Morphological markers of basic pathogenic variants of ischemic strokes in cerebral atherosclerosis

Cover Page

Cite item

Full Text


Introduction. Pathomorphological studies allow verifying clinical data concerning diagnostic features and predictors of ischemic strokes. Small number and inconsistency of such works have determined the objective of this study: to refine morphological markers of basic pathogenic of ischemic strokes in cerebral atherosclerosis.

Materials and methods. We conducted pathomorphological study of 114 cases of ischemic stroke, as well as histological, ultrastructural and immunohistochemical examinations of 20 carotid atherosclerotic plaques (ASB) removed in carotid endarterectomy.

Results. In most cases, morphological markers of strokes in cerebral atherosclerosis were particular degrees of isolated (≥70%) or tandem (≥50%) atherostenosis, as well as one or more small or medium-size infarctions in the areas of adjacent blood supply or deep regions of the brain hemispheres, cerebellum and brainstem. In occlusive atherothrombosis and arterio-arterial embolism, 98% of strokes were characterized by the development of large or medium cortical-subcortical infarction in certain vascular regions, and the presence of atherothrombotic occlusion or complicated ASB in combination with distal embolic occlusion on the side of an ischemic lesion. High frequency of the occurrence of ASB with unstable structure complicated by thrombosis, and combination of every second major recent infarction caused by thrombosis with silent small organized ischemic foci in the same blood pool as a result of stenosis were established. Significant direct relationship was found between expression of von Willebrand factor and morphological signs of carotid atherosclerosis activity (p<0.017), whereas the degree of expression of other endothelial substances did not correlate with structural changes in ASB.

Conclusions. We showed potentiality for differential diagnosis of various pathogenic variants of strokes associated with atherosclerotic narrowing and complicated pathology of cerebral arteries, as well as the role of silent infarctions, unstable ASB and von Willebrand endothelial factor as predictors of cerebral atherosclerosis complications.

About the authors

Pavel L. Anufriev

Research Center of Neurology

Author for correspondence.
Russian Federation, Moscow

Marine M. Tanashyan

Research Center of Neurology

Russian Federation, Moscow

Tat'yana S. Gulevskaya

Research Center of Neurology

Russian Federation, Moscow

Anna N. Evdokimenko

Research Center of Neurology

Russian Federation, Moscow


  1. Суслина З.А., Гулевская Т.С., Максимова М.Ю., Моргунов В.А. Нарушения мозгового кровообращения: диагностика, лечение, профилактика. М., 2016. 536 с.
  2. Touboul P., Elbaz A., Koller C. et al. GÉNIC Investigators: Common carotid artery intima-media thickness and ischemic stroke subtypes: the GÉNIC case-control study. Circulation 2000; 102: 313–318. doi: 10.1161/01.CIR.102.3.313. PMID: 10899095.
  3. Ay H., Benner T., Arsava E.M. et al. A computerized algorithm for etiologic classification of ischemic stroke: The Causative Classification of Stroke System. Stroke 2007; 38: 2979–2984. doi: 10.1161/STROKEAHA.107.490896. PMID: 17901381.
  4. Amarenco P., Bogousslavsky J., Caplan L.R. et al. The ASCOD Phenotyping of Ischemic Stroke (Updated ASCO Phenotyping). Cerebrovasc Dis 2013; 36: 1–5. doi: 10.1159/000352050. PMID: 23899749.
  5. Gao S., Wang Y.J., Xu A.D. et al. Chinese ischemic stroke subclassification. Front Neurol 2011; 2: 1–5. doi: 10.3389/fneur.2011.00006. PMID: 21427797.
  6. Bogiatzi C., Wannarong T., McLeod A.I. et al. SPARKLE (Subtypes of Ischaemic Stroke Classification System), incorporating measurement of carotid plaque burden: a new validated tool for the classification of ischemic stroke subtypes. Neuroepidemiology 2014; 42: 243–251. doi: 10.1159/000362417. PMID: 24862944.
  7. Adams H.P., Bendixen B.H., Kappelle L.J. et al. Classification of subtype of acute ischemic stroke: definitions for use in a multicenter clinical trial. Stroke 1993; 24: 35–41. doi: 10.1161/01.STR.24.1.35. PMID: 7678184.
  8. Aird W.C. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res 2007; 100 158–173. doi: 10.1161/01.RES.0000255691.76142.4a. PMID: 17272818.
  9. Танашян М.М., Раскуражев А.А., Шабалина А.А. и др. Биомаркеры церебрального атеросклероза: возможности ранней диагностики и прогнозирования индивидуального риска. Анналы клинической и экспериментальной неврологии 2015; 9(3): 20–25.
  10. Гулевская Т.С., Моргунов В.А. Патологическая анатомия нарушений мозгового кровообращения при атеросклерозе и артериальной гипертонии: руководство для врачей. М., 2009. 296 с.
  11. Momjian-Mayor I., Baron J.C. The pathophysiology of watershed infarction in internal carotid artery disease: review of cerebral perfusion studies. Stroke 2005; 36: 567–577. doi: 10.1161/01.STR.0000155727.82242.e1. PMID: 15692123.
  12. Caplan L.R., Wong K.S., Gao S., Hennerici M.G. Is hypoperfusion an important cause of strokes? If so, how? Cerebrovasc Dis 2006; 21: 145–153. doi: 10.1159/000090791. PMID: 16401883.
  13. Vermeer S., Prince N., den Heijer T. et al. Silent brain infarcts and the risk of dementia and cognitive decline. New Engl J Med 2003; 348: 1215–1222. doi: 10.1056/NEJMoa022066. PMID: 12660385.
  14. Adachi T., Kobayashi S., Yamaguchi S. Frequency and pathogenesis of silent subcortical brain infarction in acute first-ever ischemic stroke. Intern Med 2002; 41: 103–108. PMID: 11868595.
  15. Marnane M, Prendeville S, McDonnell C et al. Plaque inflammation and unstable morphology are associated with early stroke recurrence in symptomatic carotid stenosis. Stroke 2014; 45: 801–806. doi: 10.1161/STROKEAHA.113.003657. PMID: 24481971.
  16. Mono M.L., Karameshev A., Slotboom J. et al. Plaque characteristics of asymptomatic carotid stenosis and risk of stroke. Cerebrovasc Dis 2012; 34: 343–350. doi: 10.1159/000343227. PMID: 23154753.
  17. Salem M.K., Sayers R.D., Bown M.J. et al. Patients with recurrent ischaemic events from carotid artery disease have a large lipid core and low GSM. Eur J Vasc Endovasc Surg 2012; 43: 147–153. doi: 10.1016/j.ejvs.2011.11.008. PMID: 22154152.
  18. van Mourik J.A., Boertjes R., Huisveld I.A. et al. von Willebrand factor propeptide in vascular disorders: A tool to distinguish between acute and chronic endothelial cell perturbation. Blood 1999; 94: 179–185. PMID: 10381511.
  19. Blann A.D., McCollum C.N. von Willebrand factor, endothelial cell damage and atherosclerosis. Eur J Vasc Surg 1994; 8: 10–15. PMID: 8307205.
  20. Boffa M.C., Karochkine M., Berard M. Plasma thrombomodulin as a marker of endothelium damage. Nouv Rev Fr Hematol 1991; 33: 529–530. PMID: 1667951.
  21. Seigneur M., Dufourcq P., Conri C. et al. Plasma thrombomodulin – new approach of endothelial damage. Int Angiol 1993; 12: 85–93. PMID: 8207313.
  22. Ignarro L.J., Cirino G., Casini A., Napoli C. Nitric oxide as a signaling molecule in the vascular system: an overview. J Cardiovasc Pharmacol 1999; 34: 879–886. PMID: 10598133.
  23. Suslina ZA, Tanashyan MM, Domashenko MA et al. [Endothelial dysfunction in patients with ischemic stroke]. Annaly klinicheskoy i eksperimental'noy nevrologii. 2008; 2(1): 4-11. (In Russ.).
  24. Whincup PH, Danesh J, Walker M et al. Von Willebrand factor and coronary heart disease. Prospective study and meta-analysis. Eur. Heart J. 2002; 23(22): 1764-1770. PMID: 12419296.

Supplementary files

Supplementary Files

Copyright (c) 2018 Anufriev P.L., Tanashyan M.M., Gulevskaya Т.S., Evdokimenko A.N.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77-83204 от 12.05.2022.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies