Perioperative silent strokes in carotid artery surgery: a systematic review and meta-analysis

Smirnova A.V.; Berikashvili L.B.; Polyakov P.A.; Yadgarov M.Ya.; Shemetova M.M.; Makarevich D.G.; Kuzovlev A.N.; Kadantseva K.K.; Likhvantsev V.V.

doi:https://doi.org/10.17116/anaesthesiology202501181

Close metadata

BACKGROUND

Carotid artery (CA) atherosclerosis is responsible for up to 20% of all cases of cerebral ischemia and often requires surgical intervention. An important issue in contemporary medicine is perioperative silent brain infarctions (covert strokes) associated with postoperative neurocognitive disorders and subsequent ischemic strokes.

OBJECTIVE

To determine the frequency of covert strokes following elective CA surgery and to identify risk factors for this outcome.

MATERIAL AND METHODS

A meta-analysis was conducted in accordance with the PRISMA guidelines and the Cochrane Collaboration’s protocols. Literature searching was performed using PubMed (Medline) and Cochrane Library (CENTRAL) databases. Searching was supplemented by snowball sampling methods (Litmaps web application). The risk of systematic bias was assessed using the CLARITY tool. Internal validity and evidence level were evaluated using the GRADE system.

RESULTS

Analysis included 27 studies and 5644 patients. The incidence of covert strokes after CA surgery was 19%. Risk factors for this complication were diabetes mellitus (p<0.001) and hypertensive disease (p=0.036). Statin intake was a protective factor (p=0.012). Covert stroke detection rate was significantly higher for MRI compared to CT (22% versus 3%, p<0.001). The incidence of covert stroke after CA stenting was 38% compared to 10% after carotid endarterectomy (CEA) (p<0.001). The incidence of covert stroke was 3.75 (95% CI 2.89; 4.87) times higher after CA stenting compared to CEA (relative risk reduction [RRR] 73.3%, p<0.001).

CONCLUSION

About 20% of patients experience perioperative covert stroke (high evidence level) in elective CA surgery. The risk of covert stroke is 3.75 times higher for CA stenting compared to CEA (moderate evidence level). Moreover, 3 out of 4 covert strokes in patients with CA stenting could be avoided by changing the type of surgical intervention.

Keywords:

silent stroke

cerebral infarction

carotid endarterectomy

carotid artery stenting

carotid artery atherosclerosis

Authors:

Smirnova A.V.

Federal Research Clinical Center for Intensive Care and Rehabilitation

ORCID: 0000-0001-7860-6609

Berikashvili L.B.

Federal Research Clinical Center of Intensive Care and Rehabilitology

ORCID: 0000-0001-9267-3664

Polyakov P.A.

Federal Research Clinical Center for Intensive Care and Rehabilitation

ORCID: 0009-0009-6185-349X

Yadgarov M.Ya.

Federal Research and Clinical Centre of Intensive Care and Rehabilitology

ORCID: 0000-0003-3792-1682

Shemetova M.M.

Federal Research and Clinical Centre of Intensive Care and Rehabilitology

ORCID: 0000-0003-0872-1825

Makarevich D.G.

Federal Research and Clinical Centre of Intensive Care and Rehabilitology

Kuzovlev A.N.

Negovsky Research Institute of Intensive Care

SPIN RSCI: 8648-3771
Scopus AuthorID: 35201397900
ResearcherID: F-6462-2017
ORCID: 0000-0002-5930-0118

Kadantseva K.K.

Federal Research and Clinical Centre of Intensive Care and Rehabilitology

ORCID: 0000-0002-6593-8580

Likhvantsev V.V.

Federal Research Clinical Center of Intensive Care and Rehabilitology

ORCID: 0000-0002-5442-6950

Received:

16.09.2024

Accepted:

06.10.2024

Close metadata

References:

Song P, Fang Z, Wang H, Cai Y, Rahimi K, Zhu Y, Fowkes FGR, Fowkes FJI, Rudan I. Global and regional prevalence, burden, and risk factors for carotid atherosclerosis: a systematic review, meta-analysis, and modelling study. Lancet Global Health. 2020;8(5):e721-e729. https://doi.org/10.1016/S2214-109X(20)30117-0
Forgo B, Medda E, Hernyes A, Szalontai L, Tarnoki DL, Tarnoki AD. Carotid artery atherosclerosis: A review on heritability and genetics. Twin Research and Human Genetics. 2018;21(5):333-346. https://doi.org/10.1017/thg.2018.45
Aliev VA, Yavorovskii AG, Shaposhnikov AA, Loriya IZh, Vetsheva MS. Comparative Evaluation of Modern Inhalation Anesthetics in Carotid Endarterectomy. General Reanimatology. 2019;15(1):27-38. (In Russ.). https://doi.org/10.15360/1813-9779-2019-1-27-38
Flaherty ML, Kissela B, Khoury JC, Alwell K, Moomaw CJ, Woo D, Khatri P, Ferioli S, Adeoye O, Broderick JP, Kleindorfer D. Carotid artery stenosis as a cause of stroke. Neuroepidemiology. 2012;40(1):36-41. https://doi.org/10.1159/000341410
Petty GW, Brown RD, Whisnant JP, Sicks JRD, O’Fallon WM, Wiebers DO. Ischemic stroke subtypes: A population-based study of incidence and risk factors. Stroke. 1999;30(12):2513-2516. https://doi.org/10.1161/01.STR.30.12.2513
Finn C, Giambrone AE, Gialdini G, Delgado D, Baradaran H, Kamel H, Gupta A. The Association between Carotid Artery Atherosclerosis and Silent Brain Infarction: A Systematic Review and Meta-analysis. Journal of Stroke and Cerebrovascular Diseases. 2017;26(7):1594-1601. https://doi.org/10.1016/j.jstrokecerebrovasdis.2017.02.028
Syrovatskiy AA, Saiganov SA, Lebedinskii KM. Anesthesia technique choice motives for carotid endarterectomy. Russian Journal of Anesthesiology and Reanimatology. 2022;(2):73-79. (In Russ.). https://doi.org/10.17116/anaesthesiology202202173
Bonati LH, Jansen O, de Borst GJ, Brown MM. Management of atherosclerotic extracranial carotid artery stenosis. Lancet Neurology. 2022;21(3):273-283. https://doi.org/10.1016/S1474-4422(21)00359-8
Reiff T, Eckstein HH, Mansmann U, Jansen O, Fraedrich G, Mudra H, Böckler D, Böhm M, Debus ES, Fiehler J, Mathias K, Ringelstein EB, Schmidli J, Stingele R, Zahn R, Zeller T, Niesen WD, Barlinn K, Binder A, Glahn J, Hacke W, Ringleb PA; SPACE-2 Investigators. Carotid endarterectomy or stenting or best medical treatment alone for moderate-to-severe asymptomatic carotid artery stenosis: 5-year results of a multicentre, randomised controlled trial. Lancet Neurology. 2022;21(10):877-888. https://doi.org/10.1016/S1474-4422(22)00290-3
Winstein CJ, Stein J, Arena R, Bates B, Cherney LR, Cramer SC, Deruyter F, Eng JJ, Fisher B, Harvey RL, Lang CE, MacKay-Lyons M, Ottenbacher KJ, Pugh S, Reeves MJ, Richards LG, Stiers W, Zorowitz RD; American Heart Association Stroke Council, Council on Cardiovascular and Stroke Nursing, Council on Clinical Cardiology, and Council on Quality of Care and Outcomes Research. Guidelines for Adult Stroke Rehabilitation and Recovery: A Guideline for Healthcare Professionals from the American Heart Association/American Stroke Association. Stroke. 2016;47(6):e98-e169. https://doi.org/10.1161/STR.0000000000000098
Mrkobrada M, Hill MD, Chan MT, Sigamani A, Cowan D, Kurz A, Sessler DI, Jacka M, Graham M, Dasgupta M, Dunlop V, Emery DJ, Gulka I, Guyatt G, Heels-Ansdell D, Murkin J, Pettit S, Sahlas DJ, Sharma M, Sharma M, Srinathan S, St John P, Tsai S, Gelb AW, O’Donnell M, Siu D, Chiu PW, Sharath V, George A, Devereaux PJ. Covert stroke after non-cardiac surgery: A prospective cohort study. British Journal of Anaesthesia. 2016;117(2):191-197. https://doi.org/10.1093/bja/aew179
Indja B, Woldendorp K, Vallely MP, Grieve SM. Silent Brain Infarcts Following Cardiac Procedures: A Systematic Review and Meta-Analysis. Journal of the American Heart Association. 2019;8(9):e010920. https://doi.org/10.1161/JAHA.118.010920
Pagnesi M, Martino EA, Chiarito M, Mangieri A, Jabbour RJ, Van Mieghem NM, Kodali SK, Godino C, Landoni G, Colombo A, Latib A. Silent cerebral injury after transcatheter aortic valve implantation and the preventive role of embolic protection devices: A systematic review and meta-analysis. International Journal of Cardiology. 2016;221:97-106. https://doi.org/10.1016/j.ijcard.2016.06.143
Mrkobrada M, Chan MTV, Cowan D; NeuroVISION Investigators. Perioperative covert stroke in patients undergoing non-cardiac surgery (NeuroVISION): a prospective cohort study. Lancet. 2019;394(10203):1022-1029. https://doi.org/10.1016/S0140-6736(19)31795-7
Guo J, Zhou C, Yue L, Yan F, Shi J. Incidence and Risk Factors for Silent Brain Infarction After On-Pump Cardiac Surgery: A Meta-analysis and Meta-regression of 29 Prospective Cohort Studies. Neurocritical Care. 2021;34(2):657-668. https://doi.org/10.1007/s12028-020-01048-5
Shibagaki K, Shirasaka T, Sawada J, Saijo Y, Kunioka S, Kikuchi Y, Kamiya H. Silent cerebral ischemia detected by magnetic resonance imaging can predict postoperative delirium after total arch replacement for aneurysm. JTCVS Open. 2022;10:87-96. https://doi.org/10.1016/j.xjon.2022.02.026
Yu S, Li P. Cognitive declines after perioperative covert stroke: Recent advances and perspectives. Current Opinion in Anaesthesiology. 2020;33(5):651-654. https://doi.org/10.1097/ACO.0000000000000903
Gupta A, Giambrone AE, Gialdini G, Finn C, Delgado D, Gutierrez J, Wright C, Beiser AS, Seshadri S, Pandya A, Kamel H. Silent Brain Infarction and Risk of Future Stroke: A Systematic Review and Meta-Analysis. Stroke. 2016;47(3):719-725. https://doi.org/10.1161/STROKEAHA.115.011889
Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. PLoS Medicine. 2009;6(7):e1000100. https://doi.org/10.1371/journal.pmed.1000100
Cochrane Handbook for Systematic Reviews of Interventions. Published online January 01, 2019. https://doi.org/10.1002/9781119536604
Litmaps. Your Literature Review Assistant. Accessed April 27, 2024. https://www.litmaps.com
Luo D, Wan X, Liu J, Tong T. Optimally estimating the sample mean from the sample size, median, mid-range, and/or mid-quartile range. Statistical Methods in Medical Research. 2018;27(6):1785-1805. https://doi.org/10.1177/0962280216669183
Wan X, Wang W, Liu J, Tong T. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Medical Research Methodology. 2014;14(1):135. https://doi.org/10.1186/1471-2288-14-135
Tool to Assess Risk of Bias in Cohort Studies DistillerSR — DistillerSR. Accessed April 27, 2024. https://www.distillersr.com/resources/methodological-resources/tool-to-assess-risk-of-bias-in-cohort-studies-distillersr
McGuinness LA, Higgins JPT. Risk-of-bias VISualization (robvis): An R package and Shiny web app for visualizing risk-of-bias assessments. Research Synthesis Methods. 2021;12(1):55-61. https://doi.org/10.1002/jrsm.1411
Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. British Medical Journal. 1997;315(7109):629-634. https://doi.org/10.1136/bmj.315.7109.629
TSA — ctu.dk. Published 2021. Accessed April 18, 2024. https://ctu.dk/tsa
Leal I, Orgaz A, Flores Á, Gil J, Rodríguez R, Peinado J, Criado E, Doblas M. A diffusion-weighted magnetic resonance imaging-based study of transcervical carotid stenting with flow reversal versus transfemoral filter protection. Journal of Vascular Surgery. 2012;56(6):1585-1590. https://doi.org/10.1016/j.jvs.2012.05.107
Orlický M, Hrbáč T, Sameš M, Vachata P, Hejčl A, Otáhal D, Havelka J, Netuka D, Herzig R, Langová K, Školoudík D. Anesthesia type determines risk of cerebral infarction after carotid endarterectomy. Journal of Vascular Surgery. 2019;70(1):138-147. https://doi.org/10.1016/j.jvs.2018.10.066
Hassan AA, Fawzy W, Abouelnaga A, Gabr AK, Essa AA. Carotid artery stenting for symptomatic carotid artery stenosis: An early experience in 15 cases. Ain-Shams Journal of Surgery. 2012;10(2):715-722. https://doi.org/10.21608/asjs.2012.179372
Madycki G, Staszkiewicz W, Gabrusiewicz A. Carotid plaque texture analysis can predict the incidence of silent brain infarcts among patients undergoing carotid endarterectomy. European Journal of Vascular and Endovascular Surgery. 2006;31(4):373-380. https://doi.org/10.1016/j.ejvs.2005.10.010
Hammer FD, Lacroix V, Duprez T, Grandin C, Verhelst R, Peeters A, Cosnard G. Cerebral microembolization after protected carotid artery stenting in surgical high-risk patients: Results of a 2-year prospective study. Journal of Vascular Surgery. 2005;42(5):847-853. https://doi.org/10.1016/j.jvs.2005.05.065
Gossetti B, Gattuso R, Irace L, Faccenna F, Venosi S, Bozzao L, Fiorelli M, Andreoli R, Gossetti C. Embolism to the brain during carotid stenting and surgery. Acta Chirurgica Belgica. 2016;107(2):151-154. https://doi.org/10.1080/00015458.2007.11680032
Pascot R, Daoudal A, Cardon A, Godet G, Lucas A, Clochard E, Gauvrit JY, Le Teurnier Y, Kaladji A. Evaluation by Magnetic Resonance Imaging of Silent Brain Infarcts in Preoperative and Postoperative Asymptomatic Carotid Surgery. Annals of Vascular Surgery. 2017;43:258-264. https://doi.org/10.1016/j.avsg.2016.10.067
Yoshimura S, Yamada K, Kawasaki M, Asano T, Kanematsu M, Takamatsu M, Hara A, Iwama T. High-intensity signal on time-of-flight magnetic resonance angiography indicates carotid plaques at high risk for cerebral embolism during stenting. Stroke. 2011;42(11):3132-3137. https://doi.org/10.1161/STROKEAHA.111.615708
Rots ML, Fassaert LMM, Kappelle LJ, de Groot MCH, Haitjema S, Bonati LH, van Klei WA, de Borst GJ. Intra-Operative Hypotension is a Risk Factor for Post-operative Silent Brain Ischaemia in Patients with Pre-operative Hypertension Undergoing Carotid Endarterectomy. European Journal of Vascular and Endovascular Surgery. 2020;59(4):526-534. https://doi.org/10.1016/j.ejvs.2020.01.007
Huo R, Yuan W, Xu H, Yang D, Qiao H, Han H, Wang T, Liu Y, Yuan H, Zhao X. Investigating the Association of Carotid Atherosclerotic Plaque MRI Features and Silent Stroke After Carotid Endarterectomy. Journal of Magnetic Resonance Imaging: JMRI. 2024;60(1):138-149. https://doi.org/10.1002/jmri.29115
Müller M, Reiche W, Langenscheidt P, Haßfeld J, Hagen T. Ischemia after carotid endarterectomy: Comparison between transcranial Doppler sonography and diffusion-weighted MR imaging. American Journal of Neuroradiology. 2000;21(1):47-54.
Lacroix V, Hammer F, Astarci P, Duprez T, Grandin C, Cosnard G, Peeters A, Verhelst R. Ischemic Cerebral Lesions after Carotid Surgery and Carotid Stenting. European Journal of Vascular and Endovascular Surgery. 2007;33(4):430-435. https://doi.org/10.1016/j.ejvs.2006.11.012
Wolf O, Heider P, Heinz M, Poppert H, Sander D, Greil O, Weiss W, Hanke M, Eckstein HH. Microembolic signals detected by transcranial Doppler sonography during carotid endarterectomy and correlation with serial diffusion-weighted imaging. Stroke. 2004;35(11):e373-375. https://doi.org/10.1161/01.str.0000143184.69343.ec
Bonati LH, Jongen LM, Haller S, Flach HZ, Dobson J, Nederkoorn PJ, Macdonald S, Gaines PA, Waaijer A, Stierli P, Jäger HR, Lyrer PA, Kappelle LJ, Wetzel SG, van der Lugt A, Mali WP, Brown MM, van der Worp HB, Engelter ST; ICSS-MRI study group. New ischaemic brain lesions on MRI after stenting or endarterectomy for symptomatic carotid stenosis: a substudy of the International Carotid Stenting Study (ICSS). Lancet Neurology. 2010;9(4):353-362. https://doi.org/10.1016/S1474-4422(10)70057-0
Pascot R, Parat B, Le Teurnier Y, Godet G, Gauvrit JY, Gouëffic Y, Steinmetz E, Cardon A, Kaladji A. Predictive Factors of Silent Brain Infarcts after Asymptomatic Carotid Endarterectomy. Annals of Vascular Surgery. 2018;51:225-233. https://doi.org/10.1016/j.avsg.2018.02.037
Roh HG, Byun HS, Ryoo JW, Na DG, Moon WJ, Lee BB, Kim DI. Prospective analysis of cerebral infarction after carotid endarterectomy and carotid artery stent placement by using diffusion-weighted imaging. American Journal of Neuroradiology. 2005;26(2):376-384.
Kazantsev A, Korotkikh A, Lider R, Lebedev O, Sirotkin A, Palagin P, Mukhtorov O, Shmatov D, Artyukhov S, Ageev I, Rogova A, Kalichkin I, Beglaryan J, Snigur A, Belov Y. Results of carotid endarterectomy with the use of temporary shunts with reduced retrograde pressure in the internal carotid artery — analysis of the multicenter Russian register. Indian Journal of Thoracic and Cardiovascular Surgery. 2023;39(3):244-250. https://doi.org/10.1007/s12055-023-01487-7
Tedesco MM, Coogan SM, Dalman RL, et al. Risk Factors for Developing Postprocedural Microemboli following Carotid Interventions. Journal of Endovascular Therapy. 2007;14(4):561-567. https://doi.org/10.1177/152660280701400419
Kuliha M, Školoudík D, Roubec M, Herzig R, Procházka V, Jonszta T, Krajča J, Czerný D, Hrbáč T, Otáhal D, Langová K. Risk reduction of brain infarction during carotid endarterectomy or stenting using sonolysis — Prospective randomized study pilot data. AIP Conference Proceeding. 2012;1503(1):239-243. https://doi.org/10.1063/1.4769951
Pinter L, Ribo M, Loh C, Lane B, Roberts T, Chou TM, Kolvenbach RR. Safety and feasibility of a novel transcervical access neuroprotection system for carotid artery stenting in the PROOF Study. Journal of Vascular Surgery. 2011;54(5):1317-1323. https://doi.org/10.1016/j.jvs.2011.04.040
Alimi Y, Kallee K, Poncet M, Fabre D, Doddoli C, Barthelemy P, Juhan C. Silent Brain Infarct After Carotid Artery Surgery: Incidence and Prevention. Annals of Vascular Surgery. 1995;9(Suppl.):S76-80. https://doi.org/10.1016/S0890-5096(06)60455-X
Ryu JC, Lee DH, Chang JY, Kang DW, Kwon SU, Kim BJ. Silent brain infarcts after carotid or vertebrobasilar artery stenting. Journal of Neuroimaging. 2023;33(4):590-597. https://doi.org/10.1111/jon.13097
Gode S, Denli Yalvac S, Asik M, Ahmedov F, Sen O, Oz K, Erkanli K. Silent cerebral embolism after carotid endarterectomy: a two-center experience. European Research Journal. 2017;3:188-195. https://doi.org/10.18621/eurj.284652
Barth A, Remonda L, Lövblad KO, Schroth G, Seiler RW. Silent cerebral ischemia detected by diffusion-weighted MRI after carotid endarterectomy. Stroke. 2000;31(8):1824-1828. https://doi.org/10.1161/01.STR.31.8.1824
Capoccia L, Sbarigia E, Rizzo A, Mansour W, Speziale F. Silent stroke and cognitive decline in asymptomatic carotid stenosis revascularization. Vascular. 2012;20(4):181-187. https://doi.org/10.1258/vasc.2011.oa0342
Školoudík D, Kuliha M, Hrbáč T, Jonszta T, Herzig R. Sonolysis in prevention of brain infarction during carotid Endarterectomy & Stenting (SONOBUSTER): A randomized, controlled trial. European Heart Journal. 2016;37(40):3096-3102. https://doi.org/10.1093/eurheartj/ehv492
Habozit B. The Silent Brain Infarct Before and After Carotid Surgery. Annals of Vascular Surgery. 1990;4(5):485-489. https://doi.org/10.1016/S0890-5096(07)60075-2
Sun X, Lindsay J, Monsein LH, Hill PC, Corso PJ. Silent brain injury after cardiac surgery: A review: Cognitive dysfunction and magnetic resonance imaging diffusion-weighted imaging findings. Journal of the American College of Cardiology. 2012;60(9):791-797. https://doi.org/10.1016/j.jacc.2012.02.079
Naylor R, Rantner B, Ancetti S, de Borst GJ, De Carlo M, Halliday A, Kakkos SK, Markus HS, McCabe DJH, Sillesen H, van den Berg JC, Vega de Ceniga M, Venermo MA, Vermassen FEG, Esvs Guidelines Committee, Antoniou GA, Bastos Goncalves F, Bjorck M, Chakfe N, Coscas R, Dias NV, Dick F, Hinchliffe RJ, Kolh P, Koncar IB, Lindholt JS, Mees BME, Resch TA, Trimarchi S, Tulamo R, Twine CP, Wanhainen A, Document Reviewers, Bellmunt-Montoya S, Bulbulia R, Darling RC 3rd, Eckstein HH, Giannoukas A, Koelemay MJW, Lindström D, Schermerhorn M, Stone DH. Editor’s Choice — European Society for Vascular Surgery (ESVS) 2023 Clinical Practice Guidelines on the Management of Atherosclerotic Carotid and Vertebral Artery Disease. European Journal of Vascular and Endovascular Surgery. 2023;65(1):7-111. https://doi.org/10.1016/j.ejvs.2022.04.011
Hamilton GM, Wheeler K, Di Michele J, Lalu MM, McIsaac DI. A Systematic Review and Meta-analysis Examining the Impact of Incident Postoperative Delirium on Mortality. Anesthesiology. 2017;127(1):78-88. https://doi.org/10.1097/ALN.0000000000001660
AbuRahma AF, Avgerinos ED, Chang RW, Darling RC 3rd, Duncan AA, Forbes TL, Malas MB, Murad MH, Perler BA, Powell RJ, Rockman CB, Zhou W. Society for Vascular Surgery clinical practice guidelines for management of extracranial cerebrovascular disease. Journal of Vascular Surgery. 2022;75(1):4S-22S. https://doi.org/10.1016/j.jvs.2021.04.073