Asymptomatic cerebral ischemia after carotid artery stenting as a predictor of cognitive impairment
Published 2025-04-28
Keywords
- Brain Ischemia,
- Carotid Artery Stenting,
- Carotid Stenosis,
- Cognitive Impairment,
- Neurocognitive Tests
How to Cite
Copyright (c) 2025 Osipova O.S., Gostev A.A., Bugurov S.V., Ignatenko P.V., Chernyavskiy A.M.

This work is licensed under a Creative Commons Attribution 4.0 International License.
Abstract
Objective: The study aimed to compare cognitive functions in patients with asymptomatic cerebral ischemic lesions and without cerebral ischemic lesions after carotid artery stenting (CAS).
Methods: A prospective cohort study was based on a subanalysis of 100 patients from the SIBERIA study database who underwent CAS. Patients with a history of stroke or contralateral occlusion of the internal carotid artery, with the development of a vascular event or death during 12 months of follow-up, and individuals with lost contacts were excluded from the analysis. Patients completed the MMSE (Mini-Mental State Examination) test before and after CAS stenting at 6 and 12 months. All three tests were completed by 39 patients with asymptomatic cerebral ischemic lesions and 36 patients without cerebral ischemic lesions on diffusion-weighted magnetic resonance imaging (MRI) of the brain in the early postoperative period after CAS. Pseudo-randomization was performed in a 1:1 ratio using the propensity score matching method, after which 30 patients were included in each group. The primary endpoint was the development of predementia/dementia.
Results: In the group patients with asymptomatic cerebral ischemic lesions, both a significantly lower median score on the MMSE test (26 [25; 28] versus 28 [28; 29], p < 0.001) and a greater number of patients with dementia/predementia (18 (60%) versus 7 (23.3%), p = 0.008) were found compared with the control group in 12 months after CAS. Asymptomatic cerebral ischemic lesions increased the risk of developing predementia/dementia within 12 months after CAS (RR 2.57 [1.07; 6.15], p = 0.02). The total volume of asymptomatic cerebral ischemic lesions ≥ 78 mm3 predicted a decline in cognitive functions.
Conclusion: Asymptomatic cerebral ischemic lesions after CAS significantly increased the risk of developing cognitive impairment during 12 months after procedure.
Received 20 February 2025. Revised 6 March 2025. Accepted 7 March 2025.
Funding
The study did not have sponsorship.
Conflict of interest
The authors declare no conflict of interest.
Contribution of the authors
Conception and study design: O.S. Osipova,
A.A. Gostev, S.V. Bugurov, P.V. Ignatenko, A.M. Chernyavskiy
Data collection and analysis: O.S. Osipova, A.A. Gostev, S.V. Bugurov
Statistical analysis: O.S. Osipova, A.A. Gostev, S.V. Bugurov
Drafting the article: O.S. Osipova, A.A. Gostev
Critical revision of the article: P.V. Ignatenko,
A.M. Chernyavskiy
Final approval of the version to be published: O.S. Osipova, A.A. Gostev, S.V. Bugurov, P.V. Ignatenko, A.M. Chernyavskiy
References
- Eckstein H.-H., Ringleb P., Allenberg J.-R., Berger J., Fraedrich G., Hacke W., Hennerici M., Stingele R., Fiehler J., Zeumer H., Jansen O. Results of the Stent-Protected Angioplasty versus Carotid Endarterectomy (SPACE) study to treat symptomatic stenoses at 2 years: a multinational, prospective, randomised trial. Lancet Neurol. 2008;7(10):893-902. PMID: 18774746. https://doi.org/10.1016/S1474-4422(08)70196-0
- Mas J.-L., Trinquart L., Leys D., Albucher J.-F., Rousseau H., Viguier A., Bossavy J.-P., Denis B., Piquet P., Garnier P., Viader F., Touzé E., Julia P., Giroud M., Krause D., Hosseini H., Becquemin J.-P., Hinzelin G., Houdart E., Hénon H., Neau J.-P., Bracard S., Onnient Y., Padovani R., Chatellier G. Endarterectomy Versus Angioplasty in Patients with Symptomatic Severe Carotid Stenosis (EVA-3S) trial: results up to 4 years from a randomised, multicentre trial. Lancet Neurol. 2008;7(10):885-892. PMID: 18774745. https://doi.org/10.1016/S1474-4422(08)70195-9
- Halliday A., Bulbulia R., Bonati L.H., Chester J., Cradduck-Bamford A., Peto R., Pan H. Second asymptomatic carotid surgery trial (ACST-2): a randomised comparison of carotid artery stenting versus carotid endarterectomy. Lancet. 2021;398(10305):1065-1073. PMID: 34469763; PMCID: PMC8473558. https://doi.org/10.1016/s0140-6736(21)01910-3
- Rosenfield K., Matsumura J.S., Chaturvedi S., Riles T., Ansel G.M., Metzger D.C., Wechsler L., Jaff M.R., Gray W., ACT I Investigators. Randomized trial of stent versus surgery for asymptomatic carotid stenosis. New Engl J Med. 2016;374(11):1011-1020. PMID: 26886419. https://doi.org/10.1056/NEJMoa1515706
- Reiff T., Eckstein H.H., Mansmann U., Jansen O., Fraedrich G., Mudra H., Böckler D., Böhm M., Brückmann H., Debus E.S., Fiehler J., Lang W., Mathias K., Ringelstein E.B., Schmidli J., Stingele R., Zahn R., Zeller T., Hetzel A., Bodechtel U., Binder A., Glahn J., Hacke W., Ringleb P.A. Angioplasty in asymptomatic carotid artery stenosis vs. endarterectomy compared to best medical treatment: one-year interim results of SPACE-2. Int J Stroke. 2019;15(6):638-649. PMID: 30873912; PMCID: PMC7416333. https://doi.org/10.1177/1747493019833017
- Фейгин В.Л., Кришнамурзи Р. Факторы риска и стратегии профилактики инсульта в экономически менее развитых странах. Патология кровообращения и кардиохирургия. 2012;16(3):83-84. https://doi.org/10.21688/1681-3472-2012-3-83-84 Feygin V.L., Krishnamurzi R. Risk factors and strategies for stroke prevention in low to middle-income countries. Patologiya krovoobrashcheniya i kardiokhirurgiya = Circulation Pathology and Cardiac Surgery. 2012;16(3):83-84. (In Russ.) https://doi.org/10.21688/1681-3472-2012-3-83-84
- Bendszus M., Stoll G. Silent cerebral ischaemia: hidden fingerprints of invasive medical procedures. Lancet Neurol. 2006;5(4):364-372. PMID: 16545753. https://doi.org/10.1016/S1474-4422(06)70412-4
- Bonati L.H., Jongen L.M., Haller S., Flach H.Z., Dobson J., Nederkoorn P.J., Macdonald S., Gaines P.A., Waaijer A., Stierli P., Jäger H.R., Lyrer P.A., Kappelle L.J., Wetzel S.G., van der Lugt A., Mali W.P., Brown M.M., van der Worp H.B., Engelter S.T.; 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 Neurol. 2010;9(4):353-362. PMID: 20189458. https://doi.org/10.1016/S1474-4422(10)70057-0
- AbuRahma A.F., Mousa A.Y. Current status of carotid stenting versus endarterectomy. Adv Surg. 2016;50(1):235-256. PMID: 27520875. https://doi.org/10.1016/j.yasu.2016.04.004
- Малаев Д.У., Бойков А.А., Прохорихин А.А., Таркова А.Р., Байструков В.И., Фатуллоева Ш.С., Кретов Е.И. Предикторы эмболических осложнений при каротидном стентировании (TACTILE trial). Патология кровообращения и кардиохирургия. 2020;24(1):28-36. https://doi.org/10.21688/1681-3472-2020-1-28-36 Malaev D.U., Boykov A.A., Prokhorikhin A.A., Tarkova A.R., Baystrukov V.I., Fatulloeva S.S., Kretov E.I. Predictors of embolic complications during carotid stenting (TACTILE trial). Patologiya krovoobrashcheniya i kardiokhirurgiya = Circulation Pathology and Cardiac Surgery. 2020;24(1):28-36. (In Russ.) https://doi.org/10.21688/1681-3472-2020-1-28-36
- Bijuklic K., Wandler A., Tübler T., Schofer J. Impact of asymptomatic cerebral lesions in diffusion-weighted magnetic resonance imaging after carotid artery stenting. JACC Cardiovasc Interv. 2013;6(4):394-398. PMID: 23523451. https://doi.org/10.1016/j.jcin.2012.10.019
- Tatli E., Tokatli A., Vatan M.B., Agac M.T., Gunduz H., Akdemir R., Kilic H. Comparison of closed-cell and hybrid-cell stent designs in carotid artery stenting: clinical and procedural outcomes. Postepy Kardiol Interwencyjnej. 2017;13(2):135-141. PMID: 28798784; PMCID: PMC5545654. https://doi.org/10.5114/pwki.2017.67994
- Gaudet J.G., Meyers P.M., McKinsey J.F., Lavine S.D., Gray W., Mitchell E., Connolly E.S., Heyer E.J. Incidence of moderate to severe cognitive dysfunction in patients treated with carotid artery stenting. Neurosurgery. 2009;65(2):325-329. PMID: 19625912; PMCID: PMC2716040. https://doi.org/10.1227/01.NEU.0000349920.69637.78
- Vermeer S.E., Prins N.D., den Heijer T., Hofman A., Koudstaal P.J., Breteler M.M. Silent brain infarcts and the risk of dementia and cognitive decline. N Engl J Med. 2003;348(13):1215-1222. PMID: 12660385. https://doi.org/10.1056/NEJMoa022066
- Tiemann L., Reidt J.H., Esposito L., Sander D., Theiss W., Poppert H. Neuropsychological sequelae of carotid angioplasty with stent placement: correlation with ischemic lesions in diffusion weighted imaging. PLoS One. 2009;4(9):e7001. PMID: 19746158; PMCID: PMC2734991. https://doi.org/10.1371/journal.pone.0007001
- Grunwald I.Q., Papanagiotou P., Reith W., Backens M., Supprian T., Politi M., Vedder V., Zercher K., Muscalla B., Haass A., Krick C.M. Influence of carotid artery stenting on cognitive function. Neuroradiology. 2010;52(1):61-66. PMID: 20033798. https://doi.org/10.1007/s00234-009-0618-4
- Laza C., Popescu B.O., Popa M., Roceanu A.M., Tiu C., Antochi F.A., Bajenaru O.A. Microemboli detection in patients with carotid artery stenting — a potential marker for future cognitive impairment? J Neurol Sci. 2013;326(1-2):96-99. PMID: 23403326. https://doi.org/10.1016/j.jns.2013.01.025
- Huang K.-L., Ho M.-Y., Chang Y.-J., Chang C.-H., Liu C.-H., Wu H.-C., Chang T.-Y., Lee T.-H. Cognitive sequelae of silent ischemic lesions following carotid artery stenting: possible role of age-related moderation. Front Aging Neurosci. 2022;13:732617. PMID: 35095463; PMCID: PMC8789655. https://doi.org/10.3389/fnagi.2021.732617
- Karpenko A., Bugurov S., Ignatenko P., Starodubtsev V., Popova I., Malinowski K., Musialek P. Randomized controlled trial of conventional versus micronet-covered stent in carotid artery revascularization. JACC Cardiovasc Interv. 2021;14(21):2377-2387. PMID: 34736737. https://doi.org/10.1016/J.JCIN.2021.08.005
- Ruzankin P.S. A fast algorithm for maximal propensity score matching. Methodol Comput Appl Probab. 2020;22:477-495. https://doi.org/10.1007/s11009-019-09718-4
- Skjelland M., Krohg-Sørensen K., Tennøe B., Bakke S.J., Brucher R., Russell D. Cerebral microemboli and brain injury during carotid artery endarterectomy and stenting. Stroke. 2009;40(1):230-234. PMID: 18927460. https://doi.org/10.1161/STROKEAHA.107.513341
- Best L.M.J., Webb A.C., Gurusamy K.S., Cheng S.F., Richards T. Transcranial Doppler ultrasound detection of microemboli as a predictor of cerebral events in patients with symptomatic and asymptomatic carotid disease: a systematic review and meta-analysis. Eur J Vasc Endovasc Surg. 2016;52(2):565-580. PMID: 27397116. https://doi.org/10.1016/j.ejvs.2016.05.019
- AbuRahma A.F. Predictors of perioperative stroke/death after carotid artery stenting: a review article. Ann Vasc Dis. 2018;11(1):15-24. PMID: 29682104; PMCID: PMC5882357. https://doi.org/10.3400/avd.ra.17-00136
- Osipova O.S., Bugurov S.V., Gostev A.A., Saaya S.B., Cheban A.V., Ignatenko P.V., Karpenko A.A. Impact of shaggy aorta on intraoperative cerebral embolism during carotid artery stenting. Int Angiol. 2024;43(2):298-305. PMID: 38801345. https://doi.org/10.23736/S0392-9590.24.05150-2
- Plessers M., Van Herzeele I., Vermassen F., Vingerhoets G. Neurocognitive functioning after carotid revascularization: a systematic review. Cerebrovasc Dis Extra. 2014;4(2):132-148. PMID: 25076958; PMCID: PMC4105952. https://doi.org/10.1159/000362921
- Xia Z.Y., Sun Q.J., Yang H., Zhang M.X., Ban R., Xu G.L., Wu Y.P., Wang L.X., Du Y.F. Effect of carotid artery stenting on cognitive function in patients with internal carotid artery stenosis and cerebral lacunar infarction: a 3-year follow-up study in China. PLoS One. 2015;10(6):e0129917. PMID: 26067432; PMCID: PMC4466228. https://doi.org/10.1371/JOURNAL.PONE.0129917
- Gupta A.N., Bhatti A.A., Shah M.M., Mahajan N.P., Sadana D.K., Huded V. Carotid artery stenting and its impact on cognitive function: a prospective observational study. Neurointervention. 2020;15(2):74-78. PMID: 32268720; PMCID: PMC7412656. https://doi.org/10.5469/neuroint.2020.00038
- Yoon B.A., Sohn S.W., Cheon S.M., Kim D.H., Cha J.K., Yi S.J., Park K.W. Effect of carotid artery stenting on cognitive function in patients with carotid artery stenosis: a prospective, 3-month-follow-up study. J Clin Neurol. 2015;11(2):149-156. PMID: 25851893; PMCID: PMC4387480. https://doi.org/10.3988/JCN.2015.11.2.149
- Gale S.A., Acar D., Daffner K.R. Dementia. Am J Med. 2018;131(10):1161-1169. PMID: 29425707. https://doi.org/10.1016/j.amjmed.2018.01.022
- Heyer E.J., Gold M.I., Kirby E.W., Zurica J., Mitchell E., Halazun H.J., Teverbaugh L., Sciacca R.R., Solomon R.A., Quest D.O., Maldonado T.S., Riles T.S., Connolly E.S. A study of cognitive dysfunction in patients having carotid endarterectomy performed with regional anesthesia. Anesth Analg. 2008;107(2):636-642. PMID: 18633045; PMCID: PMC2606642. https://doi.org/10.1213/ane.0b013e3181770d84
