CT MR 2013; 34: 204-212
    CrossrefPubMedGoogle Scholar
  • 6 Clevert DA, Helck A, Paprottka PM. et al. Contrast-enhanced ultrasound imaging of the carotid artery. Radiologe 2011; 51: 483-489
    CrossrefPubMedGoogle Scholar
  • 7 Li Z, Luo X, Du L. Identification of carotid artery dissection by contrast enhanced ultrasonography. A case report. Med Ultrason 2015; 17: 564-565
    PubMedGoogle Scholar
  • 8 Clevert DA, Sommer WH, Zengel P. et al. Imaging of carotid arterial diseases with contrast-enhanced ultrasound (CEUS). Eur J Radiol 2011; 80: 68-76
    CrossrefPubMedGoogle Scholar
  • 9 Schinkel AFL, van den Oord SCH, van der Steen AFW. et al. Utility of contrast-enhanced ultrasound for the assessment of the carotid artery wall in patients with Takayasu or giant cell arteritis. European Heart Journal – Cardiovascular Imaging 2014; 15: 541-546
    CrossrefPubMedGoogle Scholar
  • 10 Possemato N, Macchioni P, Germano G. et al. Clinical images: PET-CT and contrast-enhanced ultrasound in Takayasu’s arteritis. Rheumatology (Oxford) 2014; 53: 447
    CrossrefPubMedGoogle Scholar
  • 11 Clevert DA, Sommer WH, Helck A. et al. Doplex and contrast enhanced ultrasound (CEUS) in evaluation of in-stent restenosis after carotid stenting. Clin Hemorheol Microcirc 2011; 48: 199-208
    CrossrefPubMedGoogle Scholar
  • 12 Clevert DA, Kubisch C, Meimarakis G. et al. Improved Visualization of Carotid-Jugular Arteriovenous Fistula by Contrast-Enhanced Ultra- sound. Ultraschall in Med 2010; 31: 610-612
    Article in Thieme ConnectPubMedGoogle Scholar
  • 13 Biasi GM, Froio A, Diethrich EB. et al. Carotid plaque echolucency increases the risk of stroke in carotid stenting: the Imaging in Carotid Angioplasty and Risk of Stroke (ICAROS) Study. Circulation 2004; 110: 756-762
    CrossrefPubMedGoogle Scholar
  • 14 Setacci C, Chisci E, Setacci F. et al. Siena carotid artery stenting score: a risk modeling study for individual patients. Stroke 2010; 41: 1259-1265
    CrossrefPubMedGoogle Scholar
  • 15 Wolfe CD, Giroud M, Kolominsky-Rabas P. et al. European Registries of Stroke (EROS) Collaboration. Variations in stroke incidence and survival in 3 areas of Europe. Stroke 2000; 31: 2074-2079
    CrossrefPubMedGoogle Scholar
  • 16 Dziewas R, Konrad C, Dräger B. et al. Cervical artery dissection clinical features, risk factors, therapy and outcome in 126 patients. J Neurol 2003; 250: 1179-1184
    CrossrefPubMedGoogle Scholar
  • 17 Reges DS, Mazzeo M, Rosalino R. et al. Cervical arterial dissection: clinical characteristics in a neurology service in São Paulo, Brazil. Arq Neuropsiquiatr 2019; 77: 632-637
    CrossrefPubMedGoogle Scholar
  • 18 Schievink WI, Mokri B, Whisnant JP. Internal carotid artery dissection in a community. Rochester, Minnesota, 1987-1992. Stroke 1993; 24: 1678-1680
    CrossrefPubMedGoogle Scholar
  • 19 Schinkel AFL, van den Oord SCH, van der Stehen AFW. et al. Utility of contrast-enhanced ultrasound for the assessment of the carotid artery wall in patients with Takayasu or giant cell arteritis. European Heart Journal – Cardiovascular Imaging 2014; 15: 541-546
    CrossrefPubMedGoogle Scholar
  • 20 Weyand CM, Goronzy JJ. Medium- and large-vessel vasculitis. N Engl J Med 2003; 349: 160-169
    CrossrefPubMedGoogle Scholar
  • 21 Watanabe Y, Miyata T, Tanemoto K. Current Clinical Features of New Patients With Takayasu Arteritis Observed From Cross-Country Research in Japan: Age and Sex Specificity. Circulation 2015; 132: 1701-1709
    CrossrefPubMedGoogle Scholar
  • 22 Pinto Ventura CA, Simao da Silva E, Cerri GG. Can contrast-enhanced ultrasound with second- generation contrast agents replace computed tomo- graphy angiography for distinguishing between occlusion and pseudo-occlusion of the internal carotid artery?. CLINICS 2015; 70: 1-6
    CrossrefPubMedGoogle Scholar
  • 23 Sieron D, Wiggerman P, Laniado M. Carotid Artery Stenosis: Comparison of 3D Time-of-Flight MR Angiography and Contrast-Enhanced MR Angiography at 3T. Radiol Res Pract 2014; 2014: 508715
    PubMedGoogle Scholar
  • 24 Gupta A, Baradaran H, Mtui EE. et al. Detection of Symptomatic Carotid Plaque Using Source Data From MR and CT Angiography: A Correlative Study. Cerebrovasc Dis 2015; 39: 151-161
    CrossrefPubMedGoogle Scholar
  • 25 Baradaran H, Al-Dasuqi K, Knight-Greenfield A. et al. Association between Carotid Plaque Features on CTA and Cerebrovascular Ischemia: A Systematic Review and Meta-Analysis. American Journal of Neuroradiology December 2017;  38:  2321-2326
    CrossrefPubMedGoogle Scholar
  • 26 ten Kate GL, van Dijk AC, van den Oord SCH. et al. Usefulness of Con- trast-Enhanced Ultrasound for Detection of Carotid Plaque Ulceration in Patients With Symptomatic Carotid  Atherosclerosis. Am J Cardiol 2013; 112: 292-298
    CrossrefPubMedGoogle Scholar
  • 27 Coli S, Magnoni M, Sangiorgi G. et al. Contrast-Enhanced Ultrasound Imaging of Intraplaque Neovascularization in Carotid Arteries: Corre- lation With Histology and Plaque Echogenicity. J Am Coll Cardiol 2008; 52: 223-230
    CrossrefPubMedGoogle Scholar
  • 28 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: 722-727
    CrossrefPubMedGoogle Scholar
  • 29 Zhang Q, Li C, Han H. et al. Spatio-temporal Quantification of Carotid Plaque Neovascularization on Contrast Enhanced Ultrasound: Correlation with Visual Grading and Histopathology. Eur J Vasc Endovas Surg 2015; 50: 289-296
    CrossrefPubMedGoogle Scholar
  • 30 Li C, He W, Guo D. et al. Quantification of Carotid Plaque Neovascularization Using Contrast-Enhanced Ultrasound With Histopathologic Validation. Ultrasound Med Biol 2014; 40: 1827-1833
    CrossrefPubMedGoogle Scholar
  • 31 Shalhoub J, Owen DRJ, Gauthier T. et al. The use of Contrast Enhanced Ultrasound in Carotid Arterial Disease. Eur J Vasc Endovasc Surg 2010; 39: 381.e387
    CrossrefPubMedGoogle Scholar
  • 32 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: 3073-3075
    CrossrefPubMedGoogle Scholar
  • 33 Hoogi A, Akkus Z, van den Oord SC. et al. Quantita- tive analysis of ultrasound contrast flow behavior in carotid plaque neovasculature. Ultrasound Med Biol 2012; 38: 2072-2083
    CrossrefPubMedGoogle Scholar
  • 34 van den Oord SC, Akkus Z, Bosch JG. et al. Quantitative contrast enhanced ultrasound of intraplaque neovascularization in patients with carotid atherosclerosis. Ultraschall in Med 2015; 36: 154-161
    PubMedGoogle Scholar
  • 35 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 in Med 2012; 33: 33-59
    Article in Thieme ConnectPubMedGoogle Scholar
  • 36 Cantisani V, David E, Mauro L. et al. CEUS: what is its role in abdominal aortic diseases?. Med Ultrason 2015; 17 (04) 419-421
    PubMedGoogle Scholar
  • 37 Cao P, De Rango P, Verzini F. et al. Endoleak after endovascular aortic repair: classification, diagnosis and management following endovascular thoracic and abdominal aortic repair. J Cardiovasc Surg 2010; 51: 53-69
    PubMedGoogle Scholar
  • 38 Mehta M, Sternbach Y, Taggert JB. et al. Long-term outcomes of secondary procedures after endovascular aneurysm repair. J Vasc Surg 2010; 52: 1442-1449
    CrossrefPubMedGoogle Scholar
  • 39 Thurnher S, Cejna M. Imaging of aortic stent-grafts and endoleaks. Radiol Clin North Am 2002; 40: 799-833
    CrossrefPubMedGoogle Scholar
  • 40 Carrafiello G, Laganà D, Recaldini C. et al. Comparison of contrast-enhanced ultrasound and computed tomography in classifying endoleaks after endovascular treatment of abdominal aorta aneurysms: preliminary experience. Cardiovasc Intervent Radiol 2006; 29: 969-974
    CrossrefPubMedGoogle Scholar
  • 41 Wieners G, Meyer F, Halloul Z. et al. Detection of type II endoleak after endovascular aortic repair: comparison between magnetic resonance angiography and blood-pool contrast agent and dual-phase computed tomography angiography. Cardiovasc Intervent Radiol 2010; 33: 1135-1142
    CrossrefPubMedGoogle Scholar
  • 42 Froelich MF, Wolfgang GK, Su HK. et al Cost-Effectiveness of Contrast-Enhanced Ultrasound (CEUS) for the Detection of Endovascular Aortic Repair-Related Endoleaks Requiring Treatment. J Vasc Surg 2020. doi:S0741-5214(20)31245-3
    PubMedGoogle Scholar
  • 43 Cantisani V, David E, Ferrari D. et al. Color Doppler Ultrasound with Superb Microvascular Imaging Compared to Contrast-enhanced Ultrasound and Computed Tomography Angiography to Identify and Classify Endoleaks in Patients Undergoing EVAR. Ann Vasc Surg 2017; 40: 136-145
    CrossrefPubMedGoogle Scholar
  • 44 David E, Cantisani V, Grazhdani H. et al. What is the role of contrast-enhanced ultrasound in the evaluation of the endoleak of aortic endoprostheses? A comparison between CEUS and CT on a widespread scale. J Ultrasound 2016; 19: 281-287
    CrossrefPubMedGoogle Scholar
  • 45 Rübenthaler J, Zimmermann H, Armbruster M. et al. Contrast-Enhanced Ultrasound in the Follow-Up of Endoleaks after Endovascular Aortic Repair (EVAR). Ultraschall in Med 2017; 38: 244-264
    Article in Thieme ConnectPubMedGoogle Scholar
  • 46 Cantisani V, Grazhdani H, Clevert DA. et al. EVAR: Benefits of CEUS for monitoring stent-graft status. Eur J Radiol 2015; 84: 1658-1665
    CrossrefPubMedGoogle Scholar
  • 47 Sessa B, Trinci M, Ianniello S. et al. Blunt abdominal trauma: role of contrast-enhanced ultrasound (CEUS) in the detection and staging of abdominal traumatic lesions compared to US and CE-MDCT. Radiol Med 2015; 120: 180-189
    CrossrefPubMedGoogle Scholar
  • 48 Cokkinos DD, Antypa E, Stefanidis K. et al. Contrast-enhanced ultra- sound for imaging blunt abdominal trauma – indications, description of the technique and imaging review. Ultraschall in Med 2012; 33: 60-67
    Article in Thieme ConnectPubMedGoogle Scholar