The management of atherosclerotic carotid occlusive disease for stroke prevention has entered a time of dramatic change. Improvements in medical management have begun to challenge traditional interventional approaches to asymptomatic carotid stenosis. Simultaneously, carotid artery stenting (CAS) has emerged as an alternative to carotid endarterectomy (CE). Finally, multiple factors beyond degree of stenosis and symptom status now mitigate clinical decision making. These factors include brain perfusion, plaque morphology, and patency of intracranial collaterals (circle of Willis). With all of these changes, it seems prudent to review the role of carotid duplex ultrasonography in the management of atherosclerotic carotid occlusive disease for stroke prevention. Carotid duplex ultrasonography (CDU) for initial and serial imaging of the carotid bifurcation remains an essential component in the management of carotid bifurcation disease. However, correlative axial imaging modalities (computer tomographic angiography (CTA) and contrast-enhanced magnetic resonance angiography (CE-MRA)) increasingly aid in the assessment of individual stroke risk and are important in treatment decisions. The purpose of this paper is twofold: (1) to discuss foundations and advances in CDU and (2) to evaluate the current role of CDU, in light of other imaging modalities, in the clinical management of carotid atherosclerosis. 1. Introduction Carotid atherosclerosis is one of several etiological factors for stroke, an important health problem with a high burden of disease in the western world and in developing countries. Of all strokes, an estimated 88% are ischemic in nature [1–5]. Less than 20% of these are caused by atheroma in the carotid bifurcation [6–8]. While the percentage of strokes attributed to carotid disease is relatively low, the overall social and economic burden is high. It is, therefore, important to identify and manage carotid atherosclerosis with the aim of stroke prevention. The mortality rate for stroke in the United States has declined by nearly 70% since 1950 [9]. In December 2010, the Center for Disease Control and Prevention announced stroke was the fourth leading cause of death in the United States (down from its third place ranking which it held for decades) [10]. The identification of major risk factors through population-based studies [1, 11, 12] and randomized controlled trials (RCTs) of symptomatic [13–15] and asymptomatic [16, 17] patients has led to effective public health and clinic-based control strategies. These strategies include combining
References
[1]
W. T. Longstreth Jr., L. Shemanski, D. Lefkowitz, D. H. O'Leary, J. F. Polak, and S. K. Wolfson Jr., “Asymptomatic internal carotid artery stenosis defined by ultrasound and the risk of subsequent stroke in the elderly. The cardiovascular health study,” Stroke, vol. 29, no. 11, pp. 2371–2376, 1998.
[2]
J. Bogousslavsky, G. van Melle, and F. Regli, “The Lausanne Stroke Registry: analysis of 1,000 consecutive patients with first stroke,” Stroke, vol. 19, no. 9, pp. 1083–1092, 1988.
[3]
G. W. Petty, R. D. Brown Jr., J. P. Whisnant, J. D. Sicks, W. M. O'Fallon, and D. O. Wiebers, “Ischemic stroke subtypes: a population-based study of incidence and risk factors,” Stroke, vol. 30, no. 12, pp. 2513–2516, 1999.
[4]
W. D. Rosamond, A. R. Folsom, L. E. Chambless et al., “Stroke incidence and survival among middle-aged adults: 9-Year follow- up of the Atherosclerosis Risk in Communities (ARIC) cohort,” Stroke, vol. 30, no. 4, pp. 736–743, 1999.
[5]
A. T. Schneider, B. Kissela, D. Woo et al., “Ischemic stroke subtypes: a population-based study of incidence rates among blacks and whites,” Stroke, vol. 35, no. 7, pp. 1552–1556, 2004.
[6]
R. L. Sacco, D. E. Kargman, Q. Gu, and M. C. Zamanillo, “Race-ethnicity and determinants of intracranial atherosclerotic cerebral infarction. The Northern Manhattan stroke study,” Stroke, vol. 26, no. 1, pp. 14–20, 1995.
[7]
R. J. Wityk, D. Lehman, M. Klag, J. Coresh, H. Ahn, and B. Litt, “Race and sex differences in the distribution of cerebral atherosclerosis,” Stroke, vol. 27, no. 11, pp. 1974–1980, 1996.
[8]
T. G. Brott, J. L. Halperin, S. Abbara, et al., “2011 ASA/ACCF/AHA/AANN/AANS/ACR/ASNR/CNS/SAIP/ SCAI/SIR/SNIS/SVM/SVS guideline on the management of patients with extracranial carotid and vertebral artery disease: executive summary: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines, and the American Stroke Association, American Association of Neuroscience Nurses, American,” Vascular Medicine, vol. 16, no. 1, pp. 35–77, 2011.
[9]
M. Heron, D. L. Hoyert, S. L. Murphy, J. Xu, K. D. Kochanek, and B. Tejada-Vera, “Deaths: final data for 2006,” National Vital Statistics System Reports, vol. 57, no. 14, pp. 1–134, 2009.
[10]
A. M. Minino, J. Xu, and K. D. Kochanek, Deaths: preliminary Data for 2008, U.S. Department of Health and Human Services, New York, NY, USA, 2010.
[11]
J. S. Fine-Edelstein, P. A. Wolf, D. H. O'Leary et al., “Precursors of extracranial carotid atherosclerosis in the Framingham Study,” Neurology, vol. 44, no. 6, pp. 1046–1050, 1994.
[12]
I. Meissner, J. P. Whisnant, B. K. Khandheria et al., “Prevalence of potential risk factors for stroke assessed by transesophageal echocardiography and carotid ultrasonography: the SPARC study. Stroke Prevention: assessment of Risk in a Community,” Mayo Clinic Proceedings, vol. 74, no. 9, pp. 862–869, 1999.
[13]
“Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. North American Symptomatic Carotid Endarterectomy Trial Collaborators,” New England Journal of Medicine, vol. 325, no. 7, pp. 445–453, 1991.
[14]
C. Warlow, B. Farrell, A. Fraser, P. Sandercock, and J. Slattery, “Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of the MRC European Carotid Surgery Trial (ECST),” Lancet, vol. 351, no. 9113, pp. 1379–1387, 1998.
[15]
A. R. Naylor, P. M. Rothwell, and P. R. Bell, “Overview of the principal results and secondary analyses from the European and North American randomised trials endarterectomy for symptomatic carotid stenosis,” European Journal of Vascular and Endovascular Surgery, vol. 26, no. 2, pp. 115–129, 2003.
[16]
“Endarterectomy for asymptomatic carotid artery stenosis,” Journal of the American Medical Association, vol. 273, no. 18, pp. 1421–1428, 1995.
[17]
P. M. Rothwell and L. B. Goldstein, “Carotid endarterectomy for asymptomatic carotid stenosis: asymptomatic carotid surgery trial,” Stroke, vol. 35, no. 10, pp. 2425–2427, 2004.
[18]
A. AbuRahma and K. Jarrett, “Duplex scanning of the carotid arteries,” in Noninvasive Vascular Diagnosis, A. AbuRahma and J. Bergan, Eds., pp. 60–88, Springer, London, UK, 2nd edition, 2007.
[19]
R. Zierler and D. Strandness, “Noninvasive dynamic and real-time assessment of extracranial cerebrovasculature,” in Cerebral Blood Flow: Physiologic and Clinical Aspects, J. Wood, Ed., pp. 311–323, McGraw-Hill, New York, NY, USA, 1987.
[20]
E. G. Grant, C. B. Benson, G. L. Moneta et al., “Carotid artery stenosis: gray-scale and Doppler US diagnosis—society of Radiologists in Ultrasound Consensus Conference,” Radiology, vol. 229, no. 2, pp. 340–346, 2003.
[21]
M. J. Gough, “Preprocedural imaging strategies in symptomatic carotid artery stenosis,” Journal of Vascular Surgery, vol. 54, no. 4, pp. 1215–1218, 2011.
[22]
M. Anzidei, A. Napoli, F. Zaccagna, et al., “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,” Radiologia Medica, vol. 117, no. 1, pp. 54–71, 2011.
[23]
M. Anzidei, B. Cavallo Marincola, A. Napoli et al., “Low-dose contrast-enhanced time-resolved MR angiography at 3 T: diagnostic accuracy for treatment planning and follow-up of vascular malformations,” Clinical Radiology, vol. 66, no. 12, pp. 1181–1192, 2011.
[24]
A. F. AbuRahma, M. Srivastava, P. A. Stone et al., “Critical appraisal of the Carotid Duplex Consensus criteria in the diagnosis of carotid artery stenosis,” Journal of Vascular Surgery, vol. 53, no. 1, pp. 53–59, 2011.
[25]
S. B. Feinstein, “Contrast ultrasound imaging of the carotid artery vasa vasorum and atherosclerotic plaque neovascularization,” Journal of the American College of Cardiology, vol. 48, no. 2, pp. 236–243, 2006.
[26]
G. M. Biasi, A. Froio, E. B. Diethrich 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, vol. 110, no. 6, pp. 756–762, 2004.
[27]
C. Krogias, C. Henneb？hl, B. Geier et al., “Transcranial ultrasound perfusion imaging and perfusion-MRI-A pilot study on the evaluation of cerebral perfusion in severe carotid artery stenosis,” Ultrasound in Medicine and Biology, vol. 36, no. 12, pp. 1973–1980, 2010.
[28]
A. F. AbuRahma, S. Abu-Halimah, J. Bensenhaver et al., “Optimal carotid duplex velocity criteria for defining the severity of carotid in-stent restenosis,” Journal of Vascular Surgery, vol. 48, no. 3, pp. 589–594, 2008.
[29]
B. K. Lal, R. W. Hobson 2nd, B. Tofighi, I. Kapadia, S. Cuadra, and Z. Jamil, “Duplex ultrasound velocity criteria for the stented carotid artery,” Journal of Vascular Surgery, vol. 47, no. 1, pp. 63–73, 2008.
[30]
J. A. Rizzo, A. Dodge, P. White, and E. D. Martin, “Magnetic resonance angiography in the evaluation of carotid stent patency,” Perspectives in Vascular Surgery and Endovascular Therapy, vol. 22, no. 4, pp. 261–263, 2010.
[31]
M. J. Davies, P. D. Richardson, N. Woolf, D. R. Katz, and J. Mann, “Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content,” British Heart Journal, vol. 69, no. 5, pp. 377–381, 1993.
[32]
E. Falk, “Why do plaques rupture?” Circulation, vol. 86, supplement 6, pp. III30–III42, 1992.
[33]
A. Falkowski, M. Parafiniuk, W. Poncyljusz, M. Kaczmarczyk, and G. Wilk, “Ultrasonographic and histological analysis of atheromatous plaques in carotid arteries and apoplectic complications,” Medical Science Monitor, vol. 13, supplement 1, pp. 78–82, 2007.
[34]
Z. Y. Li, V. Taviani, and J. H. Gillard, “The impact of wall shear stress and pressure drop on the stability of the atherosclerotic plaque,” in Proceedings of the 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBS '08), pp. 1373–1376, August 2008.
[35]
Y. J. Xue, P. Y. Gao, Q. Duan, Y. Lin, and C. B. Dai, “Preliminary study of hemodynamic distribution in patient-specific stenotic carotid bifurcation by image-based computational fluid dynamics,” Acta Radiologica, vol. 49, no. 5, pp. 558–565, 2008.
[36]
B. K. Lal, K. W. Beach, and D. S. Sumner, “Intracranial collateralization determines hemodynamic forces for carotid plaque disruption,” Journal of Vascular Surgery, vol. 54, no. 5, pp. 1461–1471, 2011.
[37]
A. R. Naylor, “The importance of initiating "best medical therapy" and intervening as soon as possible in patients with symptomatic carotid artery disease: time for a radical rethink of practice,” Journal of Cardiovascular Surgery, vol. 50, no. 6, pp. 773–782, 2009.
[38]
B. K. Lal, R. W. Hobson 2nd, J. Goldstein et al., “In-stent recurrent stenosis after carotid artery stenting: life table analysis and clinical relevance,” Journal of Vascular Surgery, vol. 38, no. 6, pp. 1162–1169, 2003.
[39]
B. K. Lal, R. W. Hobson 2nd, J. Goldstein et al., “Carotid artery stenting: is there a need to revise ultrasound velocity criteria?” Journal of Vascular Surgery, vol. 39, no. 1, pp. 58–66, 2004.
[40]
S. F. Stanziale, M. H. Wholey, T. N. Boules, F. Selzer, and M. S. Makaroun, “Determining in-stent stenosis of carotid arteries by duplex ultrasound criteria,” Journal of Endovascular Therapy, vol. 12, no. 3, pp. 346–353, 2005.
[41]
P. J. Nederkoorn and M. M. Brown, “Optimal cut-off criteria for duplex ultrasound for the diagnosis of restenosis in stented carotid arteries: review and protocol for a diagnostic study,” BMC Neurology, vol. 9, article 36, 2009.
[42]
A. Willfort-Ehringer, R. Ahmadi, D. Gruber et al., “Arterial remodeling and hemodynamics in carotid stents: a prospective duplex ultrasound study over 2 years,” Journal of Vascular Surgery, vol. 39, no. 4, pp. 728–734, 2004.
[43]
S. Chahwan, M. T. Miller, J. P. Pigott, R. C. Whalen, L. Jones, and A. J. Comerota, “Carotid artery velocity characteristics after carotid artery angioplasty and stenting,” Journal of Vascular Surgery, vol. 45, no. 3, pp. 523–526, 2007.
[44]
B. K. Lal, E. A. Kaperonis, S. Cuadra, I. Kapadia, and R. W. Hobson 2nd, “Patterns of in-stent restenosis after carotid artery stenting: classification and implications for long-term outcome,” Journal of Vascular Surgery, vol. 46, no. 5, pp. 833–840, 2007.
[45]
P. Cao and P. DeRango, “Carotid artery disease: stenting,” in Rutherford's Vascular Surgery, J. Cronenwett and J. Johnston, Eds., pp. 1469–1486, WB Saunders, Philadelphia, Pa, USA, 7th edition, 2010.
[46]
H. Sadideen, P. R. Taylor, and T. S. Padayachee, “Restenosis after carotid endarterectomy,” International Journal of Clinical Practice, vol. 60, no. 12, pp. 1625–1630, 2006.
[47]
E. F. Bernstein, S. Torem, and R. B. Dilley, “Does carotid restenosis predict an increased risk of late symptoms, stroke, or death?” Annals of Surgery, vol. 212, no. 5, pp. 629–636, 1990.
[48]
M. A. Mattos, A. R. Shamma, N. Rossi et al., “Is duplex follow-up cost-effective in the first year after carotid endarterectomy?” American Journal of Surgery, vol. 156, no. 2, pp. 91–95, 1988.
[49]
R. Bond, K. Rerkasem, A. R. Naylor, A. F. Aburahma, and P. M. Rothwell, “Systematic review of randomized controlled trials of patch angioplasty versus primary closure and different types of patch materials during carotid endarterectomy,” Journal of Vascular Surgery, vol. 40, no. 6, pp. 1126–1135, 2004.
[50]
A. F. Aburahma, “Duplex criteria for determining ≥50% and ≥80% internal carotid artery stenosis following carotid endarterectomy with patch angioplasty,” Vascular, vol. 19, no. 1, pp. 15–20, 2011.
[51]
T. Wolff, J. Guirguis-Blake, T. Miller, et al., “Screening for asymptomatic carotid artery stenosis,” Agency for Healthcare Research and Quality 50, Evidence Synthesis, Rockville, Md, USA, 2007.
[52]
S. W. Cheng, L. L. Wu, A. C. Ting, H. Lau, and J. Wong, “Screening for asymptomatic carotid stenosis in patients with peripheral vascular disease: a prospective study and risk factor analysis,” Cardiovascular Surgery, vol. 7, no. 3, pp. 303–309, 1999.
[53]
V. Nambi, L. Chambless, A. R. Folsom et al., “Carotid intima-media thickness and presence or absence of plaque improves prediction of coronary heart disease risk: the ARIC (Atherosclerosis Risk In Communities) study,” Journal of the American College of Cardiology, vol. 55, no. 15, pp. 1600–1607, 2010.
[54]
B. Coll, V. Nambi, and S. B. Feinstein, “New advances in noninvasive imaging of the carotid artery: CIMT, contrast-enhanced ultrasound, and vasa vasorum,” Current Cardiology Reports, vol. 12, no. 6, pp. 497–502, 2010.
[55]
D. Staub, M. B. Patel, A. Tibrewala et al., “Vasa vasorum and plaque neovascularization on contrast-enhanced carotid ultrasound imaging correlates with cardiovascular disease and past cardiovascular events,” Stroke, vol. 41, no. 1, pp. 41–47, 2010.
[56]
G. L. Faggioli, R. Pini, R. Mauro et al., “Identification of carotid 'vulnerable plaque' by contrast-enhanced ultrasonography: correlation with plaque histology, symptoms and cerebral computed tomography,” European Journal of Vascular and Endovascular Surgery, vol. 41, no. 2, pp. 238–248, 2011.
[57]
D. A. Clevert, W. H. Sommer, P. Zengel, A. Helck, and M. Reiser, “Imaging of carotid arterial diseases with contrast-enhanced ultrasound (CEUS),” European Journal of Radiology, vol. 80, no. 1, pp. 68–76, 2011.
