Hostname: page-component-76fb5796d-wq484 Total loading time: 0 Render date: 2024-04-30T00:45:18.567Z Has data issue: false hasContentIssue false

Carotid Stenosis and Stroke: Historical Perspectives Leading to Current Challenges

Published online by Cambridge University Press:  11 March 2024

David M. Pelz*
Affiliation:
Department of Medical Imaging, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada
Allan J. Fox
Affiliation:
University of Toronto, Toronto, ON, Canada
J. David Spence
Affiliation:
Neurology and Clinical Pharmacology, Schulich School of Medicine and Dentistry, Western University, London, ON, Canada Stroke Prevention and Atherosclerosis Research Centre, Robarts Research Institute, London, ON, Canada
Stephen P. Lownie
Affiliation:
Division of Neurosurgery, Department of Surgery, Dalhousie University, Halifax, NS, Canada Schulich School of Medicine and Dentistry, Western University, Halifax, NS, Canada
*
Corresponding author: D. M. Pelz; Email: pelz@uwo.ca

Abstract:

The carotid artery is unique; it is the only vessel to bifurcate into a bulb larger than itself. The history of its anatomic description, understanding of its pathophysiology and evolution of its imaging are relevant to current controversies regarding measurement of stenosis, surgical/endovascular therapies and medical management of carotid stenosis in stroke prevention. Treatment decisions on millions of symptomatic and asymptomatic patients are routinely based on information from clinical trials from over 30 years ago. This article briefly summarizes the highlights of past research in key areas and discuss how they led to current challenges of diagnosis and treatment.

Résumé :

RÉSUMÉ :

Sténose carotidienne et accidents vasculaires cérébraux : facteurs historiques à l’origine de controverses actuelles.

L’artère carotide est unique en son genre, en ce sens qu’elle est le seul vaisseau sanguin à se diviser en un sinus [ou bulbe] plus gros qu’elle-même. Ainsi, l’historique de sa description anatomique, la compréhension que les chercheurs avaient de sa physiopathologie et l’évolution de l’imagerie médicale sont tous des éléments qui permettent de mieux saisir les controverses qui entourent les mesures du degré de sténose ainsi que le traitement chirurgical ou endovasculaire et la prise en charge médicale de la sténose carotidienne en prévention des accidents vasculaires cérébraux. Les décisions relatives au traitement de cette obstruction artérielle chez des millions de patients qui présentent ou non des symptômes reposent généralement sur des données provenant d’essais cliniques effectués il y a plus de 30 ans. Aussi présenterons-nous dans l’article un résumé des faits saillants qui ont marqué la recherche dans le passé dans des domaines clés, et discuterons-nous de la manière dont ces éléments principaux ont conduit aux problèmes actuels de pose de diagnostic et de traitement.

Type
Review Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of Canadian Neurological Sciences Federation

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Linxin, L, Yiin, GS, Geraghty, OC, et al. Incidence, outcome, risk factors, and long-term prognosis of cryptogenic transient ischaemic attack and ischaemic stroke: a population-based study. Lancet Neurol. 2015;14:903–13.Google Scholar
Warlow, C, Sudlow, C, Dennis, M, Wardlaw, J, Sandercock, P. stroke. Lancet. 2003;362:1211–24.CrossRefGoogle ScholarPubMed
van Velzen, TJ, Kuhrij, LS, Westendorp, WF, van de Beek, D, Nederkoorn, PJ. Prevalence, predictors and outcome of carotid stenosis: a sub study in the preventive antibiotics in stroke study (PASS). BMC Neurol. 2021;21:2031.Google Scholar
Song, P, Fang, Z, Cai, Y, et al. Global and regional prevalence, burden and risk factors for carotid atherosclerosis: s systematic review, meta-analysis, and modelling study. Lancet Glob Health. 2020;8:e721e729.CrossRefGoogle ScholarPubMed
Hackam, DG, Spence, JD. Decline in the severity of carotid atherosclerosis and associated stroke risk factors from 2002-2014. Stroke. 2018;49:2786–88.CrossRefGoogle Scholar
Bogiatzi, C, Hackam, DG, McLeod, AI, Spence, JD. Secular trends in ischemic stroke subtypes and stroke risk factors. Stroke. 2014;45:3208–13.CrossRefGoogle ScholarPubMed
De Weerd, M, Greving, JP, Hedblad, B, et al. Prevalence of asymptomatic carotid stenosis in the general population: an individual participant data meta-analysis. Stroke. 2010;41:1294–7.CrossRefGoogle ScholarPubMed
Abbott, A, Paraskevas, KI, Kakkos, SK, et al. Systematic review of guidelines for the management of asymptomatic and symptomatic carotid stenosis. Stroke. 2015;46:3288–301.CrossRefGoogle ScholarPubMed
Abbott, AL. Extra-cranial carotid artery stenosis: an objective analysis of the available evidence. Front. Neurol. 2022;739999:10.3389/neur.2002.739999.Google Scholar
Robicsek, F. The medical history of extracranial cerebrovascular disease. In: Robicsek, F, ed. Extracranial cerebrovascular disease, New York: MacMillan Publishing Company; 1986:518.Google Scholar
Gurdjian, E, Gurdjian, E. History of occlusive cerebrovascular disease: from Wepfer to Moniz. Arch Neurol. 1979;36:340–3.CrossRefGoogle ScholarPubMed
Barnett, HJM. Reflections on the carotid artery: 438 BC to 2009 AD. The Karolinska 2008 Award lecture in stroke research. Stroke. 2009;40:3143–8.CrossRefGoogle ScholarPubMed
Chiari, H. Ueber verhallen des teilung-swinkels der carotis communis bei der endarteritis chronica deformans. Verh Dtsch Ges Path. 1905;9:36.Google Scholar
Hunt, JR. The role of the carotid arteries in the causation of vascular lesions of the brain, with remarks on certain special features of the symptomatology. Am J Med Sci. 1914;147:704–13.CrossRefGoogle Scholar
Moniz, E. L’encephalographie arterielle, son importance dans la localisation des tumeurs cerebrales. Rev Neurol. 1927;2:7290.Google Scholar
Fisher, M. Occlusion of the internal carotid artery. Arch Neurol Psychiat. 1951;65:346–77.CrossRefGoogle ScholarPubMed
Fisher, M. Occlusion of the carotid arteries: further experiences. Arch Neurol Psychiat. 1954;72:187204.CrossRefGoogle ScholarPubMed
Fisher, C, Gore, I, Okabe, N, White, P. Atherosclerosis of the carotid and vertebral arteries-extracranial and intracranial. J Neuropath Exp Neurology. 1965;24:455–76.CrossRefGoogle Scholar
Fisher, C, Ojemann, R. A clinico-pathologic study of carotid endarterectomy plaques. Rev Neurol (Paris). 1986;142:573–89.Google Scholar
Vander Eecken, H, Adams, R. The anatomy and functional significance of the meningeal arterial anastomoses of the human brain. J Neuropath Exp Neurol. 1953;12:132–57.CrossRefGoogle ScholarPubMed
Thompson, JE. The evolution of surgery for the treatment and prevention of stroke. Stroke. 1996;27:1427–34.CrossRefGoogle ScholarPubMed
Eastcott, HG, Pickering, GW, Rob, C. Reconstruction of the internal carotid artery in a patient with intermittent attacks of hemiplegia. Lancet. 1954;267:994–6.CrossRefGoogle Scholar
Robertson, JT. Carotid endarterectomy: a saga of clinical science, personalities, and evolving technology: the willis lecture. Stroke. 1998;29:2435–41.Google Scholar
Murphey, F. The scotomata of carotid artery disease as I remember them. J Neurosurg. 1973;39:390–3.CrossRefGoogle Scholar
Moore, WS, Boren, C, Malone, JM, et al. Natural history of Nonstenotic, asymptomatic ulcerative lesions of the carotid artery. Arch Surg. 1978;113:1352–9.CrossRefGoogle ScholarPubMed
Easton, JD. History of carotid endartectomy: then and now. Stroke. 2014;45:101–3.CrossRefGoogle Scholar
Barnett, HJM, Plum, F, Walton, JN. Carotid endarterectomy – an expression of concern. Stroke. 1984;15:941–3.CrossRefGoogle ScholarPubMed
Fields, WS, Maslenikov, V, Meyer, JS, Hass, WK, Remington, RD, Macdonald, M. Joint study of extracranial arterial occlusion. V. Progress report of prognosis following surgery or nonsurgical treatment for transient cerebral ischemic attacks and cervical carotid artery lesions. JAMA. 1970;211:19932003.Google Scholar
Kurtzke, J. Formal discussion. In: Whisnant, JP, Sandok, BA, ed. Cerebral vascular disease-ninth princeton conference. New York: Grune & Stratum; 1974:190–3.Google Scholar
Shaw, DA, Venables, GS, Cartlidge, NEF, Bates, D, Dickinson, PH. Carotid endarterectomy in patients with transient cerebral ischaemia. J Neurol Sci. 1984;64:4553.Google Scholar
European Carotid Surgery Trialists' Collaborative Group. MRC European carotid surgery trial: interim results for symptomatic patients with severe (70-99%) or with mild (0-29%) carotid stenosis. Lancet. 1991;337:1235–43.CrossRefGoogle Scholar
North American Symptomatic Carotid Endarterectomy Trial Collaborators. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med. 1991;325:445–53.CrossRefGoogle Scholar
Hobson, RW, Weiss, DG, Field, WS, et al. Efficacy of carotid endarterectomy for asymptomatic carotid stenosis. N Engl J Med. 1993;328:221–7.CrossRefGoogle ScholarPubMed
Executive Committee for the Asymptomatic Carotid Atherosclerosis Study. Endarterectomy for asymptomatic carotid artery stenosis. JAMA. 1995;273:1421–8.CrossRefGoogle Scholar
MRC Asymptomatic Carotid Surgery Trial (ACST) Collaborative Group. Prevention of disabling and fatal stroke by successful carotid endarterectomy in patients without recent neurological symptoms: randomised controlled trial. Lancet. 2004;363:1491–502s.CrossRefGoogle Scholar
Hackam, DG. Optimal medical management of asymptomatic carotid stenosis. Stroke. 2021;52:2191–8.CrossRefGoogle ScholarPubMed
Kresowik, TF, Bratzler, D, Karp, HR, et al. Multistate utilization, process, and outcomes of carotid endarterectomy. J Vasc Surg. 2001;33:227–35.CrossRefGoogle ScholarPubMed
Golnari, P, Nazari, P, Hurley, MC, et al. Continued dominance of carotid endarterectomy over stenting in the United States: volumes, outcomes, and complications from the national inpatient sample (1997-2015). World Neurosurg. 2022;163:e238e252.Google Scholar
Otite, FO, Khandelwal, P, Malik, AM, Chaturvedi, S. National patterns of carotid revascularization before and after the carotid revascularization endarterectomy vs stenting trial (CREST). JAMA Neurol. 2018;75:51–7.CrossRefGoogle ScholarPubMed
Naylor, AR. Which patients with asymptomatic carotid stenosis benefit from revascularization? Curr Opin Neurol. 2017;30:1521.CrossRefGoogle ScholarPubMed
Rieff, T, Eckstein, H-H, Mansmann, U, et al. Carotid endarterectomy or stenting or best medical treatment alone for moderate -to-severe asymptomatic carotic stenosis: 5-year results of a multicentre, randomised controlled trial. Lancet Neurol. 2022;21:877–88.CrossRefGoogle Scholar
Nederkoorn, PJDonners, S, van Velzen, T, Cheng, , Gregson, J et al. Immediate revascularization versus optimised medical therapy alone in patients with carotid stenosis at low to intermediate risk of stroke: interim results of ECST-2. (Abstr. 0313/2283). Presented at the 9th European Stroke Organization Conference, Munich, Germany, May 24–26, 2023. European Stroke Journal 2023; 8(2) suppl: ESOC Abstract Book, Sage Publications.Google Scholar
Bauer, RB, Boulos, RS, Meyer, JS. Natural history and surgical treatment of occlusive cerebrovascular disease evaluated by serial arteriography. Am J Roentgenol. 1968;104:117.CrossRefGoogle ScholarPubMed
Fox, AJ. How to measure carotid stenosis. Radiology. 1993;186:316–8.Google Scholar
Fox, AJ, Eliasziw, M, Rothwell, PM, Schmidt, MH, Warlow, CP, Barnett, HJM. Identification, prognosis, and management of patients with carotid artery near occlusion. AJNR Am J Neuroradiol. 2005;26:2086–94.Google ScholarPubMed
Johansson, E, Fox, AJ. Near-occlusion is a common variant of carotid stenosis: study and systematic review. Can J Neurol Sci. 2022;49:5561.CrossRefGoogle ScholarPubMed
Rothwell, PM, Gibson, RJ, Slattery, J, Sellar, RJ, Warlow, CP. Equivalence of measurement of carotid stenosis. A comparison of three methods on 1001 Angiograms. Stroke. 1994;25:2435–9.CrossRefGoogle ScholarPubMed
Bartlett, ES, Walters, TD, Symons, SP, Fox, AJ. Quantification of carotid stenosis on CT angiography. AJNR Am J Neuroradiol. 2006;27:13–9.Google ScholarPubMed
Horev, A, Honig, C, Goldbart, JE, et al. Overestimation of carotid stenosis on CTA- real world experience. J Clin Neurosci. 2021;85:3640.CrossRefGoogle ScholarPubMed
Jareczek, FJ, Farrell, MB, Lehman, EB, et al. Variation in carotid artery stenosis measurements among facilities seeking carotid stenting facility accreditation. Stroke. 2023;54:1578–86.CrossRefGoogle ScholarPubMed
Brinjikji, W, Huston, J, Rabinstein, AA, Kim, G-M, Lerman, A, Lanzino, G. Contemporary carotid imaging: from degree of stenosis to plaque vulnerability. J Neurosurg. 2016;124:2742.CrossRefGoogle ScholarPubMed
Saba, L, Moody, AR, Saam, T, et al. Vessel wall-imaging biomarkers of carotid plaque vulnerability in stroke prevention trials. JACC, Cardiovascular Imaging. 2020;13:2445–56.Google Scholar
Saba, L, Cau, R, Murgia, A, et al. Carotid plaque-RADS. A novel stroke risk classification system. JACC Cardiovasc Imaging. 2024;17:6275. DOI: 10.1016/j.jcmg.2023.09.005.CrossRefGoogle ScholarPubMed
Mathias, K. Perkutane transluminale Katheterbehandlung supra-aortaler Aterienobstruktionen. Angiology. 1981;3:4750.Google Scholar
Yadav, JS, Roubin, GS, Iyer, S, et al. Elective stenting of the extracranial carotid arteries. Circulation. 1997;95:376–81.CrossRefGoogle ScholarPubMed
Bettmann, MA, Katzen, BT, Whisnant, J, et al. Carotid stenting and angioplasty. Circulation. 1998;97:121–3.CrossRefGoogle ScholarPubMed
CAVATAS Investigators. Endovascular versus surgical treatment in patients with carotid stenosis in the carotid and vertebral artery transluminal angioplasty study (CAVATAS): a randomised trial. Lancet. 2001;357:1729–37.CrossRefGoogle Scholar
Yadav, JS, Wholey, MH, Kuntz, RE, et al. Stenting and angioplasty with protection in patients at high risk for endarterectomy investigators. Protected carotid-artery stenting versus endarterectomy on high-risk patients. N Engl J Med. 2004;351:1493–501.Google Scholar
The SPACE Collaborative Group. 30-day results from the SPACE trial of stent-protected angioplasty versus carotid endarterectomy in symptomatic patients: a randomised non-inferiority trial. Lancet. 2006;368:1239–47.CrossRefGoogle Scholar
Mas, J-L, Chatellier, G, Beyssen, B, et al. Endarterectomy versus stenting in patients with symptomatic severe carotid stenosis. N Engl J Med. 2006;355:16601671–1671.Google Scholar
Bonati, LH, Dobson, J, Featherstone, RL, et al. International carotid stenting study investigators. Long-term outcomes after stenting versus endarterectomy for treatment of symptomatic carotid stenosis: the international carotid stenting study (ICSS) randomised trial. Lancet. 2015;385:529–38.CrossRefGoogle Scholar
Brott, TG, Hobson, RW ll, Howard, G, et al. Stenting versus endarterectomy for treatment of carotid-artery stenosis. N Engl J Med. 2010;363:1123.CrossRefGoogle ScholarPubMed
Cohen, DJ, Stolker, JM, Wang, K, et al. Health-related quality of life after carotid stenting versus carotid endarterectomy: results from CREST (Carotid revascularization endarterectomy versus stenting trial). J Am Coll Cardiol. 2011;58:1557–65.Google Scholar
Spence, JD. Management of patients with an asymptomatic carotid stenosis-medical management, endovascular treatment, or carotid endarterectomy? Curr Neurol Neurosci Rep. 2016;16:3. DOI: 10.1007/s11910-015-0605-6.CrossRefGoogle ScholarPubMed
Almekhlafi, MA, Demchuk, AM, Mishra, S, et al. Malignant emboli on transcranial Doppler during carotid stenting predict postprocedure diffusion-weighted imaging lesions. Stroke. 2013;44:1317–22.Google Scholar
Halliday, A, Bulbulia, R, Bonati, LH, et al. Second asymptomatic carotid surgery trial (ACST-2): a randomised comparison of carotid artery stenting versus carotid endarterectomy. Lancet. 2021;398:1065–73.CrossRefGoogle ScholarPubMed
Grotta, JC. Fifty years of acute ischemic stroke treatment: a personal history. Cerebrovasc Dis. 2021;50:666–80.Google Scholar
Fisher, CM, Adams, RD. Cerebrovascular diseases. Neuropathological progress. Res Cardovasc. 1964;10:425–6.Google ScholarPubMed
Millikan, C, Siekert, R, Schick, R. Studies in cerebrovascular disease. V. The use of anticoagulant drugs in the treatment of intermittent insufficiency of the internal carotid arterial system. Proc Mayo Clin. 1955;30:578–86.Google ScholarPubMed
International Stroke Trial Collaborative Group. The international stroke trial (IST): a randomised trial of aspirin, subcutaneous heparin, both, or neither among 19,435 patients with acute ischemic stroke. Lancet. 1997;349:1569–81.CrossRefGoogle Scholar
Acute Stroke Treatment (TOAST) Investigators. Low molecular weight heparinoid (danaparoid), and outcome after acute ischemic stroke. A randomized, controlled trial. JAMA. 1998;279:1265–72.CrossRefGoogle Scholar
Fields, WS, Lemak, NA, Frankowski, RF, Hardy, RJ. Controlled trial of aspirin in cerebral ischemia. Stroke. 1977;8:301–14.CrossRefGoogle ScholarPubMed
The Canadian Cooperative Study Group. A randomized trial of aspirin and sulfinpyrazone in threatened stroke. N Engl J Med.1978;299:53–9.Google Scholar
Gent, M, Blakely, JA, Easton, JD, et al. The Canadian American ticlopidine study (CATS) in thromboembolic stroke. Lancet. 1989;1:1215–20.CrossRefGoogle ScholarPubMed
Haas, WK, Easton, JD, Adams, HP, et al. A randomized trial comparing ticlopidine hydrochloride with aspirin for the prevention of stroke in high-risk patients. N Engl J Med. 1989;321:501–7.Google Scholar
Baigent, C, Blackwell, L, Emberson, J, et al. Efficacy and safety of more intensive lowering of ldl cholesterol: a meta-analysis of data from 170,000 participants in 26 randomised trials. Lancet. 2010;376:1670–81.Google ScholarPubMed
Furberg, CD, Adams, HP, Applegate, WB, et al. Effect of lovastatin on early carotid atherosclerosis and cardiovascular events. Circulation. 1994;90:1679–87.Google Scholar
paper. Salonen, RKAPS, Nyyssonen, K, Parkkala-Sarataho, E, Salonen, JT. The kuopio atherosclerosis prevention study (KAPS): effect of pravastatin treatment on lipids, oxidative resistance of lipoproteins, and atherosclerosis progression. Am J Cardiol. 1995;76:34C–39?.CrossRefGoogle Scholar
The Stroke Prevention by Aggressive Reduction in Cholesterol Levels (SPARCL) Investigators. High-dose atorvastatin after stroke or transient ischemic attack. N Engl J Med. 2006;355:549–59.CrossRefGoogle Scholar
Stary, HC, Chandler, AB, Dinsmore, RE, et al. A definition of advanced types of atherosclerotic lesions and histological classification of atherosclerosis. Circulation. 1995;92:1355–74.Google Scholar
Kamtchum-Tatuene, J, Noubiap, JJ, Wilman, AH, Saqqur, M, Shuaib, A, Jickling, GC. Prevalence of high-risk plaques and risk of stroke in patients with asymptomatic carotid stenosis. JAMA Neurol. 2020;77:112.Google Scholar
Paraskevas, KI, Veith, FJ, Spence, JD. How to identify which patients with asymptomatic carotid stenosis could benefit from endarterectomy or stenting. Stroke Vasc Neurol. 2018;3:92100.Google Scholar
Spence, JD, Coates, V, Li, H, et al. Effects of intensive medical therapy on Microemboli and cardiovascular risk in asymptomatic carotid stenosis. Arch Neurol. 2010;67:180–6.CrossRefGoogle Scholar
Spence, JD, Hackam, DG. Treating arteries instead of risk factors. A paradigm change in management of atherosclerosis. Stroke. 2010;41:1193–9.Google Scholar
Naylor, AR. Time to rethink management strategies in asymptomatic carotid artery disease. Nat Rev Cardiol. 2011;9:116–24.CrossRefGoogle ScholarPubMed
Chang, RW, Tucker, L-Y, Rothenberg, KA, et al. Incidence of ischemic stroke in patients with asymptomatic severe carotid stenosis without surgical intervention. JAMA. 2022;327:1974–82.CrossRefGoogle ScholarPubMed
Cole, TS, Mezher, AW, Catapano, JS, et al. Nationwide trends in carotid endarterectomy and carotid artery stenting in the post-CREST era. Stroke. 2020;51:579–87.Google Scholar
Kashyap, VS, So, KL, Schneider, PA, et al. One-year outcomes after transcarotid artery revascularization (TCAR) in the ROADSTER 2 trial. J Vasc Surg. 2022;76:466–73.CrossRefGoogle ScholarPubMed
Centres for Medicare and Medicaid Services Coverage and Analysis Group. Percutaneous transluminal angioplasty (PTA)of the carotid artery concurrent with stenting. https://www.cms.gov/medicare-coverage-database/view/ncacal-decision-memo.aspx?proposed-N&ncaid-311. Accessed October 11, 2023.Google Scholar
Abbott, A, Gao, L, Budincevic, H, Ricco, J-B. Carotid artery overtreatment in the USA. Lancet Neurol. 2023;22:11021103. DOI: 10.1016/S1474-4422(23)00407-6.CrossRefGoogle ScholarPubMed
Saba, L, Scicolone, R, Johansson, E, et al. Quantifying carotid stenosis: history, current applications, limitations, and potential: how imaging is changing the scenario. Life. 2024;14:73. DOI: 10.3390/life14010073.CrossRefGoogle ScholarPubMed
Freedman, B. Equipoise and the ethics of clinical research. N Engl J Med. 1987;317:141–5.CrossRefGoogle ScholarPubMed
The EC/IC Bypass Study Group. Failure of extracranial-intracranial arterial bypass to reduce the risk of ischemic stroke – results of an international randomized trial. N Engl J Med. 1985;313:1191–200.Google Scholar