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Cerebral small vessel disease: classification, clinical manifestations, diagnosis, and features of treatment

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The paper considers the relevance of the problem of cerebral small vessel disease (CSVD) that is an important cause of ischemic and hemorrhagic stroke, associated with the development of cognitive impairment and complications of antithrombotic therapy. It presents briefly the current issues of etiology and pathogenesis of the disease. Sporadic non-amyloid microangiopathy, cerebral amyloid angiopathy, and cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) are discussed in detail from the point of view of their clinical presentation, neuroimaging, and features of therapeutic tactics. An algorithm for diagnosing CSVD in patients admitted to hospital for stroke and a differentiated approach to their treatment are proposed. Consideration of the neuroimaging manifestations of CSVD is noted to be necessary for the safe and more effective treatment of patients with cerebrovascular diseases.

About the Authors

A. A. Kulesh
Acad. E.A. Vagner Perm State Medical University, Ministry of Health of Russia
Russian Federation
26, Petropavlovskaya St., Perm 614990

V. E. Drobakha
Acad. E.A. Vagner Perm State Medical University, Ministry of Health of Russia
Russian Federation
26, Petropavlovskaya St., Perm 614990

V. V. Shestakov
Acad. E.A. Vagner Perm State Medical University, Ministry of Health of Russia
Russian Federation
26, Petropavlovskaya St., Perm 614990


1. Charidimou A, Pantoni L, Love S. The concept of sporadic cerebral small vessel disease: A road map on key definitions and current concepts. Int J Stroke. 2016;11(1):6-18. doi: 10.1177/1747493015607485

2. Pantoni L. Cerebral small vessel disease: from pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010; 9(7):689-701. doi: 10.1016/S1474-4422(10)70104-6

3. Wardlaw JM, Smith C, Dichgans M. Mechanisms of sporadic cerebral small vessel disease: insights from neuroimaging. Lancet Neurol. 2013;12(5):483-97. doi: 10.1016/S1474-4422(13)70060-7

4. Arvanitakis Z, Capuano AW, Leurgans SE, et al. Relation of cerebral vessel disease to Alzheimer's disease dementia and cognitive function in elderly people: a cross-sectional study. Lancet Neurol. 2016;15(9):934-43. doi: 10.1016/S1474-4422(16)30029-1

5. Schwartz RS, Halliday GM, Soh D, et al. Impact of small vessel disease on severity of motor and cognitive impairment in Parkinson's disease. J Clin Neurosci. 2018;58:70-4.

6. Ter Telgte A, van Leijsen EMC, Wiegertjes K, et al. Cerebral small vessel disease: from a focal to a global perspective. Nat Rev Neurol. 2018; 14(7):387-98. doi: 10.1038/s41582-018-0014-y

7. Parfenov VA. Diagnosis and treatment of chronic cerebrovascular disease. Nevrologiya, Neiropsikhiatriya, Psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2016;8(3):4-9 (In Russ.). doi: 10.14412/2074-2711-2016-3-4-9

8. Kulesh AA, Drobakha VE, Shestakov VV. Hemorrhagic manifestations of cerebral amyloid angiopathy: from pathogenesis to clinical significance. Nevrologiya, Neiropsikhiatriya, Psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2018;10(3):4-11 (In Russ.). doi: 10.14412/2074-2711-2018-3-4-11

9. Kulesh AA, Shestakov VV. Vascular cognitive impairment, no dementia: diagnosis, prognosis, treatment, and prevention. Nevrologiya, Neiropsikhiatriya, Psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2017;9(3):68-75 (In Russ.). doi: 10.14412/2074-2711-2017-3-68-75

10. Kulesh AA, Drobakha VE, Shestakov VV. Sporadic cerebral non-amyloid microangiopathy: pathogenesis, diagnosis, and features of treatment policy. Nevrologiya, Neiropsikhiatriya, Psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2018;10(4): 13-22 (In Russ.). doi: 10.14412/2074-2711-2018-4-13-22

11. Wardlaw JM, Smith EE, Biessels GJ, et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013; 12:822-38. doi: 10.1016/S1474-4422(13)70124-8

12. Lau KK, Li L, Simoni M, et al. Long-term premorbid blood pressure and cerebral small vessel disease burden on imaging in transient ischemic attack and ischemic stroke. Stroke. 2018;49(9):2053-60. doi: 10.1161/STROKEAHA.118.021578

13. Liu B, Lau KK, Li L, et al. Age-Specific Associations of Renal Impairment With Magnetic Resonance Imaging Markers of Cerebral Small Vessel Disease in Transient Ischemic Attack and Stroke. Oxford Vasc Study Stroke. 2018;49(4):899-904. doi: 10.1161/STROKEAHA.117.019650

14. Makin SDJ, Mubki GF, Doubal FN, et al. Small Vessel Disease and Dietary Salt Intake: Cross-Sectional Study and Systematic Review. J Stroke Cerebrovasc Dis. 2017;26(12):3020-8. doi: 10.1016/j.jstrokecerebrovasdis.2017.08.004

15. Umemura T, Kawamura T, Hotta N. Pathogenesis and neuroimaging of cerebral large and small vessel disease in type 2 diabetes: A possible link between cerebral and retinal microvascular abnormalities. J Diabetes Investig. 2017;8(2):134-48. doi: 10.1111/jdi.12545

16. Tsai YH, Lee M Lin LC, et al. Association of Chronic Kidney Disease With Small Vessel Disease in Patients With Hypertensive Intracerebral Hemorrhage. Front Neurol. 2018;2(9):284. doi: 10.3389/fneur.2018.00284

17. Rannikmä e K, Sivakumaran V, Millar H, et al. Stroke Genetics Network (SiGN), METASTROKE Collaboration, and International Stroke Genetics Consortium (ISGC). COL4A2 is associated with lacunar ischemic stroke and deep ICH: meta-analyses among 21,500 cases and 40,600 controls. Neurology. 2017;89:1829-39. doi: 10.1212/WNL.0000000000004560

18. Traylor M, Malik R, Nalls MA, et al. METASTROKE, UK Young Lacunar DNA Study, NINDS Stroke Genetics Network, Neurology Working Group of the CHARGE Consortium; International Stroke Genetics Consortium. Genetic variation at 16q24.2 is associated with small vessel stroke. Ann Neurol. 2017;81:383-94. doi: 10.1002/ana.24840

19. Di Donato I, Bianchi S, Gallus GN, et al. Heterozygous mutations of HTRA1 gene in patients with familial cerebral small vessel disease. CNS Neurosci Ther. 2017;23:759-65. doi: 10.1111/cns.12722

20. Lee YL, Hu HY, Huang N, et al. Dental prophylaxis and periodontal treatment are protective factors to ischemic stroke. Stroke. 2013; 44:1026-30. doi: 10.1161/STROKEAHA.111.000076

21. Miyatani F, Kuriyama N, Watanabe I, et al. Relationship between Cnm-positive Streptococcus mutans and cerebral microbleeds in humans. Oral Dis. 2015;21:886-93. doi: 10.1111/odi.12360

22. Ihara M, Yamamoto Y. Emerging Evidence for Pathogenesis of Sporadic Cerebral Small Vessel Disease. Stroke. 2016;47(2):554-60. doi: 10.1161/STROKEAHA.115.009627

23. Lawrence AJ, Chung AW, Morris RG, et al. Structural network efficiency is associated with cognitive impairment in small-vessel disease. Neurology. 2014;83:304-11. doi: 10.1212/WNL.0000000000000612

24. Rasmussen MK, Mestre H, Nedergaard M. The glymphatic pathway in neurological disorders. Lancet Neurol. 2018;17(11):1016-24. doi: 10.1016/S1474-4422(18)30318-1

25. Brown R, Benveniste H, Black SE, et al. Understanding the role of the perivascular space in cerebral small vessel disease. Cardiovasc Res. 2018;114(11):1462-73. doi: 10.1093/cvr/cvy113

26. Petrone L, Nannoni S, Del Bene A, et al. Branch Atheromatous Disease: A Clinically Meaningful, Yet Unproven Concept. Cerebrovasc Dis. 2016;41(1-2):87-95. doi: 10.1159/000442577

27. Duering M, Csanadi E, Gesierich B, et al. Incident lacunes preferentially localize to the edge of white matter hyperintensities: insights into the pathophysiology of cerebral small vessel disease. Brain. 2013;136:2717-26. doi: 10.1093/brain/awt184

28. Potter G, Doubal F, Jackson C, et al. Associations of clinical stroke misclassification ('clinical-imaging dissociation') in acute ischemic stroke. Cerebrovasc Dis. 2010;29:395- 402. doi: 10.1159/000286342

29. Auriel E, Westover MB, Bianchi MT, et al. Estimating total cerebral microinfarct burden from diffusion-weighted imaging. Stroke. 2015; 46:2129-35. doi: 10.1161/STROKEAHA.115. 009208

30. Van Veluw SJ, Shih AY, Smith EE, et al. Detection, risk factors, and functional consequences of cerebral microinfarcts. Lancet Neurol. 2017;16(9):730-40. doi: 10.1016/S1474-4422(17)30196-5

31. Summers PM, Hartmann DA, Hui ES, et al. Functional deficits induced by cortical microinfarcts. J Cereb Blood Flow Metab. 2017;37(11): 3599-614. doi: 10.1177/0271678X16685573

32. Van Veluw SJ, Hilal S, Kuijf HJ, et al. Cortical microinfarcts on 3T MRI: clinical correlates in memory-clinic patients. Alzheimers Dement. 2015;11:1500-9. doi: 10.1016/j.jalz. 2014.12.010

33. Yates PA, Villemagne VL, Ellis KA, et al. Cerebral microbleeds: a review of clinical, genetic, and neuroimaging associations. Send to Front Neurol. 2014;6(4):205. doi: 10.3389/fneur.2013.00205

34. Wilson D, Werring DJ. Antithrombotic therapy in patients with cerebral microbleeds. Curr Opin Neurol. 2017;30(1):38-47. doi: 10.1097/WCO.0000000000000411

35. Wilson D, Charidimou A, Ambler G, et al. Recurrent stroke risk and cerebral microbleed burden in ischemic stroke and TIA: A metaanalysis. Neurology. 2016;87(14):1501-10. doi: 10.1212/WNL.0000000000003183

36. Charidimou A, Shoamanesh A. Clinical relevance of microbleeds in acute stroke thrombolysis: Comprehensive meta-analysis. International META-MICROBLEEDS Initiative. Neurology. 2016;87(15):1534-41. doi: 10.1212/WNL.0000000000003207

37. Rosenberg GA. Binswanger's disease: biomarkers in the inflammatory form of vascular cognitive impairment and dementia. J Neurochem. 2018;144(5):634-43. doi: 10.1111/jnc.14218

38. Attems J, Lauda F, Jellinger KA. Unexpectedly low prevalence of intracerebral hemorrhages in sporadic cerebral amyloid angiopathy: an autopsy study. J Neurol. 2008; 255:70-6. doi: 10.1007/s00415-008-0674-4

39. Attems J, Jellinger K, Thal DR, van Nostrand W. Review: Sporadic cerebral amyloid angiopathy. Neuropathol Appl Neurobiol. 2011;37:75-93. doi: 10.1111/j.1365-2990.2010.01137.x

40. Carare RO, Kalaria R. Cerebrovascular pathology: the dark side of neurodegeneration. Acta Neuropathol. 2016;131:641-3. doi: 10.1007/s00401-016-1573-x

41. Charidimou A, Boulouis G, Gurol ME, et al. Emerging concepts in sporadic cerebral amyloid angiopathy. Brain. 2017;140(7): 1829-50. doi: 10.1093/brain/awx047

42. Charidimou A, Linn J, Vernooij MW, et al. Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain. 2015; 138(8):2126-39. doi: 10.1093/brain/awv162

43. Greenberg SM, Salman RA, Biessels GJ, et al. Outcome markers for clinical trials in cerebral amyloid angiopathy. Lancet Neurol. 2014;13:419-28. doi: 10.1016/S1474-4422(14) 70003-1

44. Arvanitakis Z, Leurgans SE, Wang Z, et al. Cerebral amyloid angiopathy pathology and cognitive domains in older persons. Ann Neurol. 2011;69:320-7. doi: 10.1002/ana.22112

45. Case NF, Charlton A, Zwiers A, et al. Cerebral amyloid angiopathy is associated with executive dysfunction and mild cognitive impairment. Stroke. 2016;47:2010-6. doi: 10.1161/STROKEAHA.116.012999

46. Parfenov VA, Zakharov VV, Preobrazhenskaya IS. Kognitivnye rasstroistva [Cognitive disorders]. Moscow: Remedium Group LLC; 2015. 187 p. (In Russ.).

47. Greenberg SM, Charidimou A. Diagnosis of Cerebral Amyloid Angiopathy: Evolution of the Boston Criteria. Stroke. 2018;49(2):491-7. doi: 10.1161/STROKEAHA.117.016990

48. Charidimou A, Martinez-Ramirez S, Shoamanesh A, et al. Cerebral amyloid angiopathy with and without hemorrhage: evidence for different disease phenotypes. Neurology. 2015;84:1206-12. doi: 10.1212/WNL.0000000000001398

49. Lin CM, Arishima H, Kikuta KI, et al. Pathological examination of cerebral amyloid angiopathy in patients who underwent removal of lobar hemorrhages. J Neurol. 2018;265(3): 567-77. doi: 10.1007/s00415-018-8740-z

50. Roh D, Sun CH, Schmidt JM, et al. Primary Intracerebral Hemorrhage: A Closer Look at Hypertension and Cerebral Amyloid Angiopathy. Neurocrit Care. 2018. doi: 10.1007/s12028-018-0514-z

51. Guidoux C, Hauw JJ, Klein IF, et al. Amyloid Angiopathy in Brain Hemorrhage: A Postmortem Neuropathological Magnetic Resonance Imaging Study. Cerebrovasc Dis. 2018;45(3-4):124-31. doi: 10.1159/000486554

52. Biffi A, Halpin A, Towfighi A, et al. Aspirin and recurrent intracerebral hemorrhage in cerebra amyloid angiopathy. Neurology. 2010;75: 693-8. doi: 10.1212/WNL.0b013e3181eee40f

53. Haley KE, Greenberg SM, Gurol ME. Cerebral microbleeds and macrobleeds: should they influence our recommendations for antithrombotic therapies? Curr Cardiol Rep. 2013;15:425. doi: 10.1007/s11886-013-0425-8

54. Rodrigues MA, Samarasekera N, Lerpiniere C, et al. The Edinburgh CT and genetic diagnostic criteria for lobar intracerebral haemorrhage associated with cerebral amyloid angiopathy: model development and diagnostic test accuracy study. Lancet Neurol. 2018;17(3): 232-40. doi: 10.1016/S1474-4422(18)30006-1

55. Kumar S, Goddeau RP, Selim MH, et al. Atraumatic convexal subarachnoid hemorrhage: clinical presentation, imaging patterns, and etiologies. Neurology. 2010;74:893-9. doi: 10.1212/WNL.0b013e3181d55efa

56. Tsai HH, Kim JS, Jouvent E, Gurol ME. Updates on Prevention of Hemorrhagic and Lacunar Strokes. J Stroke. 2018;20(2):167-79. doi: 10.5853/jos.2018.00787

57. Linn J, Herms J, Dichgans M, et al. Subarachnoid hemosiderosis and superficial cortical hemosiderosis in cerebral amyloid angiopathy. Am J Neuroradiol. 2008;29:184-6. doi: 10.3174/ajnr.A0783

58. Vernooij MW, Ikram MA, Hofman A, et al. Superficial siderosis in the general population. Neurology. 2009;73:202-5. doi: 10.1212/WNL.0b013e3181ae7c5e

59. Charidimou A, Peeters AP, Jager R, et al. Cortical superficial siderosis and intracerebral hemorrhage risk in cerebral amyloid angiopathy. Neurology. 2013;81:1666-73. doi: 10.1212/01.wnl.0000435298.80023.7a

60. Xiong L, van Veluw SJ, Bounemia N, et al. Cerebral cortical microinfarcts on magnetic resonance imaging and their association with cognition in cerebral amyloid angiopathy. Stroke. 2018;49(10):2330-6. doi: 10.1161/STROKEAHA.118.022280

61. Corovic A, Kelly S, Markus HS. Cerebral amyloid angiopathy associated with inflammation: A systematic review of clinical and imaging features and outcome. Int J Stroke. 2018; 13(3):257-67. doi: 10.1177/1747493017741569

62. Auriel E, Charidimou A, Gurol ME, et al. Validation of Clinicoradiological Criteria for the Diagnosis of Cerebral Amyloid AngiopathyRelated Inflammation. JAMA Neurol. 2016; 73(2):197-202. doi: 10.1001/jamaneurol.2015. 4078

63. Joutel A, Corpechot C, Ducros A, et al. Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature. 1996;383:707-10. doi: 10.1038/383707a0

64. Dong Y, Hassan A, Zhang Z, et al. Yield of screening for CADASIL mutations in lacunar stroke and leukoaraiosis. Stroke. 2003;34:203-5. doi: 10.1161/01.STR.0000048162.16852.88

65. Yamamoto Y, Craggs L, Baumann M, et al. Review: molecular genetics and pathology of hereditary small vessel diseases of the brain. Neuropathol Appl Neurobiol. 2011;37:94-113. doi: 10.1111/j.1365-2990.2010.01147.x

66. Chabriat H, Joutel A, Dichgans M, et al. Cadasil. Lancet Neurol. 2009;8(7):643-53. doi: 10.1016/S1474-4422(09)70127-9

67. Singhal S, Bevan S, Barrick T, et al. The influence of genetic and cardiovascular risk factors on the CADASIL phenotype. Brain. 2004; 127(Pt 9):2031-8. doi: 10.1093/brain/awh223

68. Chabriat H, Herve D, Duering M, et al. Predictors of clinical worsening in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy: prospective cohort study. Stroke. 2016;47(1):4-11. doi: 10.1161/STROKEAHA.115.010696

69. Chabriat H, Levy C, Taillia H, et al. Patterns of MRI lesions in CADASIL. Neurology. 1998; 51:452-7. doi: 10.1212/WNL.51.2.452

70. Di Donato I, Bianchi S, De Stefano N, et al. Cerebral Autosomal Dominant Arteriopathy with Subcortical Infarcts and Leukoencephalopathy (CADASIL) as a model of small vessel disease: update on clinical, diagnostic, and management aspects. BMC Med. 2017;15(1):41. doi: 10.1186/s12916-017-0778-8

71. Auer DP, Pü tz B, Gö ssl C, et al. Differential lesion patterns in CADASIL and sporadic subcortical arteriosclerotic encephalopathy: MR imaging study with statistical parametrical group comparison. Radiology. 2001;218(2):443-51. doi: 10.1148/radiology.218.2.r01fe24443

72. O'Sullivan M, Jarosz JM, Martin RJ, et al. MRI hyperintensities of the temporal lobe and external capsule in patients with CADASIL. Neurology. 2001;56(5):628-34. doi: 10.1212/ WNL.56.5.628

73. Singhal S, Rich P, Markus HS. The spatial distribution of MR imaging abnormalities in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy and their relationship to age and clinical features. AJNR Am J Neuroradiol. 2005;26(10): 2481-7.

74. Duchesnay E, Hadj Selem F, De Guio F, et al. Different types of white matter hyperintensities in CADASIL. Front Neurol. 2018;9:526. doi: 10.3389/fneur.2018.00526

75. Lee JS, Ko K, Oh JH, et al. Cerebral microbleeds, hypertension, and intracerebral hemorrhage in cerebral autosomal-dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Front Neurol. 2017;8:203. doi: 10.3389/fneur.2017.00203

76. Wollenweber FA, Baykara E, Zedde M, et al. Cortical superficial siderosis in different types of cerebral small vessel disease. Stroke. 2017;48(5):1404-7. doi: 10.1161/STROKEAHA.117.016833

77. Tikka S, Baumann M, Siitonen M, et al. CADASIL and CARASIL. Brain Pathol. 2014;24(5):525-44. doi: 10.1111/bpa.12181

78. Sondergaard CB, Nielsen JE, Hansen CK, Christensen H. Hereditary cerebral small vessel disease and stroke. Review. Clin Neurol Neurosurg. 2017;155:45-57. doi: 10.1016/j.clineuro.2017.02.015

79. Tan RY, Markus H. CADASIL: migraine, encephalopathy, stroke and their inter-relationships. PLoS One. 2016;11(6):e0157613. doi: 10.1371/journal.pone.0157613

80. Eikermann-Haerter K, Yuzawa I, Dilekoz E, et al. Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy syndrome mutations increase susceptibility to spreading depression. Ann Neurol. 2011;69(2):413-8. doi: 10.1002/ana.22281

81. Adib-Samii P, Brice G, Martin RJ, Markus HS. Clinical spectrum of CADASIL and the effect of cardiovascular risk factors on phenotype: study in 200 consecutively recruited individuals. Stroke. 2010;41(4):630-4. doi: 10.1161/STROKEAHA.109.568402

82. Peters N, Opherk C, Danek A, et al. The pattern of cognitive performance in CADASIL: a monogenic condition leading to subcortical ischemic vascular dementia. Am J Psychiatry. 2005;162(11):2078-85. doi: 10.1176/appi.ajp.162.11.2078

83. Valenti R, Poggesi A, Pescini F, et al. Psychiatric disturbancesin CADASIL: a brief review. Acta Neurol Scand. 2008;118(5):291-5. doi: 10.1111/j.1600-0404.2008.01015.x

84. Yao M, Herve D, Jouvent E, et al. Dilated perivascular spaces in small-vessel disease: a study in CADASIL. Cerebrovasc Dis. 2014; 37(3):155-63. doi: 10.1159/000356982

85. Parfenov VA, Neverovsky DV. Outpatient management of patients with dyscirculatory encephalopathy. Nevrologiya, Neiropsikhiatriya, Psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2015;7(1): 37-42 (In Russ.). doi: 10.14412/2074-2711-2015-1-37-42

86. Konialis C, Hagnefelt B, Kokkali G, et al. Pregnancy following preimplantation genetic diagnosis of cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL). Prenat Diagn. 2007; 27(11):1079-83. doi: 10.1002/pd.1837

87. Powers WJ, Rabinstein AA, Ackerson T, et al. 2018 Guidelines for the early management of patients with acute ischemic stroke. A guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2018;49(3):e46-e138. doi: 10.1161/STR.0000000000000158

88. Kirshner HS, Bradshaw M. The Inflammatory Form of Cerebral Amyloid Angiopathy or BCerebral Amyloid AngiopathyRelated Inflammation (CAARI). Curr Neurol Neurosci Rep. 2015;15(8):54. doi: 10.1007/s11910-015-0572-y

89. Ostroumova TM, Parfenov VA, Ostroumova OD. Hypertension and cognitive impairment: the standpoint of evidence-based medicine. Nevrologiya, Neiropsikhiatriya, Psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2017;9(4):70-6 (In Russ.). doi: 10.14412/2074-2711-2017-4-70-76

90. Parfenov VA, Ostroumova TM, Ostroumova OD, et al. Diffusion tensor magnetic resonance imaging in the diagnosis of white matter lesion in middle-aged patients with uncomplicated essential hypertension. Nevrologiya, Neiropsikhiatriya, Psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2018;10(2): 20-6 (In Russ.). doi: 10.14412/2074-2711-2018-2-20-26

91. Ostroumova TM, Parfenov VA, Ostroumova OD, et al. Possibilities of contrast-free magnetic resonance perfusion imaging for the detection of early brain damage in essential hypertension. Nevrologiya, Neiropsikhiatriya, Psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2018;10(1):17-23 (In Russ.). doi: 10.14412/2074-2711-2018-1-17-23

92. Kernan WN, Ovbiagele B, Black HR, et al. American Heart Association Stroke Council, Council on Cardiovascular and Stroke Nursing, Council on Clinical Cardiology, and Council on Peripheral Vascular Disease. Guidelines for the prevention of stroke in patients with stroke and transient ischemic attack: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2014;45(7):2160-236. doi: 10.1161/STR.0000000000000024

93. Van Middelaar T, Argillander TE, Schreuder FHBM, et al. Effect of antihypertensive medication on cerebral small vessel disease: A systematic review and meta-analysis. Stroke. 2018;49(6):1531-3. doi: 10.1161/STROKEAHA.118.021160

94. Croall ID, Tozer DJ, Moynihan B, et al. Effect of standard vs intensive blood pressure control on cerebral blood flow in small vessel disease: The PRESERVE randomized clinical trial. JAMA Neurol. 2018;75(6):720-7. doi: 10.1001/jamaneurol.2017.5153

95. Arima H, Tzourio C, Anderson C, et al. Effects of perindopril-based lowering of blood pressure on intracerebral hemorrhage related to amyloid angiopathy: the PROGRESS trial. Stroke. 2010;41:394-6. doi: 10.1161/STROKEAHA.109.563932

96. Biffi A, Anderson CD, Battey TW, et al. Association between blood pressure control and risk of recurrent intracerebral hemorrhage. JAMA. 2015;314:904-12. doi: 10.1001/jama.2015.10082

97. Parfenov VA, Starchina YuA. Cognitive disorders and their treatment of arterial hypertension. Nervnye Bolezni. 2015;(1): 16-22 (In Russ.).

98. Benavente OR, Hart RG, McClure LA, et al; SPS Investigators. Effects of clopidogrel added to aspirin in patients with recent lacunar stroke. N Engl J Med. 2012;367(9):817-25. doi: 10.1056/NEJMoa1204133

99. Johnston SC, Easton JD, Farrant M, et al. Clinical research collaboration, neurological emergencies treatment trials network, and the POINT investigators. Clopidogrel and aspirin in acute ischemic stroke and high-risk TIA. N Engl J Med. 2018;379(3):215-25. doi: 10.1056/ NEJMoa1800410

100. Jing J, Meng X, Zhao X, et al. Dual antiplatelet therapy in transient ischemic attack and minor stroke with different infarction patterns: subgroup analysis of the CHANCE randomized clinical trial. JAMA Neurol. 2018; 75(6):711-9. doi: 10.1001/jamaneurol.2018.0247

101. Qiu J, Ye H, Wang J, et al. Antiplatelet therapy, cerebral microbleeds, and intracerebral hemorrhage: A meta analysis. Stroke. 2018;49(7): 1751-4. doi: 10.1161/STROKEAHA.118.021789

102. Bath PM, Wardlaw JM. Pharmacological treatment and prevention of cerebral small vessel disease: a review of potential interventions. Int J Stroke. 2015;10(4):469-78. doi: 10.1111/ijs.12466

103. Kim BJ, Lee EJ, Kwon SU, et al. Prevention of cardiovascular events in Asian patients with ischaemic stroke at high risk of cerebral haemorrhage (PICASSO): A multicentre, randomised controlled trial. Lancet Neurol. 2018;17:509-18. doi: 10.1016/S1474-4422(18) 30128-5

104. DeSimone CV, Graff-Radford J, El-Harasis MA, et al. Cerebral Amyloid Angiopathy: Diagnosis, Clinical Implications, and Management Strategies in Atrial Fibrillation. J Am Coll Cardiol. 2017;70(9): 1173-82. doi: 10.1016/j.jacc.2017.07.724

105. Rosand J, Hylek EM, O'Donnell HC, Greenberg SM. Warfarin-associated hemorrhage and cerebral amyloid angiopathy: a genetic and pathologic study. Neurology. 2000;55:947-51. doi: 10.1212/WNL.55.7.947

106. Banerjee G, Carare R, Cordonnier C, et al. The increasing impact of cerebral amyloid angiopathy: essential new insights for clinical practice. J Neurol Neurosurg Psychiatry. 2017; 88(11):982-94. doi: 10.1136/jnnp-2016-314697

107. Steiner T, Köhrmann M, Schellinger PD, Tsivgoulis G. Non-vitamin K oral anticoagulants associated bleeding and its antidotes. J Stroke. 2018;20(3):292-301. doi: 10.5853/jos.2018.02250

108. O'Donnell MJ, Eikelboom JW, Yusuf S, et al. Effect of apixaban on brain infarction and microbleeds: averroes-MRi assessment study. Am Heart J. 2016;178:145-50. doi: 10.1016/j.ahj.2016.03.019

109. Holmes DR Jr, Lakkireddy DR, Whitlock RP, et al. Left atrial appendage occlusion: opportunities and challenges. J Am Coll Cardiol. 2014;63:291-8. doi: 10.1016/j.jacc. 2013.08.1631

110. Cannistraro RJ, Meschia JF. The Clinical Dilemma of Anticoagulation Use in Patients with Cerebral Amyloid Angiopathy and Atrial Fibrillation. Curr Cardiol Rep. 2018;20(11):106. doi: 10.1161/STROKEAHA.108.534107

111. Amarenco P, Benavente O, Goldstein LB, et al. Results of the stroke prevention by aggressive reduction in cholesterol levels (SPARCL) trial by stroke subtypes. Stroke. 2009;40:1405-9. doi: 10.1161/STROKEAHA.108.534107

112. Goldstein LB, Amarenco P, Szarek M, et al. Hemorrhagic stroke in the stroke prevention by aggressive reduction in cholesterol levels study. Neurology. 2008;70(24 Pt 2):2364-70. doi: 10.1212/01.wnl.0000296277.63350.77

113. Di Vergouwen M, de Haan RJ, Vermeulen M, et al. Statin treatment and the occurrence of hemorrhagic stroke in patients with a history of cerebrovascular disease. Stroke. 2008;39:497-502. doi: 10.1161/STROKEAHA. 107.488791

114. Pezzini A, Grassi M, Iacoviello L, et al. Multicenter Study on Cerebral Haemorrhage in Italy (MUCH-italy) investigators. Serum cholesterol levels, HMG-CoA reductase inhibitors and the risk of intracerebral haemorrhage. The Multicenter Study on cerebral haemorrhage in Italy (MUCH-italy). J Neurol Neurosurg Psychiatry. 2016;87:924-9. doi: 10.1136/jnnp-2015-312736

115. Westover MB, Bianchi MT, Eckman MH, et al. Statin use following intracerebral hemorrhage: a decision analysis. Arch Neurol. 2011; 68:573-9. doi: 10.1001/archneurol.2010.356

116. Ji T, Zhao Y, Wang J, et al. Effect of lowdose statins and apolipoprotein E genotype on cerebral small vessel disease in older hypertensive patients: A subgroup analysis of a randomized clinical trial. J Am Med Dir Assoc. 2018. pii: S1525-8610(18)30297-4


For citations:

Kulesh A.A., Drobakha V.E., Shestakov V.V. Cerebral small vessel disease: classification, clinical manifestations, diagnosis, and features of treatment. Neurology, Neuropsychiatry, Psychosomatics. 2019;11(3S):4-17. (In Russ.)

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