Preview

Neurology, Neuropsychiatry, Psychosomatics

Advanced search

Hemorrhagic manifestations of cerebral amyloid angiopathy: from pathogenesis to clinical significance

https://doi.org/10.14412/2074-2711-2018-3-4-11

Full Text:

Abstract

The paper characterizes the neuropathological aspects of cerebral amyloid angiopathy (CAA) and its pathogenesis. It presents in detail the current neuroimaging markers of CAA and their neuropathological correlates. The phenotypic heterogeneity of the disease and its main clinical manifestations are considered; the updated Boston diagnostic criteria are formulated. The issues of intracerebral hemorrhages, cerebral microbleeding, and cortical superficial siderosis, which are associated with CAA, are elucidated in detail. CAA is noted to be of clinical significance for the determination of therapeutic policy in hemorrhagic stroke, systemic thrombolytic therapy, and cognitive impairment.

About the Authors

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


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


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


References

1. Charidimou A, Boulouis G, Gurol ME, et al. Emerging concepts in sporadic cerebral amyloid angiopathy. Brain. 2017 Jul 1;140(7):1829-1850. doi: 10.1093/brain/awx047.

2. Attems J, Lauda F, Jellinger KA.Unexpectedly low prevalence of intracerebral hemorrhages in sporadic cerebral amyloid angiopathy: an autopsy study. J Neurol. 2008 Jan;255(1):70-6. doi: 10.1007/s00415-008-0674-4. Epub 2008 Jan 18.

3. Keage HA, Carare RO, Friedland RP, et al. Population studies of sporadic cerebral amyloid angiopathy and dementia: a systematic review. BMC Neurol. 2009 Jan 13;9:3. doi: 10.1186/ 1471-2377-9-3.

4. Jellinger KA. Alzheimer disease and cerebrovascular pathology: an update. J Neural Transm (Vienna). 2002 May;109(5-6):813-36.

5. Attems J, Jellinger K, Thal DR, Van Nostrand W. Review: Sporadic cerebral amyloid angiopathy. Neuropathol Appl Neurobiol. 2011 Feb;37(1):75-93. doi: 10.1111/j.1365-2990.2010.01137.x.

6. Carare RO, Hawkes CA, Jeffrey M, et al. Review: cerebral amyloid angiopathy, prion angiopathy, CADASIL and the spectrum of protein elimination failure angiopathies (PEFA) in neurodegenerative disease with a focus on therapy. Neuropathol Appl Neurobiol. 2013 Oct;39(6):593-611. doi: 10.1111/nan.12042.

7. Carare RO, Kalaria R. Cerebrovascular pathology: the dark side of neurodegeneration. Acta Neuropathol. 2016 May;131(5):641-3. doi: 10.1007/s00401-016-1573-x.

8. Greenberg SM, Salman RA, Biessels GJ, et al. Outcome markers for clinical trials in cerebral amyloid angiopathy. Lancet Neurol. 2014 Apr;13(4):419-28. doi: 10.1016/S1474-4422(14)70003-1. Epub 2014 Feb 27.

9. 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 Aug; 12(8):822-38. doi: 10.1016/S1474-4422(13) 70124-8.

10. Baron JC, Farid K, Dolan E, et al. Diagnostic utility of amyloid PET in cerebral amyloid angiopathyrelated symptomatic intracerebral hemorrhage. J Cereb Blood Flow Metab. 2014 May;34(5):753-8. doi: 10.1038/jcbfm. 2014.43. Epub 2014 Mar 12.

11. van Veluw SJ, Biessels GJ, Bouvy WH, et al. Cerebral amyloid angiopathy severity is linked to dilation of juxtacortical perivascular spaces. J Cereb Blood Flow Metab. 2016 Mar;36(3): 576-80. doi: 10.1177/0271678X15620434. Epub 2015 Dec 7.

12. Charidimou A, Martinez-Ramirez S, Reijmer YD, et al. Total Magnetic Resonance Imaging Burden of Small Vessel Disease in Cerebral Amyloid Angiopathy: An Imaging-Pathologic Study of Concept Validation. JAMA Neurol. 2016 Aug 1;73(8):994-1001. doi: 10.1001/jamaneurol.2016.0832.

13. Keable A, Fenna K, Yuen HM, et al. Deposition of amyloid beta in the walls of human leptomeningeal arteries in relation to perivascular drainage pathways in cerebral amyloid angiopathy. Biochim Biophys Acta. 2016 May; 1862(5):1037-46. doi: 10.1016/j.bbadis.2015.08.024. Epub 2015 Aug 29.

14. Charidimou A, Linn J, Vernooij MW, et al. Cortical superficial siderosis: detection and clinical significance in cerebral amyloid angiopathy and related conditions. Brain. 2015 Aug;138(Pt 8):2126-39. doi: 10.1093/brain/ awv162. Epub 2015 Jun 26.

15. Arvanitakis Z, Leurgans SE, Wang Z, et al. Cerebral amyloid angiopathy pathology and cognitive domains in older persons. Ann Neurol. 2011 Feb;69(2):320-7. doi: 10.1002/ana.22112. Epub 2010 Nov 8.

16. Boyle PA, Yu L, Nag S, et al. Cerebral amyloid angiopathy and cognitive outcomes in communitybased older persons. Neurology. 2015 Dec 1;85(22):1930-6. doi: 10.1212/WNL. 0000000000002175. Epub 2015 Nov 4.

17. Кулеш АА, Кайлева НА, Горст НХ, Шестаков ВВ. Связь между интегральной оценкой магнитно-резонансных маркеров церебральной болезни мелких сосудов, клиническим и функциональным статусом в остром периоде ишемического инсульта. Неврология, нейропсихиатрия, психосоматика. 2018;10(1):24-31. [Kulesh AA, Kaileva NA, Gorst NKh, Shestakov VV. A relationship between the integrated assessment of magnetic resonance imaging markers for cerebral small vessel disease and the clinical and functional status in the acute period of ischemic stroke. Nevrologiya, neiropsikhiatriya, psikhosomatika = Neurology, Neuropsychiatry, Psychosomatics. 2018;10(1):24-31. (In Russ.)]. doi: 10.14412/ 2074-2711-2018-1-24-31

18. Кулеш АА, Дробаха ВЕ, Куклина ЕМ, Шестаков ВВ. Амилоид-бета 40 как биомаркер когнитивных нарушений в остром периоде ишемического инсульта. Бюллетень сибирской медицины. 2017;16(3):79-86. [Kulesh AA, Drobakha VE, Kuklina EM, Shestakov VV. Amyloid-beta 40 as a biomarker of cognitive impairment in acute ischemic stroke. Byulleten' sibirskoi meditsiny. 2017;16(3): 79-86. (In Russ.)].

19. Case NF, Charlton A, Zwiers A, et al. Cerebral amyloid angiopathy is associated with executive dysfunction and mild cognitive impairment. Stroke. 2016 Aug;47(8):2010-6. doi: 10.1161/STROKEAHA.116.012999. Epub 2016 Jun 23.

20. Парфенов ВА, Захаров ВВ, Преображенская ИС. Когнитивные расстройства. Москва: Ремедиум; 2015. 187 с. [Parfenov VA, Zakharov VV, Preobrazhenskaya IS. Kognitivnye rasstroistva [Cognitive impairments]. Moscow: Remedium; 2015. 187 p.]

21. Кулеш АА, Шестаков ВВ. Сосудистые недементные когнитивные нарушения: диагноз, прогноз, лечение и профилактика. Неврология, нейропсихиатрия, психосоматика. 2017;9(3):68-75. [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

22. Greenberg SM, Charidimou A. Diagnosis of Cerebral Amyloid Angiopathy: Evolution of the Boston Criteria. Stroke. 2018 Feb;49(2):491-497. doi: 10.1161/STROKEAHA.117.016990. Epub 2018 Jan 15.

23. Charidimou A, Friedrich JO, Greenberg SM, Viswanathan A. Core cerebrospinal fluid biomarker profile in cerebral amyloid angiopathy: A meta analysis. Neurology. 2018 Feb 27;90(9): e754-e762. doi: 10.1212/WNL.0000000000005030. Epub 2018 Jan 31.

24. Charidimou A, Martinez-Ramirez S, Shoamanesh A, et al. Cerebral amyloid angiopathy with and without hemorrhage: evidence for different disease phenotypes. Neurology. 2015 Mar 24;84(12):1206-12. doi: 10.1212/WNL. 0000000000001398. Epub 2015 Feb 25.

25. 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 Mar; 265(3):567-577. doi: 10.1007/s00415-018-8740-z. Epub 2018 Jan 22.

26. Roh D, Sun CH, Schmidt JM, et al. Primary Intracerebral Hemorrhage: A Closer Look at Hypertension and Cerebral Amyloid Angiopathy. Neurocrit Care. 2018 Aug;29(1): 77-83. doi: 10.1007/s12028-018-0514-z.

27. 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):124-131. doi: 10.1159/000486554. Epub 2018 Mar 20.

28. 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 Mar;17(3): 232-240. doi: 10.1016/S1474-4422(18)30006-1. Epub 2018 Jan 10.

29. Yates PA, Villemagne VL, Ellis KA, et al. Cerebral microbleeds: a review of clinical, genetic, and neuroimaging associations. Front Neurol. 2014 Jan 6;4:205. doi: 10.3389/fneur.2013. 00205. eCollection 2014 Jan 6.

30. Poels MM, Vernooij MW, Ikram MA, et al. Prevalence and risk factors of cerebral microbleeds: an update of the Rotterdam scan study. Stroke. 2010 Oct;41(10 Suppl):S103-6.

31. doi: 10.1161/STROKEAHA.110.595181.

32. Chowdhury MH, Nagai A, Bokura H, et al. Age-related changes in white matter lesions, hippocampal atrophy, and cerebral microbleeds in healthy subjects without major cerebrovascular risk factors. J Stroke Cerebrovasc Dis. 2011 Jul-Aug;20(4):302-9. doi: 10.1016/j.jstrokecerebrovasdis.2009.12.010. Epub 2010 Jul 15.

33. Caunca MR, Del Brutto V, Gardener H, et al. Cerebral Microbleeds, Vascular Risk Factors, and Magnetic Resonance Imaging Markers: The Northern Manhattan Study. J Am Heart Assoc. 2016 Sep 16;5(9). pii: e003477.

34. doi: 10.1161/JAHA.116.003477.

35. Werring DJ, Gregoire SM, Cipolotti L. Cerebral microbleeds and vascular cognitive impairment. J Neurol Sci. 2010 Dec 15; 299(1-2):131-5. doi: 10.1016/j.jns.2010.08.034. Epub 2010 Sep 17.

36. Rosidi NL, Zhou J, Pattanaik S, et al. Cortical microhemorrhages cause local inflammation but do not trigger widespread dendrite degeneration. PLoS One. 2011;6(10):e26612. doi: 10.1371/journal.pone.0026612. Epub 2011 Oct 19.

37. Bokura H, Saika R, Yamaguchi T, et al. Microbleeds are associated with subsequent hemorrhagic and ischemic stroke in healthy elderly individuals. Stroke. 2011 Jul;42(7): 1867-71. doi: 10.1161/STROKEAHA.110.601922. Epub 2011 May 19.

38. Wilson D, Charidimou A, Ambler G, et al. Recurrent stroke risk and cerebral microbleed burden in ischemic stroke and TIA: A metaanalysis. Neurology. 2016 Oct 4;87(14): 1501-1510. Epub 2016 Sep 2.

39. Antithrombotic Trialists' Collaboration. Collaborative meta-analysis of randomised trials of antiplatelet therapy for prevention of death, myocardial infarction, and stroke in high risk patients. BMJ. 2002 Jan 12;324(7329):71-86.

40. Charidimou A, Shoamanesh A. Clinical relevance of microbleeds in acute stroke thrombolysis: Comprehensive meta-analysis. International META-MICROBLEEDS Initiative. Neurology. 2016 Oct 11;87(15):1534-1541. Epub 2016 Sep 14.

41. Tsivgoulis G, Zand R, Katsanos AH, et al. Risk of Symptomatic Intracerebral Hemorrhage After Intravenous Thrombolysis in Patients With Acute Ischemic Stroke and High Cerebral Microbleed Burden: A Meta analysis. JAMA Neurol. 2016 Jun 1;73(6):675-83. doi: 10.1001/ jamaneurol.2016.0292.

42. Linn J, Herms J, Dichgans M, et al. Subarachnoid hemosiderosis and superficial cortical hemosiderosis in cerebral amyloid angiopathy. AJNR Am J Neuroradiol. 2008 Jan; 29(1):184-6. Epub 2007 Oct 18.

43. Vernooij MW, Ikram MA, Hofman A, et al. Superficial siderosis in the general population. Neurology. 2009 Jul 21;73(3):202-5. doi: 10.1212/ WNL.0b013e3181ae7c5e.

44. Na HK, Park JH, Kim JH, et al. Cortical superficial siderosis: A marker of vascular amyloid in patients with cognitive impairment. Neurology. 2015 Feb 24;84(8):849-55. doi: 10.1212/WNL.0000000000001288. Epub 2015 Jan 28.

45. Khurram A, Kleinig T, Leyden J. Clinical associations and causes of convexity subarachnoid hemorrhage. Stroke. 2014 Apr;45(4): 1151-3. doi: 10.1161/STROKEAHA.113.004298. Epub 2014 Feb 4.

46. Linn J, Halpin A, Demaerel P, et al. Prevalence of superficial siderosis in patients with cerebral amyloid angiopathy. Neurology. 2010 Apr 27;74(17):1346-50. doi: 10.1212/ WNL.0b013e3181dad605.

47. Charidimou A, Peeters AP, Jager R, et al. Cortical superficial siderosis and intracerebral hemorrhage risk in cerebral amyloid angiopathy. Neurology. 2013 Nov 5;81(19):1666-73.

48. doi: 10.1212/01.wnl.0000435298.80023.7a. Epub 2013 Oct 9.

49. Kirchhof P, Benussi S, Kotecha D, et al. 2016 ESC Guidelines for the management of atrial fibrillation developed in collaboration with EACTS. Europace. 2016 Nov;18(11): 1609-1678. Epub 2016 Aug 27.

50. http://www.restarttrial.org/

51. 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 Feb;41(2):394-6. doi: 10.1161/ STROKEAHA.109.563932. Epub 2009 Dec 31.

52. Biffi A, Anderson CD, Battey TW, et al. Association between blood pressure control and risk of recurrent intracerebral hemorrhage. JAMA. 2015 Sep 1;314(9):904-12. doi: 10.1001/ jama.2015.10082.

53. Парфенов ВА, Старчина ЮА. Когнитивные расстройства и их лечение при артериальной гипертонии. Нервные болезни. 2015;(1):16-22. [Parfenov VA, Starchina YuA. Cognitive disorders and their treatment in arterial hypertension. Nervnye bolezni. 2015;(1): 16-22. (In Russ.)].

54. Остроумова ТМ, Парфенов ВА, Перепелова ЕМ и др. Поражение головного мозга как органа-мишени у пациентов среднего возраста с неосложненной артериальной гипертонией. Лечебное дело. 2017;(4):34-41. [Ostroumova TM, Parfenov VA, Perepelova EM, et al. Brain damage as a target organ in middleaged patients with uncomplicated arterial hypertension. Lechebnoe delo. 2017;(4):34-41. (In Russ.)].

55. 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 Mar;49(3):e46-e110. doi: 10.1161/STR.0000000000000158. Epub 2018 Jan 24.

56. Парфенов ВА, Вербицкая СВ. Вторичная профилактика ишемического инсульта и когнитивных нарушений. Медицинский совет. 2016;(11):18-24. [Parfenov VA, Verbitskaya SV. Secondary prevention of ischemic stroke and cognitive impairment. Meditsinskii sovet. 2016;(11):18-24. (In Russ.)].

57. Rakesh G, Szabo ST, Alexopoulos GS, Zannas AS. Strategies for dementia prevention: latest evidence and implications. Ther Adv Chronic Dis. 2017 Aug;8(8-9):121-136. doi: 10.1177/2040622317712442. Epub 2017 Jun 27.


For citation:


Kulesh A.A., Drobakha V.E., Shestakov V.V. Hemorrhagic manifestations of cerebral amyloid angiopathy: from pathogenesis to clinical significance. Neurology, Neuropsychiatry, Psychosomatics. 2018;10(3):4-11. (In Russ.) https://doi.org/10.14412/2074-2711-2018-3-4-11

Views: 227


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


ISSN 2074-2711 (Print)
ISSN 2310-1342 (Online)