Ultrasound detection of cerebral microembolism in carotid stenoses: progress and perspective (A review of the literature)

Keywords: transcranial doppler sonography; carotid artery stenosis; mycroembolic signals.

Abstract

The review summarizes available information regarding the method of Transcranial doppler sonography (TCD) usage to record microembolism in patients with carotid artery stenosis, search for information was carried out in literature 1997–2020 (PUBMED, MEDLINE).
History overview of TCD with embolodetection implementation is presented, as well as ways of its technical and methodological improvement. Evidence-based studies of the method clinical relevance in atherosclerotic carotid stenoses and their surgical treatment are outlined. Observation results of the intraoperative cerebral embolization during carotid endarterectomy and carotid artery stenting are presented along with comparison of TCD-embolodetection data, neuroimaging and clinical outcomes.
Individual centres and multicenter study ACES data on prognostic value of registration of embolic signals in asymptomatic carotid stenosis, risk assessment of vascular events in diffe-rent groups of patients and in varying degrees of stenosis of the vessel lumen was analyzed. The role of embolodetection in predicting repeated cerebrovascular disorders in symptomatic carotid stenosis and its importance for monitoring antiplatelet therapy is set out (multicenter study CARESS). The evidence of the reliability of TCD embolodetection as tool for verificarion of at-risk patients with carotid stenosis who may benefit ftom surgical treatment is presented.
Recent advances in ultrasound and other imaging techniques for assessing unstable plague are outlined along with prospects for the use of TCD monitoting for cerebrovascular disorders forecasting.

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References

Norrving B, Barrick J, Davalos A et al. Action Plan for Stroke in Europe 2018–2030. Eur Stroke J. 2018 Dec;3(4):309-36. doi:10.1177/2396987318808719.

Radu RA, Terecoasă EO, Băjenaru OA, Tiu C. Etiologic classification of ischemic stroke: Where do we stand? Clin Neurol Neurosurg. 2017 Aug;159:93-106. doi:10.1016/j.clineuro.2017.05.019.

Naylor AR, Ricco JB, de Borst GJ et al. Editor’s Choice - Management of Atherosclerotic Carotid and Vertebral Artery Disease: 2017 Clinical Practice Guidelines of the European Society for Vascular Surgery (ESVS). Eur J Vasc Endovasc Surg. 2018; Jan; 55(1):3-81. doi:10.1016/j.ejvs.2017.06.021

Аusten WG, Howry DH. Ultrasound as a method to detect bubbles or particular matter in the arterial line during cardiopulmonary bypass. J Surg Res. 1965;5:283-94.

Spencer MP, Lawrence GH, Thomas GI, Sauvage LR. The use of ultrasonics in the determination of arterial aeroembolism during open-heart surgery. Ann Thorac Surg. 1969 Dec; 8(6):489-97. doi:10.1016/s0003-4975(10)66085-7

Aaslid R, Markwalder TM, Nornes H. Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J. Neurosurg. 1982;57(6):769-74. doi:10.3171/jns.1982.57.6.0769

Valdueza JМ, Schreiber SJ, Roehl J-E, Kingebiel R. Nejrosonologija i nejrovizualizatsija pri insulti. Pod red. VG Leljuka, LV Gubskogo. 2012; M: Medpressinform, 605 p. (Rus)

Georgiadis D, Lindner A, Manz M et al. Intracranial microembolic signals in 500 patients with potential cardiac or carotid embolic source and in normal controls. Stroke. 1997 Jun;28(6):1203-07. doi:10.1161/01.str.28.6.1203

Basic identification criteria of Doppler microembolic signals. Consensus Committee of the Ninth International Cerebral Hemodynamic Symposium [No authors listed]. Stroke. 1995 Jun;26(6):1123 https://doi.org/10.1161/01.STR.26.6.1123

Ringelstein RB, Droste DW, Babikian VI et al. Consensus on microembolus detection by TCD: international consensus group on microembolus detection. Stroke. 1998 Mar;29(3):725-9. doi:10.1161/01.str.29.3.725

Ries F, Tiemann K, Pohl C et al. High-resolution emboli detection and differentiation by characteristic postembolic spectral patterns. Stroke. 1998, Mar;29(3):668-72. doi:10.1161/01.str.29.3.668

Furui E, Hanzawa K, Ohzeki H et al. «Tail sign» associated with microembolic signals. Stroke. 1999 Apr;30(4):863-6. doi:10.1161/01.str.30.4.863

Telman G, Sprecher E, Kouperberg E et al. Potential relevance of low-intensity microembolic signals by TCD monitoring. Neurol Sci. 2011 Feb;32(1):107-11. doi:10.1007/s10072-010-0429-8

Rybalko NV. Razvitije dopplerovskoj detekciji cerebralnoj emboliji. Vestnik Natsionalnogo mediko-hirurgicheskogo Centra im. N.I. Pirogova. 2014, 9 (4):89-93. (Rus).

Russell D, Brucher R. Online automatic discrimination between solid and gaseous cerebral microemboli with the first multifrequency transcranial Doppler. Stroke. 2002, 33(8):1975-80. doi:10.1161/01.str.0000022809.46400.4b

Markus Н, Punter M. Can transcranial doppler discriminate between solid and gaseous microemboli?: Assesment of dual-frequency trancducer system. Stroke. 2005;36(8):1731-4. doi:10.1161/01.STR.0000173399.20127.b3

Mess WH, Willigers JM, Ledoux LA et al. Microembolic signal description: a reappraisal based on a customized digital postprocessing system. Ultrasound Med Biol. 2002 Nov-Dec;28(11-12):1447-55. doi:10.1016/s0301-5629(02)00618-x

Leunissen T, van Vriesland D, den Ruijter H et al. Validation of the automated electronic microemboli detection system in patients undergoing carotid endarterectomy. Ultraschall Med. 2018 Apr;39(2):198-205. doi:10.1055/s-0043-106737

Choi Y, Saqqur M, Stewart E et al. Relative energy index of microembolic signal can predict malignant microemboli. Stroke 2010 Apr;41(4):700-06. doi:10.1161/STROKEAHA.109.573733. Epub 2010 Feb 25

Saedon M, Dilshad A, Tiivas C al. Prospective validation study of transorbital Doppler ultrasound imaging for the detection of transient cerebral microemboli. Br J Surg. 2014 Nov;101(12):1551-5. doi:10.1002/bjs.9634

Dittrich R, Ritter MA, Kaps M et al. The use of embo-lic signal detection in multicenter trials to evaluate antiplatelet efficacy: signal analysis and quality control mechanisms in the CARESS (clopidogrel and aspirin for reduction of emboli in symptomatic carotid stenosis) trial. Stroke 2006;37:1065-1069. doi:10.1161/01.STR.0000209331.39894.3d

Spenser MP, Thomas GI, Nicholls SC, Sauvage LR. Detection of middle cerebral artery emboli during carotid endarterectomy using transcranial Doppler ultrasonography. Stroke. 1990;21:415-23. doi:10.1161/01.str.21.3.415

Spenser MP. Transcranial Doppler monitoring and causes of stroke from carotid endarterectomy. Stroke. 1997;28:685-91. doi:10.1161/01.str.28.4.685

Levi CR, O’Malley HM, Fell G et al. Transcranial Doppler detected cerebral microembolism following carotid endarterectomy. High microembolic signal loads predict postoperative cerebral ischaemia. Brain 1997;120(Pt 4):621-9. doi:10.1093/brain/120.4.621

Cantelmo NL, BabikianVL, Samaraweera RN et al. Cerebral microembol­ism and ischemic chan-ges associated with carotid endarterectomy. J Vasc Surg. 1998;27(6):1024–30. doi:10.1016/s0741-5214(98)70005-9

Abbott AL, Levi CR, Stork JL, Donnan GA. Timing of clinically significant microembolism after carotid endarterectomy. Cerebrovasc Dis. 2007;23(5-6):362-7. PMID:17268167 doi:10.1159/000099135

Chernjak VA, Kovalevskaja OA, Dynnik OB et al. Monitoring mozkovogo krovotoka metodom transkranialnoj dopplerografiyi kak princip ocenki effektivnosti infuzionnoj terapiyi pri rekonstruktivnyh operacijah na brachiocefalnyh arterijah. Ukrajinskij himioterapevtychnyj zhurn. 2012; 3(26): 266-70 (Ukr) https://www.uf.ua/wp-content/uploads/2017/09/945071a9a2d311ea47a135a93baac4d9.pdf

Gossetti B, Gattuso R, Irace L et al. Embolism to the brain during carotid stenti­ng and surgery. Acta Chir Belg. 2007 Mar-Apr;107(2):151-4. PMID:17515263

Tedesco MM, Lee JT, Dalman RL et al. Postprocedu-ral microembolic events following carotid surgery and carotid angioplasty and stenting. J Vasc Surg. 2007 Aug;46(2):244-50. doi:10.1016 / j.jvs.2007.04.049

Timaran CH, Rosero EB, Higuera A. et al. Rando-mized clinical trial of open-cell vs closed-cell stents for carotid stenting and effects of stent design on cerebral embolization. J Vasc Surg. 2011 Nov;54(5):1310-6.e1; discussion 1316. doi:10.1016/j.jvs.2011.05.013

Rybalko NV, Batrashov NV, Vinogradov OI, Kuznet-sov AN. Cerebralnaya embolija i svjazannyje c ney sosudistyje oslozhnenija pri provedeniji karotidnoj endarterektomiji i karotidnoj angioplastiki so stentirovanijem. Ateroskleroz i dislipidemija. 2016;1:48-55. (Rus)

Piorkowski M, Kläffling C, Botsios S et al. Postinterventional microembolism signals detected by transcranial Doppler ultrasound after carotid artery stenting. Vasa. 2015 Jan;44(1):49-57. doi: 10.1024/0301-1526/a000406

Palombo G, Stella N, Fantozzi C Transcranial Doppler and diffusion-weighted magnetic resonance evaluation of cerebral embolization occurring during transfemoral carotid stenting with proximal flow blockage. J Cardiovasc Surg (Torino). 2016 Feb;57(1):52-7. PMID:26771727

Spacek M, Sorrell VL, Veselka J. Transcranial doppler ultrasound in the current era of carotid artery stenting. Ultraschall Med. 2015 Aug;36(4):337-41. doi:10.1055/s-0034-1366677

Amarenco P. Underlying pathology of stroke of unknown cause (cryptogenic stroke). Cerebrovascular diseases. 2009;27(1):97-103. doi:10.1159/000200446

Zuromskis T, Wetterholm R, Lindqvist JF et al. Prevalence of micro-emboli in symptomatic high grade carotid artery disease: A transcranial doppler study. Eur J Vasc Endovasc Surg. 2008 May;35(5):534-40. doi:10.1016/j.ejvs.2008.01.001

Spence JD. Transcranial Doppler monitoring for microemboli: a marker of a high-risk carotid plaque. Semin Vasc Surg. 2017 Mar;30(1):62-6. doi:10.1053/j.semvascsurg.2017.04.011

Ritter MA, Dittrich R, Thoenissen N et al. Prevalence and prognostic impact of microembolic signals in arterial sources of embolism. A systematic review of the literature. J Neurol. 2008 Jul;255(7):953-61. doi:10.1007/s00415-008-0638-8

King A, Markus HS. Doppler embolic signals in cerebrovascular disease and prediction of stroke risk: a systematic review and meta-analysis. Stroke. 2009 Dec;40(12):3711-7. doi:10.1161/STROKEAHA.109.563056

Boulon C, Baud J-M, Kercret G et al. Détection de signaux micro-emboliques: revue de la littérature. Journal Des Maladies Vasculaire. 2012;37(6):311-9. doi:10.1016/j.jmv.2012.10.001

Müller H, Fisch L, Viaccoz A. Embolic and hemodynamic transcranial doppler characteristics in patients with acute ischemic stroke due to carotid occlusive disease: contribution to the different infarct patterns on MRI. J Neuroimaging. 2015 Sep-Oct;25(5):766-75. doi:10.1111/jon.12197

Markus HS, King A, Shipley M et al. Asymptomatic embolisation for prediction of stroke in the Asymptomatic Carotid Emboli Study (ACES): a prospective observational study. Lancet Neurol. 2010 Jul;9(7):663-71. doi:10.1016/S1474-4422(10)70120-4

Abbott AL, Merican J, Pearce DC et al. Asymptoma-tic carotid stenosis is associated with circadian and other variability in embolus detection. Front Neurol. 2019 Apr 16;10:322. doi:10.3389/fneur.2019.00322

Spence DJ. Advances in stroke prevention. J Transl Int Med. 2018 Oct 9;6(3):105-14. doi:10.2478/jtim-2018-0024

Markus HS, Droste DW, Kaps M et al. Dual antiplatelet therapy with clopidogrel and aspirin in symptoma-tic carotid stenosis evaluated using doppler embolic signal detection: the Clopidogrel and Aspirin for Reduction of Emboli in Symptomatic Carotid Stenosis (CARESS) trial. Circulation. 2005 May 3;111(17):2233-40. doi:10.1161/01.CIR.0000163561.90680.1C

Kerasnoudis A, Meves SH, Gold R, Krogias C. Correlation between frequency of microembolic signals and efficacy of antiplatelet therapy in symptomatic carotid disease. J Neuroimaging. 2013 Oct;23(4):484-8. doi:10.1111/j.1552-6569.2012.00770.x

Lam TD, Lammers S, Munoz C et al. Diabetes, intracranial stenosis and microemboli in asymptomatic carotid stenosis. Can J Neurol Sci. 2013 Mar;40(2):177-81. doi:10.1017/s031716710001369x

Safouris A, Katsanos AH, Kerasnoudis A et al. Statin pretreatment and microembolic signals in large artery atherosclerosis. Stroke. 2018 Aug;49(8):1992-5. doi: 10.1161/STROKEAHA.118.021542

Topakian R, King A, Kwon SU et al. Ultrasonic plaque echolucency and emboli signals predict stroke in asymptomatic carotid stenosis. Neurology. 2011 Aug 23;77(8):751-8. doi:10.1212/WNL.0b013e31822b00a6

Van Lammeren GW, Van De Mortel RH, Visscher M et al. Spontaneous preoperative microembolic signals detected with transcranial Doppler are associated with vulnerable carotid plaque characteristics. J Cardiovasc Surg (Torino). 2014 Jun;55(3):375-80. PMID:23817452

Moustafa RR, Izquierdo-Garcia D, Fryer TD et al. Carotid plaque inflammation is associated with cerebral microembolism in patients with recent transient ischemic attack or stroke: a pilot study. Circ Cardiovasc Imaging. 2010 Sep;3(5):536-41. doi:10.1161/CIRCIMAGING.110.938225

Müller HF, Viaccoz A, Fisch L et al. 18FDG-PET-CT: an imaging biomarker of high-risk carotid plaques. Correlation to symptoms and microembolic signals. Stroke. 2014 Dec;45(12):3561-6. doi:10.1161/STROKEAHA.114.006488

Staub D, Partovi S, Schinkel AF et al. Correlation of carotid artery atherosclerotic lesion echogenicity and severity at standard US with intraplaque neovascularization detected at contrast-enhanced US. Radiology. 2011;258(2):618-26. doi:10.1148/radiol.10101008

Garrard JW, Ummur P, Nduwayo S et al. Shear wave elastography may be superior to greyscale median for the identification of carotid plaque vulnerability: A comparison with histology. Ultraschall in der Medizin (Stuttgart, Germany, 1980). 2015;36(4):386-90. doi:10.1055/s-0034-1399676

Skagen K, Skjelland M, Zamani M, Russell D. Unstable carotid artery plaque: new insights and controversies in diagnostics and treatment. Croat Med J. 2016 Aug;57(4):311-20. doi:10.3325/cmj.2016.57.311

Zamani M, Skagen K, Scott H et al. Advanced ultrasound methods in assessment of carotid plaque instability: a prospective multimodal study. BMC Neurol. 2020 Jan 29;20(1):39. doi:10.1186/s12883-020-1620-z

Sheriff F, Diz-Lopes M, Khawaja A et al. Microemboli after successful thrombectomy do not affect outcome but predict new embolic events. Stroke. 2020 Jan;51(1):154-61. doi:10.1161/STROKEAHA.119.025856


Abstract views: 17
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Published
2020-07-07
How to Cite
Globa, M. (2020). Ultrasound detection of cerebral microembolism in carotid stenoses: progress and perspective (A review of the literature). Endovascular Neuroradiology, 31(1), 56-67. https://doi.org/10.26683/2304-9359-2020-1(31)-56-67