По всем вопросам звоните:

+7 495 274-22-22

УДК: 616.8-005 DOI:10.33920/med-01-2009-04

Церебральная ишемия при нетравматическом субарахноидальном кровоизлиянии вследствие разрыва интракраниальных аневризм

В. А. Лукьянчиков доктор медицинских наук, профессор кафедры нейрохирургии и нейрореанимации и главный врач Клинического центра челюстно-лицевой, пластической хирургии и стоматологии ФГБОУ ВО «МГМСУ им. А. И. Евдокимова» Минздрава России, ORCID iD: 0000-0002-8263-1433
А. А. Солодов доктор медицинских наук, доцент кафедры анестезиологии, реаниматологии и неотложной медицины ФДПО и заместитель директора по научной работе Университетской клиники ФГБОУ ВО «МГМСУ им. А. И. Евдокимова» Минздрава России, ORCID iD: 0000-0002-8263-1433
И. М. Шетова кандидат медицинских наук, заместитель директора Университетской клиники ФГБОУ ВО «МГМСУ им. А. И. Евдокимова» Минздрава России, ORCID iD: 0000-0001-8975-7875
В. Д. Штадлер ординатор кафедры нейрохирургии и нейрореанимации ФГБОУ ВО «МГМСУ им. А. И. Евдокимова» Минздрава России, e-mail: vladislav.shtadler@gmail.com, ORCID iD: 0000-0002-7584-3083
В. В. Крылов академик РАН, доктор медицинских наук, профессор, заслуженный деятель науки РФ, директор Университетской клиники и заведующий кафедрой нейрохирургии и нейрореанимации ФГБОУ ВО «МГМСУ им. А. И. Евдокимова» Минздрава России, главный научный сотрудник отделения неотложной нейрохирургии ГБУЗ «НИИ СП им. Н. В. Склифосовского Департамента здравоохранения г. Москвы», главный внештатный нейрохирург Минздрава России, ORCID iD: 0000-0001-5256-0905

В статье освещены современные концепции о формировании церебральной ишемии, механизмы нарушения оксигенации и перфузии головного мозга, а также отдаленные морфологические и когнитивные нарушения при нетравматическом субарахноидальном кровоизлиянии вследствие разрыва интракраниальных аневризм.

Литература:

1. Клочихина О. А., Стаховская Л. В., Полунина Е. А. и др. Эпидемиология и прогноз уровня заболеваемости и смертности от инсульта в разных возрастных группах по данным территориально-популяционного регистра. Журнал неврологии и психиатрии им. C. С. Корсакова. 2019; 119 (8): 5–12. DOI: 10.17116/jnevro20191190825.

2. Шамалов Н. А., Стаховская Л. В., Клочихина О. А. и др. Анализ динамики основных типов инсульта и патогенетических вариантов ишемического инсульта. Журнал неврологии и психиатрии им. C. С. Корсакова. 2019; 119 (3): 5–10. DOI: 10.17116/jnevro20191190325.

3. Крылов В. В., Дашьян В. Г., Шатохин Т. А. и др. Хирургическое лечение церебральных аневризм в Российской Федерации. Вопросы нейрохирургии им. Н. Н. Бурденко. 2018; 82 (6): 5-14. DOI: 10.17116/neiro2018820615.

4. Крылов В. В., Дашьян В. Г., Шетова И. М. и др. Нейрохирургическая помощь больным с сосудистыми заболеваниями головного мозга в Российской Федерации. Нейрохирургия. 2017; 4: 11–20.

5. James S. L., Abate D., Abate K. H. et al. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. The Lancet 2018; 392 (10159): 1789–1858. DOI: 10.1016/S0140-6736 (18)32279-7.

6. Roth G. A., Abate D., Abate K. H. et al. Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980–2017: a systematic analysis for the Global Burden of Disease Study 2017. The Lancet 2018; 392 (10159): 1736–1788. DOI: 10.1016/S0140-6736 (18)32203-7.

7. Коновалов А. Н., Крылов В. В., Филатов Ю. М. и др. Рекомендательный протокол ведения больных с субарахноидальным кровоизлиянием вследствие разрыва аневризм сосудов головного мозга. Вопросы нейрохирургии им. Н. Н. Бурденко. 2006; 3: 3–10.

8. Connolly E. S., Rabinstein A. A., Carhuapoma J. R. et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association / American Stroke Association. Stroke. 2012; 43 (6): 1711–1737. DOI: 10.1161/STR.0b013e3182587839.

9. Topkoru B., Egemen E., Solaroglu I. et al. Early brain injury or vasospasm? An overview of common mechanisms. Current Drug Targets 2017; 18 (12): 1424–1429. DOI: 10.2174/1389450117666160905112923.

10. Foreman B. The pathophysiology of delayed cerebral ischemia. Journal of Clinical Neurophysiology 2016; 33 (3): 174–182. DOI: 10.1097/WNP.0000000000000273.

11. Budohoski K. P., Guilfoyle M., Helmy A. et al. The pathophysiology and treatment of delayed cerebral ischaemia following subarachnoid haemorrhage. Journal of Neurology, Neurosurgery, and Psychiatry. 2014; 85 (12): 1343–1353. DOI: 10.1136/jnnp-2014-307711.

12. Geraghty J. R., Testai F. D. Delayed cerebral ischemia after subarachnoid hemorrhage: beyond vasospasm and towards a multifactorial pathophysiology. Current Atherosclerosis Reports. 2017; 19 (12): 50. DOI: 10.1007/s11883-017-0690-x.

13. Francoeur C. L., Mayer S. A. Management of delayed cerebral ischemia after subarachnoid hemorrhage. Critical Care. 2016; 20 (1): 277. DOI: 10.1186/s13054-016-1447-6.

14. Schweizer T. A., Al-Khindi T., Macdonald R. L. Mini-Mental State Examination versus Montreal Cognitive Assessment: rapid assessment tools for cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Journal of the Neurological Sciences. 2012; 316 (1–2): 137–140. DOI: 10.1016/j.jns.2012.01.003.

15. Millikan C. H. Cerebral vasospasm and ruptured intracranial aneurysm. Archives of Neurology. 1975; 32 (7): 433–449. DOI: 10.1001/archneur.1975.00490490037003.

16. Крылов В. В., Природов А. В., Титова Г. П. др. Методы профилактики сосудистого спазма и отсроченной ишемии головного мозга у пациентов с массивным субарахноидальным кровоизлиянием вследствие разрыва аневризм сосудов головного мозга. Нейрохирургия. 2019; 21 (1): 12–26. DOI: 10.17650/1683-3295-2019-21-1-12-26.

17. Crompton M. R. The pathogenesis of cerebral infarction following the rupture of cerebral berry aneurysms. Brain. 1964; 87 (3): 491–510. DOI: 10.1093/brain/87.3.491.

18. Dhar R., Scalfani M. T., Blackburn S. et al. Relationship between angiographic vasospasm and regional hypoperfusion in aneurysmal subarachnoid hemorrhage. Stroke. 2012; 43 (7): 1788–1794. DOI: 10.1161/STROKEAHA.111.646836.

19. Macdonald R. L., Kassell N. F., Mayer S. et al. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke. 2008; 39 (11): 3015–3021. DOI: 10.1161/STROKEAHA.108.519942.

20. Macdonald R. L., Higashida R. T., Keller E. et al. Preventing vasospasm improves outcome after aneurysmal subarachnoid hemorrhage: rationale and design of CONSCIOUS-2 and CONSCIOUS-3 trials. Neurocritical Care. 2010; 13 (3): 416–424. DOI: 10.1007/s12028-010-9433-3.

21. Tam A. K. H., Ilodigwe D., Mocco J. et al. Impact of systemic inflammatory response syndrome on vasospasm, cerebral infarction, and outcome after subarachnoid hemorrhage: exploratory analysis of CONSCIOUS-1 database. Neurocritical Care. 2010; 13 (2): 182–189. DOI: 10.1007/s12028-010-9402-x.

22. Bruder N., Rabinstein A. Cardiovascular and pulmonary complications of aneurysmal subarachnoid hemorrhage. Neurocritical Care. 2011; 15 (2): 257–269. DOI: 10.1007/s12028-011-9598-4.

23. Cavallo C., Safavi-Abbasi S., Kalani M. Y. S. et al. Pulmonary complications after spontaneous aneurysmal subarachnoid hemorrhage: experience from Barrow Neurological Institute. World Neurosurgery. 2018; 119: e366– e373. DOI: 10.1016/j.wneu.2018.07.166.

24. Soyalp C., Kocak M. N., Ahiskalioglu A. et al. New determinants for casual peripheral mechanism of neurogenic lung edema in subarachnoid hemorrhage due to ischemic degeneration of vagal nerve, kidney and lung circuitry. Experimental study. Acta Cirurgica Brasileira. 2019; 34 (3): e201900303. DOI: 10.1590/s0102-865020190030000003.

25. Распутина Д. А., Рутковский Р. В., Мерцалов С. А. и др. Нейрогенная стрессорная кардиомиопатия вызванная аневризматическим субарахноидальным кровоизлиянием. Российский кардиологический журнал. 2019; 24 (2): 81–85. DOI: 10.15829/1560-4071-2019-2-81–85.

26. Kerro A., Woods T., Chang J. J. Neurogenic stunned myocardium in subarachnoid hemorrhage. Journal of Critical Care. 2017; 38: 27–34. DOI: 10.1016/j.jcrc.2016.10.010.

27. Weiner M. M., Asher D. I., Augoustides J. G. et al. Takotsubo cardiomyopathy: a clinical update for the cardiovascular anesthesiologist. Journal of Cardiothoracic and Vascular Anesthesia. 2017; 31 (1): 334–344. DOI: 10.1053/j.jvca.2016.06.004.

28. Sehba F. A., Friedrich V. Early events after aneurysmal subarachnoid hemorrhage. Acta Neurochirurgica Supplement. 2015; 120: 23–28. DOI: 10.1007/978-3-319-04981-6_4.

29. Rifkind J. M., Mohanty J. G., Nagababu E. The pathophysiology of extracellular hemoglobin associated with enhanced oxidative reactions. Frontiers in Physiology. 2015; 5: 500. DOI: 10.3389/fphys.2014.00500.

30. Blackburn S. L., Kumar P. T., McBride D. et al. Unique contribution of haptoglobin and haptoglobin genotype in aneurysmal subarachnoid hemorrhage. Frontiers in Physiology 2018; 9: 592. DOI: 10.3389/fphys.2018.00592.

31. Galea J., Cruickshank G., Teeling J. L. et al. The intrathecal CD163-haptoglobin-hemoglobin scavenging system in subarachnoid hemorrhage. Journal of Neurochemistry. 2012; 121 (5): 785–792. DOI: 10.1111/j.1471-4159.2012.07716.x.

32. Ohnishi H., Iihara K., Kaku Y. et al. Haptoglobin phenotype predicts cerebral vasospasm and clinical deterioration after aneurysmal subarachnoid hemorrhage. Journal of Stroke and Cerebrovascular Diseases. 2013; 22 (4): 520–526. DOI: 10.1016/j.jstrokecerebrovasdis.2013.02.005.

33. Kantor E., Bayır H., Ren D. et al. Haptoglobin genotype and functional outcome after aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery. 2014; 120 (2): 386–390. DOI: 10.3171/2013.10.JNS13219.

34. Leclerc J. L., Blackburn S., Neal D. et al. Haptoglobin phenotype predicts the development of focal and global cerebral vasospasm and may influence outcomes after aneurysmal subarachnoid hemorrhage. Proceedings of the National Academy of Sciences. 2015; 112 (4): 1155–1160. DOI: 10.1073/pnas.1412833112.

35. Leao A. A. P. Spreading depression of activity in the cerebral cortex. Journal of Neurophysiology 1944; 7 (6): 359–390. DOI: 10.1152/jn.1944.7.6.359.

36. Leao A. A. P. Further observations on the spreading depression of activity in the cerebral cortex. Journal of Neurophysiology. 1947; 10 (6): 409–414. DOI: 10.1152/jn.1947.10.6.409.

37. Куксова Н. С., Хамидова Л. Т., Трофимова Е. Ю. Оценка функционального состояния головного мозга при нетравматическом субарахноидальном кровоизлиянии. Часть I. Сосудистый спазм, ишемия мозга и электрическая активность. Нейрохирургия. 2011; (3): 34–42.

38. Куксова Н. С., Хамидова Л. Т. Оценка функционального состояния головного мозга при нетравматическом субарахноидальном кровоизлиянии. Часть II. Электрическая активность мозга при внутримозговых и внутрижелудочковых кровоизлияниях, зависимость исхода заболевания от уровня функциональных нарушений. Нейрохирургия. 2012; (2): 27–33.

39. Dreier J. P. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nature Medicine. 2011; 17 (4): 439–447. DOI: 10.1038/nm.2333.

40. Sánchez-Porras R., Zheng Z., Santos E. et al. The role of spreading depolarization in subarachnoid hemorrhage. European Journal of Neurology. 2013; 20 (8): 1121–1127. DOI: 10.1111/ene.12139.

41. Dreier J. P., Woitzik J., Fabricius M. et al. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain. 2006; 129 (12): 3224–3237. DOI: 10.1093/brain/awl297.

42. Sehba F. A., Ding W. H., Chereshnev I. et al. Effects of S-nitrosoglutathione on acute vasoconstriction and glutamate release after subarachnoid hemorrhage. Stroke. 1999; 30 (9): 1955–1961. DOI: 10.1161/01.str.30.9.1955.

43. Pradilla G., Chaichana K. L., Hoang S. et al. Inflammation and cerebral vasospasm after subarachnoid hemorrhage. Neurosurgery Clinics of North America. 2010; 21 (2): 365–379. DOI: 10.1016/j.nec.2009.10.008.

44. Ahn S.-H., Savarraj J. P. J., Parsha K. et al. Inflammation in delayed ischemia and functional outcomes after subarachnoid hemorrhage. Journal of Neuroinflammation. 2019; 16 (1): 213. DOI: 10.1186/s12974-019-1578-1.

45. Croci D. M., Wanderer S., Strange F. et al. Systemic and CSF interleukin-1α expression in a rabbit closed cranium subarachnoid hemorrhage model: an exploratory study. Brain Sciences. 2019; 9: 249. DOI: 10.3390/brainsci9100249.

46. Ridwan S., Greschus S., Boström J. et al. Spontaneous aneurysmal subarachnoid hemorrhage and related cortisol and immunologic alterations: impact on patients’ Health-related Quality of Life. Journal of Neurological Surgery Part A: Central European Neurosurgery. 2019; 80: 371–380. DOI: 10.1055/s-0039-1677827.

47. Wu W., Guan Y., Zhao G. et al. Elevated IL-6 and TNF-α levels in cerebrospinal fluid of subarachnoid hemorrhage patients. Molecular Neurobiology. 2016; 53 (5): 3277–3285. DOI: 10.1007/s12035-015-9268-1.

48. Wolf M. E. Functional TCD: regulation of cerebral hemodynamics — cerebral autoregulation, vasomotor reactivity, and neurovascular coupling. Frontiers of Neurology and Neuroscience. 2015; 36: 40–56. DOI: 10.1159/000366236.

49. Титова Ю. В., Петриков С. С., Солодов А. А. и др. Влияние церебрального перфузионного давления и сердечного выброса на оксигенацию и метаболизм головного мозга. Анестезиология и реаниматология. 2013; 4: 54–59.

50. Wellman G. C., Koide M. Impact of subarachnoid hemorrhage on parenchymal arteriolar function. Acta Neurochirurgica Supplementum. 2013; 115: 173–177. DOI: 10.1007/978-3-7091-1192-5_33.

51. Крылов В. В., Калинкин А. А., Петриков С. С. Патогенез сосудистого спазма и ишемии головного мозга при нетравматическом субарахноидальном кровоизлиянии вследствие разрыва церебральных аневризм. Неврологический журнал. 2014; 5 (19): 4–12.

52. Sehba F. A., Friedrich V. Cerebral microvasculature is an early target of subarachnoid hemorrhage. Acta Neurochirurgica Supplementum. 2013; 115: 199–205. DOI: 10.1007/978-3-7091-1192-5_37.

53. Yundt K. D., Grubb R. L., Diringer M. N. et al. Autoregulatory vasodilation of parenchymal vessels is impaired during cerebral vasospasm. Journal of Cerebral Blood Flow & Metabolism. 1998; 18 (4): 419–424. DOI: 10.1097/00004647-199804000-00010.

54. Крылов В. В., Петриков С. С., Калинкин А. А. и др. Влияние терапии антагонистами кальция на исходы лечения больных с разрывом церебральных аневризм и высоким риском развития сосудистого спазма. Неврологический журнал. 2016; 21 (5): 280–286. DOI: 10.18821/1560-9545-2016-21-5-280-286.

55. Suzuki S., Suzuki M., Iwabuchi T. et al. Role of multiple cerebral microthrombosis in symptomatic cerebral vasospasm: with a case report. Neurosurgery. 1983; 13 (2): 199–203. DOI: 10.1227/00006123-198308000-00018.

56. Sabri M., Ai J., Lakovic K. et al. Mechanisms of microthrombi formation after experimental subarachnoid hemorrhage. Neuroscience. 2012; 224: 26–37. DOI: 10.1016/j.neuroscience.2012.08.002.

57. Vergouwen M. D. I., Vermeulen M., Coert B. A. et al. Microthrombosis after aneurysmal subarachnoid hemorrhage: an additional explanation for delayed cerebral ischemia. Journal of Cerebral Blood Flow & Metabolism. 2008; 28 (11): 1761–1770. DOI: 10.1038/jcbfm.2008.74.

58. Al-Mufti F., Amuluru K., Damodara N. et al. Novel management strategies for medically-refractory vasospasm following aneurysmal subarachnoid hemorrhage. Journal of the Neurological Sciences. 2018; 390: 44–51. DOI: 10.1016/j.jns.2018.02.039.

59. De Oliveira Manoel A. L., Macdonald R. L. Neuroinflammation as a target for intervention in subarachnoid hemorrhage. Frontiers in Neurology. 2018; 9: 292. DOI: 10.3389/fneur.2018.00292.

60. Wang A. Y.-C., Hsieh P.-C., Chen C.-C. et al. Effect of intracranial pressure control on improvement of cerebral perfusion after acute subarachnoid hemorrhage: a comparative angiography study based on temporal changes of intracranial pressure and systemic pressure. World Neurosurgery. 2018; 120: e290–e296. DOI: 10.1016/j.wneu.2018.08.053.

61. Солодов А. А., Петриков С. С., Клычникова Е. В. и др. Влияние нормобарической гипероксии на оксигенацию и метаболизм головного мозга, состояние окислительного стресса у больных с субарахноидальным кровоизлиянием вследствие разрыва аневризмы сосудов головного мозга. Анестезиология и реаниматология. 2013; 4: 66–71.

62. Klychnikova E. V., Tazina E. V., Solodov A. A. et al. The effects of normobaric hyperoxia on oxidative stress and factors of endogenous vascular regulation in patients who suffered from non-traumatic subarachnoid hemorrhages and remained in critical condition. Neurochemical Journal. 2013; 7 (3): 234–239. DOI: 10.1134/S1819712413030057.

63. Chong S. P., Merkle C. W., Leahy C. et al. Cerebral metabolic rate of oxygen (CMRO2) assessed by combined doppler and spectroscopic OCT. Biomedical Optics Express. 2015; 6 (10): 3941–3951. DOI: 10.1364/BOE.6.003941.

64. Liu P., Huang H., Rollins N. et al. Quantitative assessment of global cerebral metabolic rate of oxygen (CMRO2) in neonates using MRI. NMR in Biomedicine. 2014; 27 (3): 332–340. DOI: 10.1002/nbm.3067.

65. Madsen P. L., Holm S., Herning M. et al. Average blood flow and oxygen uptake in the human brain during resting wakefulness: a critical appraisal of the Kety-Schmidt technique. Journal of Cerebral Blood Flow & Metabolism. 1993; 13 (4): 646–655. DOI: 10.1038/jcbfm.1993.83.

66. Vavilala M. S., Lee L. A., Lam A. M. Cerebral blood flow and vascular physiology. Anesthesiol Anesthesiology Clinics of North America. 2002; 20 (2): 247–264. DOI: 10.1016/s0889-8537 (01)00012-8.

67. Fan A. P., Jahanian H., Holdsworth S. J. et al. Comparison of cerebral blood flow measurement with [15O]water positron emission tomography and arterial spin labeling magnetic resonance imaging: a systematic review. Journal of Cerebral Blood Flow & Metabolism. 2016; 36 (5): 842–861. DOI: 10.1177/0271678X16636393.

68. Crone C. The permeability of capillaries in various organs as determined by use of the «indicator diffusion» method. Acta Physiologica Scandinavica. 1963; 58 (4): 292–305. DOI: 10.1111/j.1748-1716.1963.tb02652.x.

69. Renkin E. M. Effects of blood flow on diffusion kinetics in isolated, perfused hindlegs of cats; a double circulation hypothesis. American Journal of Physiology-Legacy Content. 1955; 183 (1): 125–136. DOI: 10.1152/ ajplegacy.1955.183.1.125.

70. Fox P. T., Raichle M. E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proceedings of the National Academy of Sciences. 1986; 83 (4): 1140–1144. DOI: 10.1073/pnas.83.4.1140.

71. Pawlik G., Rackl A., Bing R. J. Quantitative capillary topography and blood flow in the cerebral cortex of cats: an in vivo microscopic study. Brain Research. 1981; 208 (1): 35–58. DOI: 10.1016/0006-8993 (81)90619-3.

72. Villringer A., Them A., Lindauer U. et al. Capillary perfusion of the rat brain cortex. An in vivo confocal microscopy study. Circulation Research. 1994; 75 (1): 55–62. DOI: 10.1161/01.res.75.1.55.

73. Jespersen S. N., Østergaard L. The roles of cerebral blood flow, capillary transit time heterogeneity, and oxygen tension in brain oxygenation and metabolism. Journal of Cerebral Blood Flow & Metabolism. 2012; 32 (2): 264–277. DOI: 10.1038/jcbfm.2011.153.

74. Peppiatt C. M., Howarth C., Mobbs P. et al. Bidirectional control of CNS capillary diameter by pericytes. Nature. 2006; 443 (7112): 700–704. DOI: 10.1038/nature05193.

75. Østergaard L., Jespersen S. N., Mouridsen K. et al. The role of the cerebral capillaries in acute ischemic stroke: the extended penumbra model. Journal of Cerebral Blood Flow & Metabolism. 2013; 33 (5): 635–648. DOI: 10.1038/jcbfm.2013.18.

76. Østergaard L., Aamand R., Karabegovic S. et al. The role of the microcirculation in delayed cerebral ischemia and chronic degenerative changes after subarachnoid hemorrhage. Journal of Cerebral Blood Flow & Metabolism. 2013; 33 (12): 1825–1837. DOI: 10.1038/jcbfm.2013.173.

77. Krzyzewski R. M., Klis K. M., Kwinta B. M. et al. High leukocyte count and risk of poor outcome after subarachnoid hemorrhage: a meta-analysis. World Neurosurgery. 2020; 135: e541–e547. DOI: 10.1016/j.wneu.2019.12.056.

78. Anzabi M., Angleys H., Aamand R. et al. Capillary flow disturbances after experimental subarachnoid hemorrhage: a contributor to delayed cerebral ischemia? Microcirculation. 2019; 26 (3): e12516. DOI: 10.1111/micc.12516.

79. Wang H.-C., Tsai J.-C., Lee J.-E. et al. Direct visualization of microcirculation impairment after acute subdural hemorrhage in a novel animal model. Journal of Neurosurgery. 2017; 129 (4): 997–1007. DOI: 10.3171/2017.5.JNS162579.

80. Lovelock C. E., Rinkel G. J. E., Rothwell P. M. Time trends in outcome of subarachnoid hemorrhage: populationbased study and systematic review. Neurology. 2010; 74 (19): 1494–1501. DOI: 10.1212/WNL.0b013e3181dd42b3.

81. Claassen J., Carhuapoma J. R., Kreiter K. T. et al. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke. 2002; 33 (5): 1225–1232. DOI: 10.1161/01.str.0000015624.29071.1f.

82. Rosengart A. J., Schultheiss K. E., Tolentino J. et al. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007; 38 (8): 2315–2321. DOI: 10.1161/STROKEAHA.107.484360.

83. Rabinstein A. A., Weigand S., Atkinson J. L. D. et al. Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2005; 36 (5): 992–997. DOI: 10.1161/01.STR.0000163090.59350.5a.

84. Wartenberg K. E., Schmidt J. M., Claassen J. et al. Impact of medical complications on outcome after subarachnoid hemorrhage. Critical Care Medicine. 2006; 34 (3): 617–623. DOI: 10.1097/01.ccm.0000201903.46435.35.

85. Мельникова Е. А., Крылов В. В. Когнитивные нарушения после хирургического лечения внутричерепных артериальных аневризм в остром периоде кровоизлияния. Журнал неврологии и психиатрии им. C. С. Корсакова. 2007; 107 (S21): 16–24.

86. Dombovy M. L., Drew-Cates J., Serdans R. Recovery and rehabilitation following subarachnoid haemorrhage: Part II. Long-term follow-up. Brain Injury. 1998; 12 (10): 887–894. DOI: 10.1080/026990598122106.

87. Al-Khindi T., Macdonald R. L., Schweizer T. A. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke. 2010; 41 (8): e519–e536. DOI: 10.1161/STROKEAHA.110.581975.

88. Von Vogelsang A.-C., Forsberg C., Svensson M. et al. Patients experience high levels of anxiety 2 years following aneurysmal subarachnoid hemorrhage. World Neurosurgery. 2015; 83 (6): 1090–1097. DOI: 10.1016/j.wneu.2014.12.027.

89. Крылов В. В., Григорьева Е. В., Лукьянчиков В. А. и др. Оценка церебральной перфузии в отдаленном послеоперационном периоде у пациентов с интракраниальными аневризмами. Неврологический журнал. 2018; 23 (5): 241–247. DOI: 10.18821/1560-9545-2018-23-5-241-247.

90. Bendel P., Koivisto T., Äikiä M. et al. Atrophic enlargement of CSF volume after subarachnoid hemorrhage: correlation with neuropsychological outcome. American Journal of Neuroradiology. 2010; 31 (2): 370–376. DOI: 10.3174/ajnr.A1804.

91. Tam A. K. H., Ilodigwe D., Li Z. et al. Global cerebral atrophy after subarachnoid hemorrhage: a possible marker of acute brain injury and assessment of its impact on outcome. Acta Neurochirurgica Supplementum. 2013; 115: 17–21. DOI: 10.1007/978-3-7091-1192-5_5.

92. Anzabi M., Ardalan M., Iversen N. K. et al. Hippocampal atrophy following subarachnoid hemorrhage correlates with disruption of astrocyte morphology and capillary coverage by AQP4. Frontiers in Cellular Neuroscience. 2018; 12: 19. DOI: 10.3389/fncel.2018.00019.

93. Мельникова Е. А., Крылов В. В. Нейропсихологические исходы после раннего хирургического лечения аневризм сосудов головного мозга. Нейрохирургия. 2008; 4: 21–29.

94. Войцеховский Д. В., Свистов Д. В., Савелло А. В. и др. Нейропсихологические последствия и качество жизни пациентов после хирургического лечения аневризм головного мозга. Нейрохирургия. 2017; 4: 74–79.

1. Klochihina O. A., Stakhovskaya L. V., Polunina E. A. et al. Epidemiology and prognosis of the level of morbidity and mortality from stroke in different age groups according to the territorial-population register. Zhurnal nevrologii i psikhiatrii imeni S. S. Korsakova (S. S. Korsakov Journal of Neurology and Psychiatry). 2019; 119 (8): 5–12. DOI: 10.17116/jnevro20191190825 (In Russ.).

2. Shamalov N. A., Stakhovskaya L. V., Klochihina O. A. et al. An analysis of the dynamics of the main types of stroke and pathogenetic variants of ischemic stroke. Zhurnal nevrologii i psikhiatrii imeni S. S. Korsakova (S. S. Korsakov Journal of Neurology and Psychiatry). 2019; 119 (3): 5–10. DOI: 10.17116/jnevro20191190325 (In Russ.).

3. Krylov V. V., Dash’yan V. G., Shatokhin T. A. et al. Surgical treatment of cerebral aneurysms in the Russian Federation. Zhurnal «Voprosy neirokhirurgii» imeni N. N. Burdenko (Burdenko’s Journal of Neurosurgery). 2018; 82 (6): 5–14. DOI: 10.17116/neiro2018820615 (In Russ.).

4. Krylov V. V., Dash`yan V. G., Shetova I. M. et al. Neurosurgical care for patients with cerebrovascular pathology in Russian Federation. Neirokhirurgiya (Russian Journal of Neurosurgery). 2017; (4): 11–20 (In Russ.).

5. James S. L., Abate D., Abate K. H. et al. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. The Lancet 2018; 392 (10159): 1789–1858. DOI: 10.1016/S0140-6736 (18)32279-7.

6. Roth G. A., Abate D., Abate K. H. et al. Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980–2017: a systematic analysis for the Global Burden of Disease Study 2017. The Lancet 2018; 392 (10159): 1736–1788. DOI: 10.1016/S0140-6736 (18)32203-7.

7. Konovalov A. N., Krylov V. V., Filatov Yu. M. et al. Advisable management protocol for patients with subarachnoidal hemorrhage resulting from cerebral vascular aneurysmal rupture. Zhurnal «Voprosy neirokhirurgii» imeni N. N. Burdenko (Burdenko’s Journal of Neurosurgery). 2006; 3: 3–10 (In Russ.).

8. Connolly E. S., Rabinstein A. A., Carhuapoma J. R. et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association / American Stroke Association. Stroke. 2012; 43 (6): 1711–1737. DOI: 10.1161/STR.0b013e3182587839.

9. Topkoru B., Egemen E., Solaroglu I. et al. Early brain injury or vasospasm? An overview of common mechanisms. Current Drug Targets 2017; 18 (12): 1424–1429. DOI: 10.2174/1389450117666160905112923.

10. Foreman B. The pathophysiology of delayed cerebral ischemia. Journal of Clinical Neurophysiology 2016; 33 (3): 174–182. DOI: 10.1097/WNP.0000000000000273.

11. Budohoski K. P., Guilfoyle M., Helmy A. et al. The pathophysiology and treatment of delayed cerebral ischaemia following subarachnoid haemorrhage. Journal of Neurology, Neurosurgery, and Psychiatry. 2014; 85 (12): 1343–1353. DOI: 10.1136/jnnp-2014-307711.

12. Geraghty J. R., Testai F. D. Delayed cerebral ischemia after subarachnoid hemorrhage: beyond vasospasm and towards a multifactorial pathophysiology. Current Atherosclerosis Reports. 2017; 19 (12): 50. DOI: 10.1007/ s11883-017-0690-x.

13. Francoeur C. L., Mayer S. A. Management of delayed cerebral ischemia after subarachnoid hemorrhage. Critical Care. 2016; 20 (1): 277. DOI: 10.1186/s13054-016-1447-6.

14. Schweizer T. A., Al-Khindi T., Macdonald R. L. Mini-Mental State Examination versus Montreal Cognitive Assessment: rapid assessment tools for cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Journal of the Neurological Sciences. 2012; 316 (1–2): 137–140. DOI: 10.1016/j.jns.2012.01.003.

15. Millikan C. H. Cerebral vasospasm and ruptured intracranial aneurysm. Archives of Neurology. 1975; 32 (7): 433–449. DOI: 10.1001/archneur.1975.00490490037003.

16. Krylov V. V., Prirodov A. V., Titova G. P. et al. Prevention of cerebral vasospasm and delayed cerebral ischemia in patients with massive aneurysmal subarachnoid hemorrhage. Neirokhirurgiya (Russian Journal of Neurosurgery). 2019; 21 (1): 12–26. DOI: 10.17650/1683-3295-2019-21-1-12-26 (In Russ.).

17. Crompton M. R. The pathogenesis of cerebral infarction following the rupture of cerebral berry aneurysms. Brain. 1964; 87 (3): 491–510. DOI: 10.1093/brain/87.3.491.

18. Dhar R., Scalfani M. T., Blackburn S. et al. Relationship between angiographic vasospasm and regional hypoperfusion in aneurysmal subarachnoid hemorrhage. Stroke. 2012; 43 (7): 1788–1794. DOI: 10.1161/STROKEAHA.111.646836.

19. Macdonald R. L., Kassell N. F., Mayer S. et al. Clazosentan to overcome neurological ischemia and infarction occurring after subarachnoid hemorrhage (CONSCIOUS-1): randomized, double-blind, placebo-controlled phase 2 dose-finding trial. Stroke. 2008; 39 (11): 3015–3021. DOI: 10.1161/STROKEAHA.108.519942.

20. Macdonald R. L., Higashida R. T., Keller E. et al. Preventing vasospasm improves outcome after aneurysmal subarachnoid hemorrhage: rationale and design of CONSCIOUS-2 and CONSCIOUS-3 trials. Neurocritical Care. 2010; 13 (3): 416–424. DOI: 10.1007/s12028-010-9433-3.

21. Tam A. K. H., Ilodigwe D., Mocco J. et al. Impact of systemic inflammatory response syndrome on vasospasm, cerebral infarction, and outcome after subarachnoid hemorrhage: exploratory analysis of CONSCIOUS-1 database. Neurocritical Care. 2010; 13 (2): 182–189. DOI: 10.1007/s12028-010-9402-x.

22. Bruder N., Rabinstein A. Cardiovascular and pulmonary complications of aneurysmal subarachnoid hemorrhage. Neurocritical Care. 2011; 15 (2): 257–269. DOI: 10.1007/s12028-011-9598-4.

23. Cavallo C., Safavi-Abbasi S., Kalani M. Y. S. et al. Pulmonary complications after spontaneous aneurysmal subarachnoid hemorrhage: experience from Barrow Neurological Institute. World Neurosurgery. 2018; 119: e366– e373. DOI: 10.1016/j.wneu.2018.07.166.

24. Soyalp C., Kocak M. N., Ahiskalioglu A. et al. New determinants for casual peripheral mechanism of neurogenic lung edema in subarachnoid hemorrhage due to ischemic degeneration of vagal nerve, kidney and lung circuitry. Experimental study. Acta Cirurgica Brasileira. 2019; 34 (3): e201900303. DOI: 10.1590/s0102-865020190030000003.

25. Rasputina D. A., Rutkovsky R. V., Mertsalov S. A. et al. Neurogenic stressor cardiomyopathy caused by aneurysmal subarachnoid hemorrhage. Rossijskij kardiologicheskij zhurnal (Russian Journal of Cardiology). 2019; 24 (2): 81–85. DOI: 10.15829/1560-4071-2019-2-81-85 (In Russ.).

26. Kerro A., Woods T., Chang J. J. Neurogenic stunned myocardium in subarachnoid hemorrhage. Journal of Critical Care. 2017; 38: 27–34. DOI: 10.1016/j.jcrc.2016.10.010.

27. Weiner M. M., Asher D. I., AugoustidesJ. G. et al. Takotsubo cardiomyopathy: a clinical update for the cardiovascular anesthesiologist. Journal of Cardiothoracic and Vascular Anesthesia. 2017; 31 (1): 334–344. DOI: 10.1053/j.jvca.2016.06.004.

28. Sehba F. A., Friedrich V. Early events after aneurysmal subarachnoid hemorrhage. Acta Neurochirurgica Supplement. 2015; 120: 23–28. DOI: 10.1007/978-3-319-04981-6_4.

29. Rifkind J. M., Mohanty J. G., Nagababu E. The pathophysiology of extracellular hemoglobin associated with enhanced oxidative reactions. Frontiers in Physiology. 2015; 5: 500. DOI: 10.3389/fphys.2014.00500.

30. Blackburn S. L., Kumar P. T., McBride D. et al. Unique contribution of haptoglobin and haptoglobin genotype in aneurysmal subarachnoid hemorrhage. Frontiers in Physiology 2018; 9: 592. DOI: 10.3389/fphys.2018.00592.

31. Galea J., Cruickshank G., Teeling J. L. et al. The intrathecal CD163-haptoglobin-hemoglobin scavenging system in subarachnoid hemorrhage. Journal of Neurochemistry. 2012; 121 (5): 785–792. DOI: 10.1111/j.1471-4159.2012.07716.x.

32. Ohnishi H., Iihara K., Kaku Y. et al. Haptoglobin phenotype predicts cerebral vasospasm and clinical deterioration after aneurysmal subarachnoid hemorrhage. Journal of Stroke and Cerebrovascular Diseases. 2013; 22 (4): 520–526. DOI: 10.1016/j.jstrokecerebrovasdis.2013.02.005.

33. Kantor E., Bayır H., Ren D. et al. Haptoglobin genotype and functional outcome after aneurysmal subarachnoid hemorrhage. Journal of Neurosurgery. 2014; 120 (2): 386–390. DOI: 10.3171/2013.10.JNS13219.

34. Leclerc J. L., Blackburn S., Neal D. et al. Haptoglobin phenotype predicts the development of focal and global cerebral vasospasm and may influence outcomes after aneurysmal subarachnoid hemorrhage. Proceedings of the National Academy of Sciences. 2015; 112 (4): 1155–1160. DOI: 10.1073/pnas.1412833112.

35. Leao A. A. P. Spreading depression of activity in the cerebral cortex. Journal of Neurophysiology 1944; 7 (6): 359–390. DOI: 10.1152/jn.1944.7.6.359.

36. Leao A. A. P. Further observations on the spreading depression of activity in the cerebral cortex. Journal of Neurophysiology. 1947; 10 (6): 409–414. DOI: 10.1152/jn.1947.10.6.409.

37. Kuksova N. S., Khamidova L. T., Trofimova E. Ju. Estimation of brain functional state during non-traumatic subarachnoid hemorrhage. Part 1. Angiospasm, brain ischemia and electrical activity. Neirokhirurgiya (Russian Journal of Neurosurgery). 2011; 3: 34–42 (In Russ.).

38. Kuksova N. S., Khamidova L. T. Estimation of brain functional condition in case of nontraumatic subarachnoid hemorrhage. Part 2. Electric activity of brain under condition of intracerebral and ventricular hemorrhages; dependence of disease outcome from level of functional disturbances. Neirokhirurgiya (Russian Journal of Neurosurgery) 2012; (2): 27–33 (In Russ.).

39. Dreier J. P. The role of spreading depression, spreading depolarization and spreading ischemia in neurological disease. Nature Medicine. 2011; 17 (4): 439–447. DOI: 10.1038/nm.2333.

40. Sánchez-Porras R., Zheng Z., Santos E. et al. The role of spreading depolarization in subarachnoid hemorrhage. European Journal of Neurology. 2013; 20 (8): 1121–1127. DOI: 10.1111/ene.12139.

41. DreierJ. P., Woitzik J., Fabricius M. et al. Delayed ischaemic neurological deficits after subarachnoid haemorrhage are associated with clusters of spreading depolarizations. Brain. 2006; 129 (12): 3224–3237. DOI: 10.1093/brain/awl297.

42. Sehba F. A., Ding W. H., Chereshnev I. et al. Effects of S-nitrosoglutathione on acute vasoconstriction and glutamate release after subarachnoid hemorrhage. Stroke. 1999; 30 (9): 1955–1961. DOI: 10.1161/01.str.30.9.1955.

43. Pradilla G., Chaichana K. L., Hoang S. et al. Inflammation and cerebral vasospasm after subarachnoid hemorrhage. Neurosurgery Clinics of North America. 2010; 21 (2): 365–379. DOI: 10.1016/j.nec.2009.10.008.

44. Ahn S.-H., Savarraj J. P. J., Parsha K. et al. Inflammation in delayed ischemia and functional outcomes after subarachnoid hemorrhage. Journal of Neuroinflammation. 2019; 16 (1): 213. DOI: 10.1186/s12974-019-1578-1.

45. Croci D. M., Wanderer S., Strange F. et al. Systemic and CSF interleukin-1α expression in a rabbit closed cranium subarachnoid hemorrhage model: an exploratory study. Brain Sciences. 2019; 9: 249. DOI: 10.3390/brainsci9100249.

46. Ridwan S., Greschus S., Boström J. et al. Spontaneous aneurysmal subarachnoid hemorrhage and related cortisol and immunologic alterations: impact on patients’ Health-related Quality of Life. Journal of Neurological Surgery Part A: Central European Neurosurgery. 2019; 80: 371–380. DOI: 10.1055/s-0039-1677827.

47. Wu W., Guan Y., Zhao G. et al. Elevated IL-6 and TNF-α levels in cerebrospinal fluid of subarachnoid hemorrhage patients. Molecular Neurobiology. 2016; 53 (5): 3277–3285. DOI: 10.1007/s12035-015-9268-1.

48. Wolf M. E. Functional TCD: regulation of cerebral hemodynamics — cerebral autoregulation, vasomotor reactivity, and neurovascular coupling. Frontiers of Neurology and Neuroscience. 2015; 36: 40–56. DOI: 10.1159/000366236.

49. Titova Yu. V., Petrikov S. S., Solodov A. A. et al. Influence of cerebral perfusion pressure and cardiac output on brain oxygenation and metabolism. Anesteziologiya i reanimatologiya (Russian journal of Anaesthesiology and Reanimatology). 2013; (4): 54–59 (In Russ.).

50. Wellman G. C., Koide M. Impact of subarachnoid hemorrhage on parenchymal arteriolar function. Acta Neurochirurgica Supplementum. 2013; 115: 173–177. DOI: 10.1007/978-3-7091-1192-5_33.

51. Krylov V. V., Kalinkin A. A., Petrikov S. S. The pathogenesis of cerebral angiospasm and brain ischemia in patients with non-traumatic subarachnoid hemorrhage due to cerebral aneurysm rupture. Nevrologicheskij zhurnal (The Neurological Journal). 2014 (5); 19: 4–12 (In Russ.).

52. Sehba F. A., Friedrich V. Cerebral microvasculature is an early target of subarachnoid hemorrhage. Acta Neurochirurgica Supplementum. 2013; 115: 199–205. DOI: 10.1007/978-3-7091-1192-5_37.

53. Yundt K. D., Grubb R. L., Diringer M. N. et al. Autoregulatory vasodilation of parenchymal vessels is impaired during cerebral vasospasm. Journal of Cerebral Blood Flow & Metabolism. 1998; 18 (4): 419–424. DOI: 10.1097/00004647-199804000-00010.

54. Krylov V. V., Petrikov S. S., Kalinkin A. A. et al. The Influence of calcium antagonists treatment on the outcomes of patients with aneurysmal haemorrhage and high risk factor of vascular spasm. Nevrologicheskij zhurnal (The Neurological Journal). 2016; 21 (5): 280–286. DOI: 10.18821/1560-9545-2016-21-5-280-286 (In Russ.).

55. Suzuki S., Suzuki M., Iwabuchi T. et al. Role of multiple cerebral microthrombosis in symptomatic cerebral vasospasm: with a case report. Neurosurgery. 1983; 13 (2): 199–203. DOI: 10.1227/00006123-198308000-00018.

56. Sabri M., Ai J., Lakovic K. et al. Mechanisms of microthrombi formation after experimental subarachnoid hemorrhage. Neuroscience. 2012; 224: 26–37. DOI: 10.1016/j.neuroscience.2012.08.002.

57. Vergouwen M. D. I., Vermeulen M., Coert B. A. et al. Microthrombosis after aneurysmal subarachnoid hemorrhage: an additional explanation for delayed cerebral ischemia. Journal of Cerebral Blood Flow & Metabolism. 2008; 28 (11): 1761–1770. DOI: 10.1038/jcbfm.2008.74.

58. Al-Mufti F., Amuluru K., DamodaraN. et al. Novel management strategies for medically-refractory vasospasm following aneurysmal subarachnoid hemorrhage. Journal of the Neurological Sciences. 2018; 390: 44–51. DOI: 10.1016/j.jns.2018.02.039.

59. De Oliveira Manoel A. L., Macdonald R. L. Neuroinflammation as a target for intervention in subarachnoid hemorrhage. Frontiers in Neurology. 2018; 9: 292. DOI: 10.3389/fneur.2018.00292.

60. Wang A. Y.-C., Hsieh P.-C., Chen C.-C. et al. Effect of intracranial pressure control on improvement of cerebral perfusion after acute subarachnoid hemorrhage: a comparative angiography study based on temporal changes of intracranial pressure and systemic pressure. World Neurosurgery. 2018; 120: e290–e296. DOI: 10.1016/j.wneu.2018.08.053.

61. Solodov A. A., Petrikov S. S., Klychnikova E. V. et al. Normobaric hyperoxia influence on cerebral oxygenation, metabolism and oxidative stress in patients with nontraumatic subarachnoid hemorrhage due to cerebral aneurysms rupture. Anesteziologiya i reanimatologiya (Russian journal of Anaesthesiology and Reanimatology). 2013; (4): 66–71 (In Russ.).

62. Klychnikova E. V., Tazina E. V., Solodov A. A. et al. The effects of normobaric hyperoxia on oxidative stress and factors of endogenous vascular regulation in patients who suff ered from non-traumatic subarachnoid hemorrhages and remained in critical condition. Neurochemical Journal. 2013; 7 (3): 234–239. DOI: 10.1134/S1819712413030057.

63. Chong S. P., Merkle C. W., Leahy C. et al. Cerebral metabolic rate of oxygen (CMRO2) assessed by combined doppler and spectroscopic OCT. Biomedical Optics Express. 2015; 6 (10): 3941–3951. DOI: 10.1364/BOE.6.003941.

64. Liu P., Huang H., Rollins N. et al. Quantitative assessment of global cerebral metabolic rate of oxygen (CMRO2) in neonates using MRI. NMR in Biomedicine. 2014; 27 (3): 332–340. DOI: 10.1002/nbm.3067.

65. Madsen P. L., Holm S., Herning M. et al. Average blood flow and oxygen uptake in the human brain during resting wakefulness: a critical appraisal of the Kety-Schmidt technique. Journal of Cerebral Blood Flow & Metabolism. 1993; 13 (4): 646–655. DOI: 10.1038/jcbfm.1993.83.

66. Vavilala M. S., Lee L. A., Lam A. M. Cerebral blood flow and vascular physiology. Anesthesiol Anesthesiology Clinics of North America. 2002; 20 (2): 247–264. DOI: 10.1016/s0889-8537 (01)00012-8.

67. Fan A. P., Jahanian H., Holdsworth S. J. et al. Comparison of cerebral blood flow measurement with [15O]water positron emission tomography and arterial spin labeling magnetic resonance imaging: a systematic review. Journal of Cerebral Blood Flow & Metabolism. 2016; 36 (5): 842–861. DOI: 10.1177/0271678X16636393.

68. Crone C. The permeability of capillaries in various organs as determined by use of the «indicator diffusion» method. Acta Physiologica Scandinavica. 1963; 58 (4): 292–305. DOI: 10.1111/j.1748-1716.1963.tb02652.x.

69. Renkin E. M. Effects of blood flow on diffusion kinetics in isolated, perfused hindlegs of cats; a double circulation hypothesis. American Journal of Physiology-Legacy Content. 1955; 183 (1): 125–136. DOI: 10.1152/ajplegacy.1955.183.1.125.

70. Fox P. T., Raichle M. E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proceedings of the National Academy of Sciences. 1986; 83 (4): 1140–1144. DOI: 10.1073/pnas.83.4.1140.

71. Pawlik G., Rackl A., Bing R. J. Quantitative capillary topography and blood flow in the cerebral cortex of cats: an in vivo microscopic study. Brain Research. 1981; 208 (1): 35–58. DOI: 10.1016/0006-8993 (81)90619-3.

72. Villringer A., Them A., Lindauer U. et al. Capillary perfusion of the rat brain cortex. An in vivo confocal microscopy study. Circulation Research. 1994; 75 (1): 55–62. DOI: 10.1161/01.res.75.1.55.

73. Jespersen S. N., Østergaard L. The roles of cerebral blood flow, capillary transit time heterogeneity, and oxygen tension in brain oxygenation and metabolism. Journal of Cerebral Blood Flow & Metabolism. 2012; 32 (2): 264–277. DOI: 10.1038/jcbfm.2011.153.

74. Peppiatt C. M., Howarth C., Mobbs P. et al. Bidirectional control of CNS capillary diameter by pericytes. Nature. 2006; 443 (7112): 700–704. DOI: 10.1038/nature05193.

75. Østergaard L., Jespersen S.N., Mouridsen K. et al. The role of the cerebral capillaries in acute ischemic stroke: the extended penumbra model. Journal of Cerebral Blood Flow & Metabolism. 2013; 33 (5): 635–648. DOI: 10.1038/jcbfm.2013.18.

76. Østergaard L., Aamand R., Karabegovic S. et al. The role of the microcirculation in delayed cerebral ischemia and chronic degenerative changes after subarachnoid hemorrhage. Journal of Cerebral Blood Flow & Metabolism. 2013; 33 (12): 1825–1837. DOI: 10.1038/jcbfm.2013.173.

77. Krzyzewski R. M., Klis K. M., Kwinta B. M. et al. High leukocyte count and risk of poor outcome after subarachnoid hemorrhage: a meta-analysis. World Neurosurgery. 2020; 135: e541–e547. DOI: 10.1016/j.wneu.2019.12.056.

78. Anzabi M., Angleys H., Aamand R. et al. Capillary flow disturbances after experimental subarachnoid hemorrhage: a contributor to delayed cerebral ischemia? Microcirculation. 2019; 26 (3): e12516. DOI: 10.1111/micc.12516.

79. Wang H.-C., Tsai J.-C., Lee J.-E. et al. Direct visualization of microcirculation impairment after acute subdural hemorrhage in a novel animal model. Journal of Neurosurgery. 2017; 129 (4): 997–1007. DOI: 10.3171/2017.5.JNS162579.

80. Lovelock C. E., Rinkel G. J. E., Rothwell P. M. Time trends in outcome of subarachnoid hemorrhage: populationbased study and systematic review. Neurology. 2010; 74 (19): 1494–1501. DOI: 10.1212/WNL.0b013e3181dd42b3.

81. Claassen J., Carhuapoma J. R., Kreiter K. T. et al. Global cerebral edema after subarachnoid hemorrhage: frequency, predictors, and impact on outcome. Stroke. 2002; 33 (5): 1225–1232. DOI: 10.1161/01.str.0000015624.29071.1f.

82. Rosengart A. J., Schultheiss K. E., Tolentino J. et al. Prognostic factors for outcome in patients with aneurysmal subarachnoid hemorrhage. Stroke. 2007; 38 (8): 2315–2321. DOI: 10.1161/STROKEAHA.107.484360.

83. Rabinstein A. A., Weigand S., Atkinson J. L. D. et al. Patterns of cerebral infarction in aneurysmal subarachnoid hemorrhage. Stroke. 2005; 36 (5): 992–997. DOI: 10.1161/01.STR.0000163090.59350.5a.

84. Wartenberg K. E., Schmidt J. M., Claassen J. et al. Impact of medical complications on outcome after subarachnoid hemorrhage. Critical Care Medicine. 2006; 34 (3): 617–623. DOI: 10.1097/01.ccm.0000201903.46435.35.

85. Melnikova E. A., Krylov V. V. Cognitive disturbances after the operative treatment of intracranial arterial aneurisms in the acute stage of hemorrhage. Zhurnal nevrologii i psikhiatrii imeni S. S. Korsakova (S. S. Korsakov Journal of Neurology and Psychiatry). 2007; 107 (S21): 16–24 (In Russ.).

86. Dombovy M. L., Drew-Cates J., Serdans R. Recovery and rehabilitation following subarachnoid haemorrhage: Part II. Long-term follow-up. Brain Injury. 1998; 12 (10): 887–894. DOI: 10.1080/026990598122106.

87. Al-Khindi T., Macdonald R. L., Schweizer T. A. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke. 2010; 41 (8): e519–e536. DOI: 10.1161/STROKEAHA.110.581975.

88. Von Vogelsang A.-C., Forsberg C., Svensson M. et al. Patients experience high levels of anxiety 2 years following aneurysmal subarachnoid hemorrhage. World Neurosurgery. 2015; 83 (6): 1090–1097. DOI: 10.1016/j.wneu.2014.12.027.

89. Krylov V. V., Grigor’eva E. V., Lukyanchikov V. A. et al. Delayed postoperative changes after intracranial aneurysm surgery. Nevrologicheskij zhurnal (The Neurological Journal). 2018; 23 (5): 241–247. DOI: 10.18821/1560-95452018-23-5-241-247 (In Russ.).

90. Bendel P., Koivisto T., Äikiä M. et al. Atrophic enlargement of CSF volume after subarachnoid hemorrhage: correlation with neuropsychological outcome. American Journal of Neuroradiology. 2010; 31 (2): 370–376. DOI: 10.3174/ajnr.A1804.

91. Tam A. K. H., Ilodigwe D., Li Z. et al. Global cerebral atrophy after subarachnoid hemorrhage: a possible marker of acute brain injury and assessment of its impact on outcome. Acta Neurochirurgica Supplementum. 2013; 115: 17–21. DOI: 10.1007/978-3-7091-1192-5_5.

92. Anzabi M., Ardalan M., Iversen N. K. et al. Hippocampal atrophy following subarachnoid hemorrhage correlates with disruption of astrocyte morphology and capillary coverage by AQP4. Frontiers in Cellular Neuroscience. 2018; 12: 19. DOI: 10.3389/fncel.2018.00019.

93. Melnikova E. A., Krylov V. V. Neuropsychological outcomes after early surgical treatment of cerebral vessels. Neirokhirurgiya (Russian Journal of Neurosurgery). 2008; (4): 21–29 (In Russ.).

94. Voitsekhovskii D. V., Svistov D. V., Savello A. V. Neuropsychological sequellae and life quality of patients after surgical treatment of cerebral aneurysms. Neirokhirurgiya (Russian Journal of Neurosurgery). 2017; (4): 74–79 (In Russ.).

МК — мозговой кровоток

ОНМК — острое нарушение мозгового кровообращения

ОЦИ — отсроченная церебральная ишемия

ПЭТ — позитронно-эмиссионная томография

САК — субарахноидальное кровоизлияние

ЦПД — центральное перфузионное давление

CBF — cerebral blood flow

CMRO2 — cerebral metabolic rate of oxygen

CTTH — capillary transit time heterogeneity

O2EF — oxygen extraction fraction

Лечение пациентов с острым нарушением мозгового кровообращения (ОНМК) остается важной социально-экономической проблемой современной медицины. Субарахноидальное кровоизлияние (САК) составляет 2,9 % в структуре ОНМК, заболеваемость среди населения старше 25 лет — 8,5:100 000 [1, 2]. Главной причиной нетравматического САК является разрыв интракраниальных аневризм. В 2018 г. опубликованы данные ретроспективного исследования работы 22 нейрохирургических отделений РЦС Российской Федерации, наиболее активно занимающихся сосудистой патологией головного мозга, проводившегося в рамках Российского исследования хирургии аневризм (РИХА; Russian Aneurismal Surgery Trial — RAST). За год в этих центрах прооперировано 3160 пациентов по поводу аневризм головного мозга. Результаты анализа продемонстрировали лучшие исходы хирургии аневризм в стационарах с высокой хирургической активностью (свыше 100 операций в год по поводу аневризм), где развиты как микрохирургическая, так и эндоваскулярная методики [3, 4]. Несмотря на совершенствование хирургии и методов интенсивной терапии, летальность и инвалидизация пациентов остается на высоком уровне, что определяет важность и актуальность исследования данного заболевания [5, 6].

Одним из важнейших факторов неблагоприятного исхода при нетравматическом САК является формирование ишемии головного мозга [7, 8]. В основе патогенеза церебральной ишемии лежит несоответствие между перфузией и оксигенацией мозга, его метаболическими потребностями. Выделяют раннее повреждение головного мозга, непосредственно связанное с разрывом аневризмы, и отсроченную церебральную ишемию (ОЦИ). Причиной раннего повреждения является внезапное повышение внутричерепного давления вследствие субарахноидального кровоизлияния, которое может вызвать снижение перфузии головного мозга и транзиторную глобальную церебральную ишемию [9]. Объем первичного повреждения мозга зависит от выраженности и локализации кровоизлияния, а также индивидуальных особенностей мозгового кровотока. Ранняя церебральная ишемия, как правило, формируется в течение первых 72 часов после кровоизлияния. При более поздних сроках диагностируют отсроченную ишемию головного мозга [10–12].

Для Цитирования:
В. А. Лукьянчиков, А. А. Солодов, И. М. Шетова, В. Д. Штадлер, В. В. Крылов, Церебральная ишемия при нетравматическом субарахноидальном кровоизлиянии вследствие разрыва интракраниальных аневризм. Вестник неврологии, психиатрии и нейрохирургии. 2020;9.
Полная версия статьи доступна подписчикам журнала
Язык статьи:
Действия с выбранными: