Abstract
The cause of ischemic stroke in 5–8% of cases is acute thrombosis and acute occlusion of the internal carotid artery (ICAO). Acute occlusion of the internal carotid artery is associated with deaths and their frequency in acute ischemic events is 6–15%. Acute ICAO responds poorly to intravenous thrombolysis and portends worse clinical outcomes. Extracranial and intracranial ICAOs have varied clinical course and imaging patterns, with discrete cervical acute occlusion of the internal carotid artery usually associated with better clinical outcomes while tandem occlusions predispose poor outcomes. Diagnostic catheter-based angiogram is often required since appearances of ICAO using non-invasive neuroimaging modalities are often deceiving. Repeated vascular imaging in acute to subacute phase to determine recanalization of ICAO is critical for secondary prevention.
References
- Malhotra K., Goyal N., Tsivgoulis G.Internal carotid artery occlusion: Pathophysiology, diagnosis, and management. Curr. Atheroscler. Rep. 2017; 19 (10): 41. DOI: 10.1007/s11883-017-0677-7
- Bhatia R., Hill M.D., Shobha N., Menon B. Low rates of acute recanalization with intravenous recombinant tissue plasminogen activator in ischemic stroke: real-world experience and a call for action. Stroke. 2010; 41 (10): 2254–8. DOI: 10.1161/strokeaha.110.592535
- Paciaroni M., Inzitari D., Agnelli G., Caso V. Intravenous thrombolysis or endovascular therapy for acute ischemic stroke associated with cervical internal carotid artery occlusion: the ICARO-3 study. J. Neurol. 2015; 262 (2): 459–68. DOI: 10.1007/s00415-014-7550-1
- Paciaroni M., Caso V., Venti M., Milia P., Kappelle L.J., Silvestrelli G. et al. Outcome in patients with stroke associated with internal carotid artery occlusion. Cerebrovasc. Dis. (Basel, Switzerland). 2005; 20 (2): 108–13. DOI: 10.1159/000086800
- Buslovich S., Hines G.L. Spontaneous recanalization of chronic internal carotid artery occlusions: report of 3 cases. Vasc. Endovasc. Surg. 2011; 45 (1): 93–7. DOI: 10.1177/1538574410380792
- Faught W.E., van Bemmelen P.S., Mattos M.A., Hodgson K.J., Hodgson K.J., Barkmeier L.D. et al. Presentation and natural history of internal carotid artery occlusion. J. Vasc. Surg. 1993; 18 (3): 512–23. disc. 24. DOI: 10.1016/0741-5214(93)90270-v
- PowersW.J., Derdeyn C.P., Fritsch S.M., Carpenter D.A., Yundt K.D., Videen T.O. et al. Benign prognosis of never-symptomatic carotid occlusion. Neurology. 2000; 54 (4): 878–82.
- Malhotra K., Liebeskind D.S. Collaterals in ischemic stroke. eNeuroscience. 2017; 1 (1): 1–10. DOI: 10.1177/1747493017701942
- Paciaroni M., Balucani C., Agnelli G., Caso V., Silvestrelli G., Grotta J.C. et al. Systemic thrombolysis in patients with acute ischemic stroke and Internal Carotid ARtery Occlusion: the ICARO study. Stroke. 2012; 43 (1): 125–30. DOI: 10.1161/strokeaha.111.630624
- Saqqur M., Uchino K., Demchuk A.M., Molina C.A., Garami Z., Calleja S. et al. Site of arterial occlusion identified by transcranial Doppler predicts the response to intravenous thrombolysis for stroke. Stroke. 2007; 38 (3): 948–54. DOI: 10.1161/01.STR.0000257304.21967.ba
- Rubiera M., Ribo M., Delgado-Mederos R., Santamarina E., Delgado P., Montaner J. et al. Tandem internal carotid artery/middle cerebral artery occlusion: an independent predictor of poor outcome after systemic thrombolysis. Stroke. 2006; 37 (9): 2301–5. DOI: 10.1161/01.STR.0000237070.80133.1d
- Goyal M., Menon B.K. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet (London, England). 2016; 387 (10029): 1723–31. DOI: 10.1016/s0140-6736(16)00163-x
- Fisher M. Occlusion of the internal carotid artery. AMA Arch. Neurol. Psychiatr. 1951; 65 (3): 346–77. DOI: 10.1001/archneurpsyc.1951.02320030083009
- Barnett H.J.M., Taylor D.W., Haynes R.B., Sackett D.L., Peerless S.J., Ferguson G.G. et al. Beneficial effect of carotid endarterectomy in symptomatic patients with highgrade carotid stenosis. N. Engl. J. Med. 1991; 325 (7): 445–53. DOI: 10.1056/nejm199108153250701
- North American Symptomatic Carotid Endarterectomy Trial Collaborators, Barnett H.J.M., Taylor D.W., Haynes R.B., Sackett D.L., Peerless S.J., Ferguson G.G. et al. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N. Engl. J. Med. 1991; 1991 (325): 445–53. DOI: 10.1056/nejm199108153250701
- Nakamura M., Okamoto F., Nakanishi K., Maruyama R. Does intensive management of cerebral hemodynamics and atheromatous aorta reduce stroke after coronary artery surgery? Ann. Thorac. Surg. 2008; 85 (2): 513–9. DOI: 10.1016/j.athoracsur.2007.08.056
- Tunio A.M., Hingorani A., Ascher E. The impact of an occluded internal carotid artery on the mortality and morbidity of patients undergoing coronary artery bypass grafting. Am. J. Surg.1999; 178 (3): 201–5. DOI: 10.1016/s0002-9610(99)00116-6
- Caplan L.R., van Gijn J. Stroke syndromes. 3rd ed. Cambridge UK: Cambridge University Press; 2012: 364–74. DOI: 10.1017/cbo9781139093286.031
- Leys D. Atherothrombosis: a major health burden. Cerebrovasc. Dis.2001; 11 (Suppl. 2): 1–4. DOI: 10.1159/000049137
- Caplan L.R. Diagnosis and treatment of ischemic stroke. JAMA. 1991; 266 (17): 2413–8. DOI: 10.1001/jama.1991. 03470170101032
-
Tallarita T., Lanzino G., Rabinstein A.A. Carotid intervention in acute stroke. Perspect Vasc. Surg. Endovasc. Ther. 2010; 22 (1): 49–57. DOI: 10.1177/1531003510380469
- Bos D., Ikram M.A., Elias-Smale S.E., Krestin G.P. Calcification in major vessel beds relates to vascular brain disease. Arterioscler. Thromb. Vasc. Biol. 2011; 31 (10): 2331–7. DOI: 10.1161/atvbaha.111.232728
- Hong J.M., Lee S.E., Lee S.-J., Lee J.S., Demchuk A.M. Distinctive patterns on CT angiography characterize acute internal carotid artery occlusion subtypes. Medicine. 2017; 96 (5): e5722. DOI: 10.1097/MD.0000000000005722
- Warlow C., Dennis M., van Gijn J., Hankey G.J., PAG S., Bamford J.M. et al. Stroke: A practical guide to management. Oxford: Blackwell Science; 1996. DOI: 10.1002/9780470696361
- Tsiskaridze A., Devuyst G., de Freitas G.R., van Melle G., Bogousslavsky J. Stroke with internal carotid artery stenosis. Arch. Neurol.2001; 58 (4): 605–9. DOI: 10.1001/archneur.58.4.605
- Kang D.-W., Chu K. Lesion patterns and mechanism of ischemia in internal carotid artery disease: a diffusionweighted imaging study. Arch. Neurol. 2002; 59 (10): 1577–82. DOI: 10.1001/archneur.59.10.1577
- Fusco M.R., Harrigan M.R. Cerebrovascular dissections– a review, part I: spontaneous dissections. Neurosurgery. 2011; 68 (1): 242–57. DOI: 10.1227/neu.0b013e3182012323
- Chang Y.-J., Lin S.-K., Ryu S.-J., Wai Y.-Y. Common carotid artery occlusion: evaluation with duplex sonography. Am. J. Neuroradiol. 1995; 16 (5): 1099–105.
- Ferro J.M. Cardioembolic stroke: an update. Lancet Neurol. 2003; 2 (3): 177–88. DOI: 10.1016/s1474-4422 (03)00324-7
- Jovin T.G., Gupta R., Uchino K., Jungreis C.A. Emergent stenting of extracranial internal carotid artery occlusion in acute stroke has a high revascularization rate. Stroke. 2005; 36 (11): 2426–30. DOI: 10.1161/01.str. 0000185924.22918.51
- Marder V.J., Chute D.J., Starkman S., Abolian A.M., Kidwell C., Liebeskind D. et al. Analysis of thrombi retrieved from cerebral arteries of patients with acute ischemic stroke. Stroke. 2006; 37 (8): 2086–93. DOI: 10.1161/01.STR.0000230307.03438.94
- McBane R.D., Hodge D.O., Wysokinski W.E. Clinical and echocardiographic measures governing thromboembolism destination in atrial fibrillation. Thromb. Haemost. 2008; 99 (5): 951–5. DOI: 10.1160/th07-12-0734
- Kwak J., Zhao L., Kim J., Park S., Shim J., Lee D.H. et al. The outcome and efficacy of recanalization in patients with acute internal carotid artery occlusion. Am. J. Neuroradiol. 2014; 35 (4): 747–53. DOI: 10.3174/ajnr.A3747
- Blum C.A., Yaghi S. Cervical artery dissection: a review of the epidemiology, pathophysiology, treatment, and outcome. Arch. Neurosci. 2015; 2 (4): e26670. DOI: 10.5812/archneurosci.26670
- SchievinkW.I., Mokri B., O'Fallon W.M. Recurrent spontaneous cervical-artery dissection. N. Engl. J. Med. 1994; 330 (6): 393–7. DOI: 10.1056/nejm199402103300604
- Li J., Shi D., Wei Y., Xiao J. Blood flow in the internal carotid artery with common carotid artery–occluding lesions in Takayasu arteritis. J. Ultrasound. Med. 2010; 29 (11): 1547–53. DOI: 10.7863/jum.2010.29.11.1547
- Sorteberg A., Sorteberg W., Bakke S.J., Lindegaard K.F., Boysen M., Nornes H. Cerebral haemodynamics in internal carotid artery trial occlusion. Acta Neurochir. 1997; 139 (11): 1066–73. DOI; 10.1007/bf01411562
- Malhotra K., Liebeskind D.S. Imaging in endovascular stroke trials. J. Neuroimaging. 2015; 25 (4): 517–27. DOI: 10.1111/jon.12272
- Nederkoorn P.J., Mali W.P., Eikelboom B.C., Elgersma O.E. Preoperative diagnosis of carotid artery stenosis: accuracy of noninvasive testing. Stroke. 2002; 33 (8): 2003–8. DOI: 10.1161/01.str.0000021900.58396.44
- AbuRahma A.F., Pollack J.A., Robinson P.A., Mullins D. The reliability of color duplex ultrasound in diagnosing total carotid artery occlusion. Am. J. Surg. 1997; 174 (2): 185–7. DOI: 10.1016/s0002-9610(97)90080-9
- Rundek T. Beyond percent stenosis: carotid plaque surface irregularity and risk of stroke. Int. J. Stroke. 2007; 2 (3): 169–71. DOI: 10.1111/j.1747-4949.2007.00135.x
- Alexandrov A.V. Neurovascular examination: the rapid evaluation of stroke patients using ultrasound waveform interpretation. Wiley; 2013. DOI: 10.1002/9781118583906
- Ohm C., Bendick P.J., Monash J., Bove P.G. Diagnosis of total internal carotid occlusions with duplex ultrasound and ultrasound contrast. Vasc. Endovasc. Surg. 2005; 39(3): 237–43. DOI: 10.1177/153857440503900304
- Malhotra K., Conners J.J., Lee V.H., Prabhakaran S. Relative changes in transcranial Doppler velocities are inferior to absolute thresholds in prediction of symptomatic vasospasm after subarachnoid hemorrhage. J. Stroke Cerebrovasc. Dis. 2014; 23 (1): 31–6. DOI: 10.1016/j.jstrokecerebrovasdis.2012.08.004
- Giller C.A., Mathews D., Walker B., Purdy P., Roseland A.M. Prediction of tolerance to carotid artery occlusion using transcranial Doppler ultrasound. J. Neurosurg. 1994; 81 (1): 15–9. DOI: 10.3171/jns.1994.81.1.0015
- Ritter M.A., Dittrich R., Thoenissen N., Ringelstein E.B. Prevalence and prognostic impact of microembolic signals in arterial sources of embolism. J. Neurol. 2008; 255 (7): 953–61. DOI: 10.1007/s00415-008-0638-8
- Goertler M., Blaser T., Krueger S., Hofmann K., Baeumer M., Wallesch C. Cessation of embolic signals after antithrombotic prevention is related to reduced risk of recurrent arterioembolic transient ischaemic attack and stroke. J. Neurol. Neurosurg. Psychiatry. 2002; 72 (3): 338–42. DOI: 10.1136/jnnp.72.3.338
- Buratti L., Balucani C., Viticchi G., Falsetti L., Altamura C., Avitabile E. et al. Cognitive deterioration in bilateral asymptomatic severe carotid stenosis. Stroke. 2014; 45 (7): 2072–7. DOI: 10.1161/strokeaha.114.005645
- Silvestrini M., Paolino I., Vernieri F., Pedone C. Cerebral hemodynamics and cognitive performance in patients with asymptomatic carotid stenosis. Neurology. 2009; 72 (12): 1062–8. DOI: 10.1212/01.wnl. 0000345015.35520.52
- Buratti L., Viticchi G., Falsetti L., Balucani C., Altamura C., Petrelli C. Thresholds of impaired cerebral hemodynamics that predict short-term cognitive decline in asymptomatic carotid stenosis. J. Cereb. Blood Flow Metab. 2016; 36 (10): 1804–12. DOI: 10.1177/0271678x15613526
- Bash S., Villablanca J.P., Jahan R., Duckwiler G., Tillis M., Kidwell C. et al. Intracranial vascular stenosis and occlusive disease: evaluation with CT angiography, MR angiography, and digital subtraction angiography. Am. J. Neuroradiol. 2005; 26 (5): 1012–21.
- Skutta B., Fürst G. Intracranial stenoocclusive disease: double-detector helical CT angiography versus digital subtraction angiography. Am. J. Neuroradiol. 1999; 20 (5): 791–9.
- Hirai T., Korogi Y., Ono K., Nagano M. Prospective evaluation of suspected stenoocclusive disease of the intracranial artery: combined MR angiography and CT angiography compared with digital subtraction angiography. Am. J. Neuroradiol. 2002; 23 (1): 93–101. DOI: 10.1007/3-540-26984-3_5
- Anzidei M., Napoli A., Marincola B.C. 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. 2012; 117 (1): 54–71. DOI: 10.1007/s11547-011-0651-3
- Michel P., Ntaios G., Delgado M.G., Meuli R. CT angiography helps to differentiate acute from chronic carotid occlusion: the “carotid ring sign”. Neuroradiology. 2012; 54 (2): 139–46. DOI: 10.1007/s00234-011-0868-9
- Korogi Y., Takahashi M., Nakagawa T., Mabuchi N., Shiokawa Y. Intracranial vascular stenosis and occlusion: MR angiographic findings. Am. J. Neuroradiol. 1997; 18 (1): 135–43. DOI: 10.1097/00041327-199906000-00037
- Brinjikji W., Huston J. III, Rabinstein A.A., Kim G.-M., Lerman A. Contemporary carotid imaging: from degree of stenosis to plaque vulnerability. J. Neurosurg. 2016; 124 (1): 27–42. DOI: 10.3171/2015.1.jns142452
- Kilburg C., Scott McNally J., de Havenon A., Taussky P., Kalani M.Y.S., Park M.S. Advanced imaging in acute ischemic stroke. Neurosurg. Focus. 2017; 42 (4): E10. DOI: 10.3171/2017.1.focus16503
- De Havenon A., Yuan C. Nonstenotic culprit plaque: the utility of high-resolution vessel wall MRI of intracranial vessels after ischemic stroke. Case Rep. Radiol. 2015; 2015: 356582. DOI: 10.1155/2015/356582
- Bouthillier A., Van Loveren H.R., Keller J.T. Segments of the internal carotid artery: a new classification. Neurosurgery. 1996; 38 (3): 425–33. DOI: 10.1227/00006123-199603000-00001
About the authors
- Ramiz A. Abdulgasanov, Dr. Med. Sc., Chief Researcher, orcid.org/0000-0002-2126-3139
- Mukhamed A. Shogenov, Postgraduate, orcid.org/0000-0002-9467-3729
- Valeriy S. Arakelyan, Dr. Med. Sc., Professor, Head of the Department, orcid.org/0000-0002-0284-6793