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Published in: European Radiology 4/2019

01-04-2019 | Ultrasound

A comparative study of color Doppler imaging and contrast-enhanced ultrasound for the detection of ulceration in patients with carotid atherosclerotic disease

Authors: Vasileios Rafailidis, Ioannis Chryssogonidis, Chrysostomos Xerras, Irini Nikolaou, Thomas Tegos, Konstantinos Kouskouras, Dimitrios Rafailidis, Afroditi Charitanti-Kouridou

Published in: European Radiology | Issue 4/2019

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Abstract

Objectives

To evaluate the diagnostic accuracy of color Doppler imaging (CDI) and contrast-enhanced ultrasound (CEUS) for diagnosing carotid ulceration, having multi-detector computed tomography angiography (MDCTA) as the reference method.

Methods

Patients with carotid disease referred for ultrasound (US), either due to the occurrence of neurovascular symptoms or for screening purposes, were included in this study if at least one plaque causing moderate (50–69%) or severe (70–99%) internal carotid artery stenosis was detected. Carotid US with CDI technique, CEUS, and MDCTA were performed in all patients, investigating the presence of ulceration. The agreement between modalities was evaluated using kappa statistics.

Results

The study population included 54 patients (median age 62 years, inter-quartile range 16.2) and 66 carotid arteries. The mean degree of stenosis was 68.5% (SD 12.2%) while 47.1% of plaques were symptomatic. MDCTA characterized 28.8% of plaques as smooth, 45.5% irregular, and 24.3% ulcerated. Flow reversal was detected with CDI in 65.5% of ulcerations, while swirling of the microbubbles and neovessels adjacent to the ulcer were detected with CEUS in 17.64%. The agreement for ulceration diagnosis was moderate between CDI and CEUS (kappa 0.473) and between CDI and MDCTA (kappa 0.473) and very good between CEUS and MDCTA (kappa 0.921). The sensitivity, specificity, and positive and negative predictive values of CDI for the diagnosis of ulceration were 41.2%, 97.95%, 87.5%, 82.8% respectively, while CEUS respective measures were 94.1%, 97.95%, 94.1%, and 97.95%.

Conclusion

CEUS outperformed CDI in terms of agreement with MDCTA and diagnostic accuracy for the diagnosis of ulcerated carotid plaque.

Key Points

• Superficial ulceration is a significant feature of carotid plaque vulnerability.
• Color Doppler imaging has the potential to demonstrate carotid plaque ulceration but is characterized by limited sensitivity and moderate agreement with the reference method of multi-detector computed tomography angiography.
• Contrast-enhanced ultrasound outperforms color Doppler imaging in terms of sensitivity for the detection of carotid plaque ulceration and in agreement with the reference method of multi-detector computed tomography angiography.
Literature
1.
go back to reference 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 25:304–308CrossRefPubMed 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 25:304–308CrossRefPubMed
2.
go back to reference Handa N, Matsumoto M, Maeda H, Hougaku H, Kamada T (1995) Ischemic stroke events and carotid atherosclerosis. Results of the Osaka Follow-up Study for Ultrasonographic Assessment of Carotid Atherosclerosis (the OSACA Study). Stroke 26:1781–1786CrossRefPubMed Handa N, Matsumoto M, Maeda H, Hougaku H, Kamada T (1995) Ischemic stroke events and carotid atherosclerosis. Results of the Osaka Follow-up Study for Ultrasonographic Assessment of Carotid Atherosclerosis (the OSACA Study). Stroke 26:1781–1786CrossRefPubMed
3.
go back to reference Rafailidis V, Chryssogonidis I, Tegos T, Kouskouras K, Charitanti-Kouridou A (2017) Imaging of the ulcerated carotid atherosclerotic plaque: a review of the literature. Insights Imaging 8:213–225CrossRefPubMedPubMedCentral Rafailidis V, Chryssogonidis I, Tegos T, Kouskouras K, Charitanti-Kouridou A (2017) Imaging of the ulcerated carotid atherosclerotic plaque: a review of the literature. Insights Imaging 8:213–225CrossRefPubMedPubMedCentral
4.
go back to reference Orlandi G, Parenti G, Landucci Pellegrini L et al (1999) Plaque surface and microembolic signals in moderate carotid stenosis. Ital J Neurol Sci 20:179–182CrossRefPubMed Orlandi G, Parenti G, Landucci Pellegrini L et al (1999) Plaque surface and microembolic signals in moderate carotid stenosis. Ital J Neurol Sci 20:179–182CrossRefPubMed
5.
go back to reference Jovanović ZB, Pavlović MA, Vujisić Tešić PB et al (2013) The significance of the ultrasound diagnostics in evaluation of the emboligenic pathogenesis of transient ischemic attacks. Ultrasound Med Biol 39:597–603CrossRefPubMed Jovanović ZB, Pavlović MA, Vujisić Tešić PB et al (2013) The significance of the ultrasound diagnostics in evaluation of the emboligenic pathogenesis of transient ischemic attacks. Ultrasound Med Biol 39:597–603CrossRefPubMed
6.
go back to reference Gao P, Chen ZQ, Jiao LQ, Ling F (2007) The correlation of carotid plaque pathohistologic features and neurological symptoms: a meta-analysis of observational studies. Neurol India 55:122–129CrossRefPubMed Gao P, Chen ZQ, Jiao LQ, Ling F (2007) The correlation of carotid plaque pathohistologic features and neurological symptoms: a meta-analysis of observational studies. Neurol India 55:122–129CrossRefPubMed
7.
go back to reference Saba L, Yuan C, Hatsukami TS et al (2018) Carotid artery wall imaging: perspective and guidelines from the ASNR Vessel Wall Imaging Study Group and Expert Consensus Recommendations of the American Society of Neuroradiology. AJNR Am J Neuroradiol 39:E9–e31CrossRefPubMed Saba L, Yuan C, Hatsukami TS et al (2018) Carotid artery wall imaging: perspective and guidelines from the ASNR Vessel Wall Imaging Study Group and Expert Consensus Recommendations of the American Society of Neuroradiology. AJNR Am J Neuroradiol 39:E9–e31CrossRefPubMed
8.
go back to reference Fürst H, Hartl WH, Jansen I, Liepsch D, Lauterjung L, Schildberg FW (1992) Color-flow Doppler sonography in the identification of ulcerative plaques in patients with high-grade carotid artery stenosis. AJNR Am J Neuroradiol 13:1581–1587PubMed Fürst H, Hartl WH, Jansen I, Liepsch D, Lauterjung L, Schildberg FW (1992) Color-flow Doppler sonography in the identification of ulcerative plaques in patients with high-grade carotid artery stenosis. AJNR Am J Neuroradiol 13:1581–1587PubMed
9.
go back to reference Comerota AJ, Katz ML, White JV, Grosh JD (1990) The preoperative diagnosis of the ulcerated carotid atheroma. J Vasc Surg 11:505–510CrossRefPubMed Comerota AJ, Katz ML, White JV, Grosh JD (1990) The preoperative diagnosis of the ulcerated carotid atheroma. J Vasc Surg 11:505–510CrossRefPubMed
10.
go back to reference Anzidei M, Napoli A, Zaccagna F et al (2012) Diagnostic accuracy of colour Doppler ultrasonography, CT angiography and blood-pool-enhanced MR angiography in assessing carotid stenosis: a comparative study with DSA in 170 patients. Radiol Med 117:54–71CrossRefPubMed Anzidei M, Napoli A, Zaccagna F et al (2012) Diagnostic accuracy of colour Doppler ultrasonography, CT angiography and blood-pool-enhanced MR angiography in assessing carotid stenosis: a comparative study with DSA in 170 patients. Radiol Med 117:54–71CrossRefPubMed
11.
go back to reference Saba L, Caddeo G, Sanfilippo R, Montisci R, Mallarini G (2007) CT and ultrasound in the study of ulcerated carotid plaque compared with surgical results: potentialities and advantages of multidetector row CT angiography. AJNR Am J Neuroradiol 28:1061–1066CrossRefPubMed Saba L, Caddeo G, Sanfilippo R, Montisci R, Mallarini G (2007) CT and ultrasound in the study of ulcerated carotid plaque compared with surgical results: potentialities and advantages of multidetector row CT angiography. AJNR Am J Neuroradiol 28:1061–1066CrossRefPubMed
12.
go back to reference Rafailidis V, Charitanti A, Tegos T, Destanis E, Chryssogonidis I (2017) Contrast-enhanced ultrasound of the carotid system: a review of the current literature. J Ultrasound 20:97–109CrossRefPubMedPubMedCentral Rafailidis V, Charitanti A, Tegos T, Destanis E, Chryssogonidis I (2017) Contrast-enhanced ultrasound of the carotid system: a review of the current literature. J Ultrasound 20:97–109CrossRefPubMedPubMedCentral
13.
go back to reference 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 112:292–298CrossRefPubMed 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 112:292–298CrossRefPubMed
14.
go back to reference van den Oord SC, Akkus Z, Renaud G et al (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 15:1213–1218CrossRefPubMed van den Oord SC, Akkus Z, Renaud G et al (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 15:1213–1218CrossRefPubMed
15.
go back to reference Hamada O, Sakata N, Ogata T, Shimada H, Inoue T (2016) Contrast-enhanced ultrasonography for detecting histological carotid plaque rupture: quantitative analysis of ulcer. Int J Stroke 11:791–798CrossRefPubMed Hamada O, Sakata N, Ogata T, Shimada H, Inoue T (2016) Contrast-enhanced ultrasonography for detecting histological carotid plaque rupture: quantitative analysis of ulcer. Int J Stroke 11:791–798CrossRefPubMed
16.
go back to reference 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 229:340–346CrossRef 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 229:340–346CrossRef
17.
go back to reference Rafailidis V, Charitanti A, Tegos T, Rafailidis D, Chryssogonidis I (2016) Swirling of microbubbles: demonstration of a new finding of carotid plaque ulceration on contrast-enhanced ultrasound explaining the arterio-arterial embolism mechanism. Clin Hemorheol Microcirc 64:245–250CrossRefPubMed Rafailidis V, Charitanti A, Tegos T, Rafailidis D, Chryssogonidis I (2016) Swirling of microbubbles: demonstration of a new finding of carotid plaque ulceration on contrast-enhanced ultrasound explaining the arterio-arterial embolism mechanism. Clin Hemorheol Microcirc 64:245–250CrossRefPubMed
18.
go back to reference (1998) Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST). Lancet 351:1379–87 (1998) Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST). Lancet 351:1379–87
19.
go back to reference Lovett JK, Gallagher PJ, Hands LJ, Walton J, Rothwell PM (2004) Histological correlates of carotid plaque surface morphology on lumen contrast imaging. Circulation 110:2190–2197CrossRefPubMed Lovett JK, Gallagher PJ, Hands LJ, Walton J, Rothwell PM (2004) Histological correlates of carotid plaque surface morphology on lumen contrast imaging. Circulation 110:2190–2197CrossRefPubMed
20.
go back to reference Saba L, Anzidei M, Marincola BC et al (2014) Imaging of the carotid artery vulnerable plaque. Cardiovasc Intervent Radiol 37:572–585CrossRefPubMed Saba L, Anzidei M, Marincola BC et al (2014) Imaging of the carotid artery vulnerable plaque. Cardiovasc Intervent Radiol 37:572–585CrossRefPubMed
21.
go back to reference Brajović MD, Marković N, Loncar G et al (2009) The influence of various morphologic and hemodynamic carotid plaque characteristics on neurological events onset and deaths. ScientificWorldJournal 9:509–521CrossRefPubMedPubMedCentral Brajović MD, Marković N, Loncar G et al (2009) The influence of various morphologic and hemodynamic carotid plaque characteristics on neurological events onset and deaths. ScientificWorldJournal 9:509–521CrossRefPubMedPubMedCentral
22.
go back to reference Nakamura T, Tsutsumi Y, Shimizu Y, Uchiyama S (2013) Ulcerated carotid plaques with ultrasonic echolucency are causatively associated with thromboembolic cerebrovascular events. J Stroke Cerebrovasc Dis 22:93–99CrossRefPubMed Nakamura T, Tsutsumi Y, Shimizu Y, Uchiyama S (2013) Ulcerated carotid plaques with ultrasonic echolucency are causatively associated with thromboembolic cerebrovascular events. J Stroke Cerebrovasc Dis 22:93–99CrossRefPubMed
23.
go back to reference Singh TD, Kramer CL, Mandrekar J, Lanzino G, Rabinstein AA (2015) Asymptomatic carotid stenosis: risk of progression and development of symptoms. Cerebrovasc Dis 40:236–243CrossRefPubMed Singh TD, Kramer CL, Mandrekar J, Lanzino G, Rabinstein AA (2015) Asymptomatic carotid stenosis: risk of progression and development of symptoms. Cerebrovasc Dis 40:236–243CrossRefPubMed
24.
go back to reference Snow M, Ben-Sassi A, Winter RK et al (2007) Can carotid ultrasound predict plaque histopathology? J Cardiovasc Surg (Torino) 48:299–303 Snow M, Ben-Sassi A, Winter RK et al (2007) Can carotid ultrasound predict plaque histopathology? J Cardiovasc Surg (Torino) 48:299–303
25.
go back to reference Berg M, Zhang Z, Ikonen A et al (2005) Multi-detector row CT angiography in the assessment of carotid artery disease in symptomatic patients: comparison with rotational angiography and digital subtraction angiography. AJNR Am J Neuroradiol 26:1022–1034PubMed Berg M, Zhang Z, Ikonen A et al (2005) Multi-detector row CT angiography in the assessment of carotid artery disease in symptomatic patients: comparison with rotational angiography and digital subtraction angiography. AJNR Am J Neuroradiol 26:1022–1034PubMed
26.
go back to reference Randoux B, Marro B, Koskas F et al (2001) Carotid artery stenosis: prospective comparison of CT, three-dimensional gadolinium-enhanced MR, and conventional angiography. Radiology 220:179–185CrossRefPubMed Randoux B, Marro B, Koskas F et al (2001) Carotid artery stenosis: prospective comparison of CT, three-dimensional gadolinium-enhanced MR, and conventional angiography. Radiology 220:179–185CrossRefPubMed
27.
go back to reference Piscaglia F, Nolsøe 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 33:33–59CrossRef Piscaglia F, Nolsøe 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 33:33–59CrossRef
28.
go back to reference Sidhu PS, Cantisani V, Dietrich CF et al (2018) The EFSUMB guidelines and recommendations for the clinical practice of contrast-enhanced ultrasound (CEUS) in non-hepatic applications: update 2017 (long version). Ultraschall Med 39:e2–e44CrossRef Sidhu PS, Cantisani V, Dietrich CF et al (2018) The EFSUMB guidelines and recommendations for the clinical practice of contrast-enhanced ultrasound (CEUS) in non-hepatic applications: update 2017 (long version). Ultraschall Med 39:e2–e44CrossRef
29.
go back to reference Sirlin CB, Lee YZ, Girard MS et al (2001) Contrast-enhanced B-mode US angiography in the assessment of experimental in vivo and in vitro atherosclerotic disease. Acad Radiol 8:162–172CrossRefPubMed Sirlin CB, Lee YZ, Girard MS et al (2001) Contrast-enhanced B-mode US angiography in the assessment of experimental in vivo and in vitro atherosclerotic disease. Acad Radiol 8:162–172CrossRefPubMed
30.
go back to reference Kono Y, Pinnell SP, Sirlin CB et al (2004) Carotid arteries: contrast-enhanced US angiography--preliminary clinical experience. Radiology 230:561–568CrossRefPubMed Kono Y, Pinnell SP, Sirlin CB et al (2004) Carotid arteries: contrast-enhanced US angiography--preliminary clinical experience. Radiology 230:561–568CrossRefPubMed
31.
go back to reference de Bray JM, Baud JM, Dauzat M (1997) Consensus concerning the morphology and the risk of carotid plaques. Cerebrovasc Dis 7:289–296 de Bray JM, Baud JM, Dauzat M (1997) Consensus concerning the morphology and the risk of carotid plaques. Cerebrovasc Dis 7:289–296
32.
33.
go back to reference 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 38:2841–2843CrossRefPubMed 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 38:2841–2843CrossRefPubMed
34.
go back to reference Yusuf GT, Sellars ME, Deganello A, Cosgrove DO, Sidhu PS (2017) Retrospective analysis of the safety and cost implications of pediatric contrast-enhanced ultrasound at a single center. AJR Am J Roentgenol 208:446–452CrossRef Yusuf GT, Sellars ME, Deganello A, Cosgrove DO, Sidhu PS (2017) Retrospective analysis of the safety and cost implications of pediatric contrast-enhanced ultrasound at a single center. AJR Am J Roentgenol 208:446–452CrossRef
35.
go back to reference Lorusso A, Quaia E, Poillucci G, Stacul F, Grisi G, Cova MA (2015) Activity-based cost analysis of contrast-enhanced ultrasonography (CEUS) related to the diagnostic impact in focal liver lesion characterisation. Insights Imaging 6:499–508CrossRefPubMedPubMedCentral Lorusso A, Quaia E, Poillucci G, Stacul F, Grisi G, Cova MA (2015) Activity-based cost analysis of contrast-enhanced ultrasonography (CEUS) related to the diagnostic impact in focal liver lesion characterisation. Insights Imaging 6:499–508CrossRefPubMedPubMedCentral
36.
go back to reference Tahmasebpour HR, Buckley AR, Cooperberg PL, Fix CH (2005) Sonographic examination of the carotid arteries. Radiographics 25:1561–1575CrossRefPubMed Tahmasebpour HR, Buckley AR, Cooperberg PL, Fix CH (2005) Sonographic examination of the carotid arteries. Radiographics 25:1561–1575CrossRefPubMed
37.
go back to reference Arning C, Eckert B (2004) The diagnostic relevance of colour Doppler artefacts in carotid artery examinations. Eur J Radiol 51:246–251CrossRefPubMed Arning C, Eckert B (2004) The diagnostic relevance of colour Doppler artefacts in carotid artery examinations. Eur J Radiol 51:246–251CrossRefPubMed
Metadata
Title
A comparative study of color Doppler imaging and contrast-enhanced ultrasound for the detection of ulceration in patients with carotid atherosclerotic disease
Authors
Vasileios Rafailidis
Ioannis Chryssogonidis
Chrysostomos Xerras
Irini Nikolaou
Thomas Tegos
Konstantinos Kouskouras
Dimitrios Rafailidis
Afroditi Charitanti-Kouridou
Publication date
01-04-2019
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 4/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5773-8

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