Document Type : Review Article

Authors

1 Department of Cardiology and Vascular Medicine, Pertamina Central Hospital, South Jakarta, Indonesia

2 Faculty of Medicine, Universitas Muhammadiyah Prof Dr Hamka, Tangerang, Indonesia

3 General Practitioner, Pertamina Central Hospital, South Jakarta, Indonesia

Abstract

Carotid atherosclerosis disease assessment can predict the patient’s risk of cardiovascular disease (CVD). The purpose of this review is to provide a comprehensive review of carotid atherosclerosis disease’s pathophysiology, diagnostic evaluation, imaging applications, and treatment strategies. Carotid atherosclerosis is diagnosed using a variety of techniques, including transcranial Doppler imaging (TCD), computed tomography angiography (CTA), magnetic resonance angiography (MRA), and cerebral digital subtraction angiography (DSA), with duplex ultrasound (DUS) as the primary screening. Measurements of carotid intima-media thickness (CIMT) have drawn attention recently as a marker of early-stage carotid atherosclerosis or CVD risk prediction. The classification of cardiovascular risk may be enhanced by the expanding fields of stress testing and carotid plaque screening.

Keywords

1. Tardif JC, Heinonen T, Orloff D, Libby P. Vascular biomarkers and surrogates in cardiovascular disease. Circulation. 2006 Jun 27;113(25):2936-42. https://doi.org/10.1161/circulationaha.105.598987
2. Hoffmann U, Ferencik M, Udelson JE, Picard MH, Truong QA, Patel MR, et al. Prognostic Value of Noninvasive Cardiovascular Testing in Patients With Stable Chest Pain: Insights From the PROMISE Trial (Prospective Multicenter Imaging Study for Evaluation of Chest Pain). Circulation. 2017 Jun 13;135(24):2320-32. https://doi.org/10.1161/circulationaha.116.024360
3. Enomoto Y, Yoshimura S, Yamada K, Kawasaki M, Nishigaki K, Minatoguchi S, et al. Silent coronary artery disease in Japanese patients undergoing carotid artery stenting. J Stroke Cerebrovasc Dis. 2013 Oct;22(7):1163-8. https://doi.org/10.1016/j.jstrokecerebrovasdis.2012.12.013
4. Naqvi TZ, Lee MS. Carotid intima-media thickness and plaque in cardiovascular risk assessment. JACC Cardiovasc Imaging. 2014 Oct;7(10):1025-38. https://doi.org/10.1016/j.jcmg.2013.11.014
5. Hingwala D, Kesavadas C, Sylaja PN, Thomas B, Kapilamoorthy TR. Multimodality imaging of carotid atherosclerotic plaque: Going beyond stenosis. Indian J Radiol Imaging. 2013 Jan;23(1):26-34. https://doi.org/10.4103/0971-3026.113616
6. Nicolaides A, Beach KW, Kyriacou E, Pattichis CS. Ultrasound and carotid bifurcation atherosclerosis. Ultrasound and Carotid Bifurcation Atherosclerosis. 2013 Oct 1;9781848826885:1–649.
7. Saxena A, Ng EYK, Lim ST. Imaging modalities to diagnose carotid artery stenosis: progress and prospect. Biomed Eng Online. 2019 May 28;18(1):66. https://doi.org/10.1186/s12938-019-0685-7
8. Bytyçi I, Shenouda R, Wester P, Henein MY. Carotid Atherosclerosis in Predicting Coronary Artery Disease: A Systematic Review and Meta-Analysis. Arterioscler Thromb Vasc Biol. 2021 Apr;41(4):e224-e237. https://doi.org/10.1161/atvbaha.120.315747
9. Saam T, Cai J, Ma L, Cai YQ, Ferguson MS, Polissar NL, et al. Comparison of symptomatic and asymptomatic atherosclerotic carotid plaque features with in vivo MR imaging. Radiology. 2006 Aug;240(2):464-72. https://doi.org/10.1148/radiol.2402050390
10. Kolodgie FD, Yahagi K, Mori H, Romero ME, Trout HH Rd, Finn AV, et al. High-risk carotid plaque: lessons learned from histopathology. Semin Vasc Surg. 2017 Mar;30(1):31-43. https://doi.org/10.1053/j.semvascsurg.2017.04.008
11. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W, et al.  A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation. 1995 Sep 1;92(5):1355-74. https://doi.org/10.1161/01.cir.92.5.1355
12. Madani A, Beletsky V, Tamayo A, Munoz C, Spence JD. High-risk asymptomatic carotid stenosis: ulceration on 3D ultrasound vs TCD microemboli. Neurology. 2011 Aug 23;77(8):744-50. https://doi.org/10.1212/wnl.0b013e31822b0090
13. van Dam-Nolen DHK, van Egmond NCM, Dilba K, Nies K, van der Kolk AG, Liem MI, et al. Sex Differences in Plaque Composition and Morphology Among Symptomatic Patients With Mild-to-Moderate Carotid Artery Stenosis. Stroke. 2022 Feb;53(2):370-8. https://doi.org/10.1161/strokeaha.121.036564
14. Shaalan WE, Cheng H, Gewertz B, McKinsey JF, Schwartz LB, Katz D, et al. Degree of carotid plaque calcification in relation to symptomatic outcome and plaque inflammation. J Vasc Surg. 2004 Aug;40(2):262-9. https://doi.org/10.1016/j.jvs.2004.04.025
15. T Touzé E, Varenne O, Calvet D, Mas JL. Coronary risk stratification in patients with ischemic stroke or transient ischemic stroke attack. Int J Stroke. 2007 Aug;2(3):177-83. https://doi.org/10.1111/j.1747-4949.2007.00136.x
16. Sulženko J, Pieniazek P. The cardiovascular risk of patients with carotid artery stenosis. Vol. 60, Cor et Vasa. Elsevier Science B.V.; 2018. p. e42–8.
17. Krist AH, Davidson KW, Mangione CM, Barry MJ, Cabana M, Caughey AB, et al. Screening for Asymptomatic Carotid Artery Stenosis: US Preventive Services Task Force Recommendation Statement. JAMA. 2021 Feb 2;325(5):476-81. https://doi.org/10.1001/jama.2020.26988
18. Martin K. Introduction to B-mode imaging In: Hoskins P, Martin K. Cambridge University Press. Diagnostic Ultrasound-Physics and Equipment. 2nd ed Cambridge, UK: Cambridge; 2010. p. 1-10.
19. Netuka D, Belšán T, Broulíková K, Mandys V, Charvát F, Malík J, et al. Detection of carotid artery stenosis using histological specimens: a comparison of CT angiography, magnetic resonance angiography, digital subtraction angiography and Doppler ultrasonography. Acta Neurochir (Wien). 2016 Aug;158(8):1505-14. https://doi.org/10.1007/s00701-016-2842-0
20. Hartley CJ, Cole JS. An ultrasonic pulsed Doppler system for measuring blood flow in small vessels. J Appl Physiol. 1974 Oct;37(4):626-9. https://doi.org/10.1152/jappl.1974.37.4.626
21. Grant EG, Benson CB, Moneta GL, Alexandrov AV, Baker JD, Bluth EI, et al. Carotid artery stenosis: gray-scale and Doppler US diagnosis--Society of Radiologists in Ultrasound Consensus Conference. Radiology. 2003 Nov;229(2):340-6. https://doi.org/10.1148/radiol.2292030516
22. Kingstone LL, Currie GM, Torres C. The Pathogenesis, Analysis, and Imaging Methods of Atherosclerotic Disease of the Carotid Artery: Review of the Literature. J Med Imaging Radiat Sci. 2012 Jun;43(2):84-94. https://doi.org/10.1016/j.jmir.2011.09.003
23. Johri AM, Nambi V, Naqvi TZ, Feinstein SB, Kim ESH, Park MM, et al. Recommendations for the Assessment of Carotid Arterial Plaque by Ultrasound for the Characterization of Atherosclerosis and Evaluation of Cardiovascular Risk: From the American Society of Echocardiography. J Am Soc Echocardiogr. 2020 Aug;33(8):917-33. https://doi.org/10.1016/j.echo.2020.04.021
24. Johri AM, Behl P, Hétu MF, Haqqi M, Ewart P, Day AG, et al. Carotid Ultrasound Maximum Plaque Height-A Sensitive Imaging Biomarker for the Assessment of Significant Coronary Artery Disease. Echocardiography. 2016 Feb;33(2):281-9. https://doi.org/10.1111/echo.13007
25. Adams A, Bojara W, Schunk K. Adams A, Bojara W, Schunk K. Early Diagnosis and Treatment of Coronary Heart Disease in Asymptomatic Subjects With Advanced Vascular Atherosclerosis of the Carotid Artery (Type III and IV b Findings Using Ultrasound) and Risk Factors. Cardiol Res. 2018 Feb;9(1):22-27. https://doi.org/10.14740/cr667w
26. Sillesen H, Sartori S, Sandholt B, Baber U, Mehran R, Fuster V. Carotid plaque thickness and carotid plaque burden predict future cardiovascular events in asymptomatic adult Americans. Eur Heart J Cardiovasc Imaging. 2018 Sep 1;19(9):1042-50. https://doi.org/10.1093/ehjci/jex239
27. Johri AM, Chitty DW, Matangi M, Malik P, Mousavi P, Day A, et al. Can carotid bulb plaque assessment rule out significant coronary artery disease? A comparison of plaque quantification by two- and three-dimensional ultrasound. J Am Soc Echocardiogr. 2013 Jan;26(1):86-95. https://doi.org/10.1016/j.echo.2012.09.005
28. Adla T, Adlova R. Multimodality Imaging of Carotid Stenosis. Int J Angiol. 2015 Sep;24(3):179-84. https://doi.org/10.1055/s-0035-1556056
29. Dos Santos FL, Joutsen A, Paci M, Salenius J, Eskola H. Automatic detection of carotid arteries in computed tomography angiography: a proof of concept protocol. Int J Cardiovasc Imaging. 2016 Aug;32(8):1299-310. https://doi.org/10.1007/s10554-016-0880-6
30. Silvennoinen HM, Ikonen S, Soinne L, Railo M, Valanne L. CT angiographic analysis of carotid artery stenosis: comparison of manual assessment, semiautomatic vessel analysis, and digital subtraction angiography. AJNR Am J Neuroradiol. 2007 Jan;28(1):97-103.
31. Bash S, Villablanca JP, Jahan R, Duckwiler G, Tillis M, Kidwell C, Saver J, Sayre J. Intracranial vascular stenosis and occlusive disease: evaluation with CT angiography, MR angiography, and digital subtraction angiography. AJNR Am J Neuroradiol. 2005 May;26(5):1012-21.
32. Bivard A, Spratt N, Levi C, Parsons M. Perfusion computer tomography: imaging and clinical validation in acute ischaemic stroke. Brain. 2011 Nov;134(Pt 11):3408-16. https://doi.org/10.1093/brain/awr257
33. Wardlaw JM, Chappell FM, Stevenson M, de Nigris E, Thomas S, Gillard J, et al. Accurate, practical and cost-effective assessment of carotid stenosis in the UK. Health Technol Assess. 2006 Aug;10(30):iii-iv, ix-x, 1-182. https://doi.org/10.3310/hta10300
34. Bir SC, Kelley RE. Carotid atherosclerotic disease: A systematic review of pathogenesis and management. Brain Circ. 2022 Sep 21;8(3):127-36. https://doi.org/10.4103/bc.bc_36_22
35. Davies KN, Humphrey PR. Complications of cerebral angiography in patients with symptomatic carotid territory ischaemia screened by carotid ultrasound. J Neurol Neurosurg Psychiatry. 1993 Sep;56(9):967-72. https://doi.org/10.1136/jnnp.56.9.967
36. Ahmadvazir S, Zacharias K, Shah BN, Pabla JS, Senior R. Role of simultaneous carotid ultrasound in patients undergoing stress echocardiography for assessment of chest pain with no previous history of coronary artery disease. Am Heart J. 2014 Aug;168(2):229-36. https://doi.org/10.1016/j.ahj.2014.04.016
37. Ahmadvazir S, Shah BN, Zacharias K, Senior R. Incremental Prognostic Value of Stress Echocardiography With Carotid Ultrasound for Suspected CAD. JACC Cardiovasc Imaging. 2018 Feb;11(2 Pt 1):173-80. https://doi.org/10.1016/j.jcmg.2016.12.020
38. 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 Aug 1;37(29):2315-81. https://doi.org/10.1093/eurheartj/ehw106
39. Baigent C, Keech A, Kearney PM, Blackwell L, Buck G, Pollicino C, et al. Efficacy and safety of cholesterol-lowering treatment: prospective meta-analysis of data from 90,056 participants in 14 randomised trials of statins. Lancet. 2005 Oct 8;366(9493):1267-78. https://doi.org/10.1016/s0140-6736(05)67394-1
40. ESC Guidelines for the management of acute coronary syndromes in patients presenting without persistent ST-segment elevation: The Task Force for the management of acute coronary syndromes (ACS) in patients presenting without persistent ST-segment elevation of the European Society of Cardiology (ESC). Eur Heart J. 2011 Dec;32(23):2999-3054. https://doi.org/10.1093/eurheartj/ehr236
41. Adams RJ, Chimowitz MI, Alpert JS, Awad IA, Cerqueria MD, Fayad P, et al. Coronary risk evaluation in patients with transient ischemic attack and ischemic stroke: a scientific statement for healthcare professionals from the Stroke Council and the Council on Clinical Cardiology of the American Heart Association/American Stroke Association. Circulation. 2003 Sep 9;108(10):1278-90. https://doi.org/10.1161/01.cir.0000090444.87006.cf
42. Narins CR, Illig KA. Patient selection for carotid stenting versus endarterectomy: a systematic review. J Vasc Surg. 2006 Sep;44(3):661-72. https://doi.org/10.1016/j.jvs.2006.05.042
43. Tomai F, Pesarini G, Castriota F, Reimers B, de Luca L, de Persio G, et al. Early and long-term outcomes after combined percutaneous revascularization in patients with carotid and coronary artery stenoses. JACC Cardiovasc Interv. 2011 May;4(5):560-8. https://doi.org/10.1016/j.jcin.2011.01.012
44. Thom T, Haase N, Rosamond W, Howard VJ, Rumsfeld J, Manolio T, et al. Heart disease and stroke statistics--2006 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2006 Feb 14;113(6):e85-151. https://doi.org/10.1161/circulat ionaha.105.171600