Clinical Physiology of Circulation

ISSN 1814-6910 (Print)
ISSN 2410-9134 (Online)

 

Chief Editor

Leo A. Bockeria, MD, PhD, DSc, Professor, Academician of Russian Academy of Sciences, President of Bakoulev National Medical Research Center for Cardiovascular Surgery


Issue's catalogue ➤ КФК. 2021; 18 (2): 93-180 ➤ Церебральный гиперперфузионный синдром: проблема разграничения близких синдромов, вероятные механизмы развития, клинические проявления и факторы риска

Cerebral hyperperfusion syndrome: the problem of distinguishing between similar syndromes, probable mechanisms of development, clinical manifestations and risk factors

Authors: Emets E.V., Shumilina M.V.

Company:
1 Institute of Training of Highly Qualified Personnel and Professional Education of the Bakoulev National Medical Research Center for Cardiovascular Surgery, Moscow, 121552, Russian Federation
2 Voronezh Regional Clinical Hospital No. 1, Voronezh, 394066, Russian Federation

E-mail: Сведения доступны для зарегистрированных пользователей.

DOI: https://doi.org/10.24022/1814-6910-2021-18-2-118-127

UDC: 616.831-005

Link: Clinical Physiology of Blood Circulaiton. 2021; 2 (18): 118-127

Quote as: Emets E.V., Shumilina M.V. Cerebral hyperperfusion syndrome: the problem of distinguishing between similar syndromes, probable mechanisms of development, clinical manifestations and risk factors. Clinical Physiology of Circulation. 2021; 18 (2): 118–27 (in Russ.). DOI: 10.24022/1814-6910-2021-18-2-118-127

Keywords:  cerebral hyperperfusion syndrome disorders of venous outflow arteriovenous balance

Received / Accepted:  26.02.2021 / 01.03.2021

Full text:  

Abstract

The review is devoted to the generalization of modern data on cerebral hyperperfusion syndrome (CHS). CHS is similar to the luxury perfusion syndrome, hypertensive encephalopathy, posterior reversible encephalopathy syndrome and reversible cerebral vasoconstriction syndrome. The problem of distinguishing CHS and related syndromes is considered. The probable mechanisms of the CHS development after revascularization of carotid and other arteries are discussed: 1) increased cerebral blood flow; 2) violation of cerebral autoregulation; 3) damage to the cerebral vessels by free radicals; 4) destruction of the reflex mechanism of the baroreceptor; 5) the connection of CHS with the trigeminovascular reflex; 6) the connection of CHS with the cerebral arteriovenous imbalance. The importance of studying arteriovenous imbalance as a mechanism of the CHS development is emphasized. The risk factors of the CHS development after carotid endarterectomy and stenting of the carotid arteries are considered.

References

  1. Radak D.M., Ševković M., Babić S. How to identify risk for cerebral hyperperfusion syndrome after carotid revascularization procedures? Vojnosanit. Pregl. 2019; 76 (8): 834–8. DOI: 10.2298/VSP170910154R
  2. Radak D., Ilijevski N., Djukic N. Carotid surgery today: an update after 14000 carotid endarterectomy procedures. Vojnosanit. Pregl. 2016; 73 (5): 472–9. DOI: 10.2298/vsp160305060r
  3. Abou-Chebl A., Yadav J.S., Reginelli J.P., Bajzer C., Bhatt D., Krieger D.W. Intracranial haemorrhage and hyperperfusion syndrome following carotid artery stenting. J. Am. Coll. Cardiol. 2004; 43 (9): 1596–601. DOI: 10.1016/j.jacc.2003.12.039
  4. Ogasawara K., Sakai N., Kuroiwa T., Hosoda K., Iihara K., Toyoda K. et al. Japanese Society for Treatment at Neck in Cerebrovascular Disease Study Group. Intracranial hemorrhage associated with cerebral hyperperfusion syndrome following carotid endarterectomy and carotid artery stenting: retrospective review of 4494 patients. J. Neurosurg. 2007; 107 (6): 1130–6. DOI: 10.3171/JNS-07/12/1130
  5. Hobson R.W. 2nd, Mackey W.C., Ascher E., Murad M.H., Calligaro K.D., Comerota A.J. et al. Society for Vascular Surgery. Management of atherosclerotic carotid artery disease: clinical practice guidelines of the Society for Vascular Surgery. J. Vasc. Surg. 2008; 48 (2): 480–6. DOI: 10.1016/j.jvs.2008.05.036
  6. Sundt T.M., Sandok B.A., Whisnant J.P. Carotid endarterectomy. Complications and preoperative assessment of risk. Mayo Clin. Proc. 1975; 50 (1): 301–6.
  7. Lin Y.-H., Liu H.-M. Update on cerebral hyperperfusion syndrome. J. Neurointervent. Surg. 2020; 12: 788–93. DOI: 10.1136/neurintsurg-2019-015621
  8. Delgado M.G., Bogousslavsky J. Cerebral hyperperfusion syndrome and related conditions. Eur. Neurol. 2020; 83: 453–7. DOI: 10.1159/000511307
  9. Lassen N.A. The luxury-perfusion syndrome and its possible relation to acute metabolic acidosis localised within the brain. Lancet. 1966; 2 (7473): 1113–5. DOI: 10.1016/s0140-6736(66)92199-4
  10. Cho A.H., Cho Y.P., Lee D.H., Kwon T.W., Kwon S.U., Suh D.C. et al. Reperfusion injury on magnetic resonance imaging after carotid revascularization. Stroke. 2014; 45 (2): 602–4. DOI: 10.1161/STROKEAHA. 113.003792
  11. Oppenheimer B.S., Fishbery A.M. Hypertensive encephalopathy. Arch. Intern. Med. 1928; 41 (2): 264–78. DOI: 10.1001/archinte.1928.00130140126010
  12. Bernstein M., Fleming J.F., Deck J.H. Cerebral hyperperfusion after carotid endarterectomy: a cause of cerebral hemorrhage. Neurosurgery. 1984; 15 (1): 50–6. DOI: 10.1227/00006123-198407000-00010
  13. Moulakakis K.G., Mylonas S.N., Sfyroeras G.S., Andrikopoulos V. Hyperperfusion syndrome after carotid revascularization. J. Vasc. Surg. 2009; 49 (4): 1060–68. DOI: 10.1016/j.jvs.2008.11.026
  14. Spetzler R.F., Wilson C.B., Weinstein P., Mehdorn M., Townsend J., Telles D. Normal perfusion pressure breakthrough theory. Clin. Neurosurg. 1978; 25: 651–72. DOI: 10.1093/neurosurgery/25.cn_suppl_1.651
  15. Naylor A.R., Evans J., Thompson M.M., London N.J., Abbott R.J., Cherryman G. et al. Seizures after carotid endarterectomy: hyperperfusion, dysautoregulation or hypertensive encephalopathy? Eur. J. Vasc. Endovasc. Surg. 2003; 26 (1): 39–44. DOI: 10.1053/ejvs.2002.1925
  16. Hinchey J., Chaves C., Appignani B., Breen J., Pao L., Wang A. et al. A reversible posterior leukoencephalopathy syndrome. N. Engl. J. Med. 1996; 334 (8): 494–500. DOI: 10.1056/NEJM199602223340803
  17. Ay H., Buonanno F.S., Schaefer P.W., Le D.A., Wang B., Gonzalez R.G. et al. Posterior leukoencephalopathy without severe hypertension: utility of diffusion-weighted MRI. Neurology. 1998; 51 (5): 1369–76. DOI: 10.1212/wnl.51.5.1369
  18. Bartynski W.S. Posterior reversible encephalopathy syndrome. Part 2: controversies surrounding pathophysiology of vasogenic edema. Am. J. Neurorad. 2008; 29: 1043–9. DOI: 10.3174/ajnr.A0929
  19. Fugate J.E., Rabinstein A.A. Posterior reversible encephalopathy syndrome: clinical and radiological manifestations, pathophysiology, and outstanding questions. Lancet Neurol. 2015; 14 (9): 914–25. DOI: 10.1007/s12028-012-9733-x
  20. Levitt A., Zampolin R., Burns J., Bello J.A., Slasky S.E. Posterior reversible encephalopathy syndrome and reversible cerebral vasoconstriction syndrome. Distinct clinical entities with overlapping pathophysiology. Radiol. Clin. North Am. 2019; 57 (6): 1133–46. DOI: 10.1016/j.rcl.2019.07.001
  21. Calabrese L.H., Dodick D.W., Schwedt T.J., Singhal A.B. Narrative review: reversible cerebral vasoconstriction syndromes. Ann. Intern. Med. 2007; 146 (1): 34–44. DOI: 10.7326/0003-4819-146-1-200701020-00007
  22. Ducros A. Reversible cerebral vasoconstriction syndrome. Lancet Neurol. 2012; 11 (10): 906–17. DOI: 10.1016/S1474-4422(12)70135-7
  23. Ducros A., Bousser M.G. Reversible cerebral vasoconstriction syndrome. Pract. Neurol. 2009; 9 (5): 256–67. DOI: 10.1136/jnnp.2009.187856
  24. Ogasawara K., Inoue T., Kobayashi M., Endo H., Yoshida K., Fukuda T. et al. Cerebral hyperperfusion following carotid endarterectomy: diagnostic utility of intraoperative transcranial Doppler ultrasonography compared with single-photon emission computed tomography study. Am. J. Neuroradiol. 2005; 26 (2): 252–7.
  25. Mitrasinović A., Kolar J., Radak S., Nenezić D., Kupresanin I., Aleksić N. Ultrasonografic monitoring of hemodynamic parameters in symptomatic and asymptomatic patients with high-grade carotid stenosis prior and following carotid endarterectomy. Vojnosanit. Pregl. 2012; 69 (5): 399–404 (Serbian). DOI: 10.2298/VSP1205399M
  26. Henderson R.D., Phan T.G., Piepgras D.G., Wijdicks E.F. Mechanisms of intracerebral hemorrhage after carotid endarterectomy. J. Neurosurg. 2001; 95 (6): 964–9. DOI: 10.3171/jns.2001.95.6.0964
  27. Huibers A., Calvet D., Kennedy F., Czuriga-Kovács K.R., Featherstone R.L., Moll F.L. et al. Mechanism of procedural stroke following carotid endarterectomy or carotid artery stenting within the International Carotid Stenting Study (ICSS) randomised trial. Eur. J. Vasc. Endovasc. Surg. 2015; 50: 281–8. DOI: 10.1016/j.ejvs.2015.05.017
  28. Tang S., Huang Y., Shieh J., Huang S., Yip P., Jeng J. Dynamic cerebral autoregulation in carotid stenosis before and after carotid stenting. J. Vasc. Surg. 2008; 48: 88–92. DOI: 10.1016/j.jvs.2008.02.025
  29. Guo Z.-N., Xing Y., Wang S., Ma H., Liu J., Yang Y. Characteristics of dynamic cerebral autoregulation in cerebral small vessel disease: diffuse and sustained. Sci. Rep. 2015; 5: 15269. DOI: 10.1038/srep15269
  30. Liang F., Fukasaku K., Liu H., Takagi Sh. A computational model study of the influence of the anatomy of the circle of Willis on cerebral hyperperfusion following carotid artery surgery. Biomed. Eng. Online. 2011; 10: 84. DOI: 10.1186/1475-925X-10-84
  31. Shimamura N., Naraoka M., Matsuda N., Katayama K., Kakuta K., Katagai T. et al. Intra-arterial oxidative stress correlates negatively with cognitive function and positively with postoperative ischemic lesions in carotid artery stenosis stenting. J. Neurointerv. Surg. 2018; 10: 440–5. DOI: 10.1136/neurintsurg-2017-013465
  32. Suga Y., Ogasawara K., Saito H., Komoribayashi N., Kobayashi M., Inoue T. et al. Preoperative cerebral hemodynamic impairment and reactive oxygen species produced during carotid endarterectomy correlate with development of postoperative cerebral hyperperfusion. Stroke. 2007; 38 (10): 2712–7. DOI: 10.1161/STROKEAHA.107.483495
  33. Soong C.V., Young I.S., Hood J.M., Rowlands B.J., Trimble E.R., Barros D’Sa A.A. The generation of byproducts of lipid peroxidation following carotid endarterectomy. Eur. J. Vasc. Endovasc. Surg. 1996; 12 (4): 455–8. DOI: 10.1016/s1078-5884(96)80014-1
  34. Nouraei S.A.R., Al-Rawi P.G., Sigaudo-Roussel D., Giussani D.A., Gaunt M.E. Carotid endarterectomy impairs blood pressure homeostasis by reducing the physiologic baroreflex reserve. J. Vasc. Surg. 2005; 41: 631–7. DOI: 10.1016/j.jvs.2005.01.009
  35. Macfarlane R., Moskowitz M.A., Sakas D.E., Tasdemiroglu E., Wei E.P., Kontos H.A. The role of neuroeffector mechanisms in cerebral hyperperfusion syndromes. J. Neurosurg. 1991; 75: 845–55. DOI: 10.3171/jns.1991.75.6.0845
  36. Шумилина М.В. Нарушения венозного церебрального кровообращения у пациентов с сердечно-сосудистой патологией. Клиническая физиология кровообращения. 2013; 3: 5–16.
  37. Шумилина М.В., Айроян А.Г. Церебральный гиперперфузионный синдром. Сердечно-сосудистые заболевания. Бюллетень НЦССХ им. А.Н. Бакулева РАМН. 2015; 16 (S3): 77.
  38. Стрелкова Т.В., Айроян А.Г. Церебральный гиперперфузионный синдром. Клиническая физиология кровообращения. 2015; 3: 5–16.
  39. Czosnyka M. Brain venous blood outfow. Neurocrit. Care. 2019; 31: 249–50. DOI: 10.1007/s12028-019- 00744-1
  40. Wang Z., Ding J., Bai C., Ding Y., Ji X., Meng R. Clinical classification and collateral circulation in chronic cerebrospinal venous insufficiency. Front. Neurol. 2020; 11: 913. DOI: 10.3389/fneur.2020.00913
  41. Bateman A.R., Bateman G.A., Barber T. The relationship between cerebral blood flow and venous sinus pressure: can hyperemia induce idiopathic intracranial hypertension? Fluids Barriers CNS. 2021; 18: 5. DOI: 10.1186/s12987-021-00239-2
  42. Huibers A.E., Westerink J., de Vries E.E., Hoskam A., den Ruijter H.M., Moll F.L. et al. Editor’s choice – cerebral hyperperfusion syndrome after carotid artery stenting: a systematic review and meta-analysis. Eur. J. Vasc. Endovasc. Surg. 2018; 56: 322–33. DOI: 10.1016/j.ejvs.2018.05.012
  43. Galyfos G., Sianou A., Filis K. Cerebral hyperperfusion syndrome and intracranial hemorrhage after carotid endarterectomy or carotid stenting: a meta-analysis. J. Neurol. Sci. 2017; 381: 74–82. DOI: 10.1016/j.jns.2017.08.020
  44. Hussain M.A., Alali A.S., Mamdani M., Tu J.V., Saposnik G., Salata K. et al. Risk of intracranial hemorrhage after carotid artery stenting versus endarterectomy: a population-based study. J. Neurosurg. 2018; 129: 1522–9. DOI: 10.3171/2017.8.JNS171142
  45. González G.A., Moniche F., Escudero-Martinez I., Mancha F., Tomasello A., Ribó M. et al. Clinical predictors of hyperperfusion syndrome following carotid stenting: results from a national prospective multicenter study. JACC Cardiovasc Interv. 2019; 12: 873–82. DOI: 10.1016/j.jcin.2019.01.247
  46. Mondel P.K., Udare A.S., Anand S., Kulkarni A.V., Kapadia F.N., Modhe J.M. et al. Cerebral hyperperfusion syndrome after endovascular reconstruction of carotid artery in high-flow carotid-jugular fistula. Cardiovasc. Intervent. Radiol. 2014; 37 (5): 1369–75.
  47. Oh S.I., Lee S.J., Lee Y.J., Kim H.J. Delayed cerebral hyperperfusion syndrome three weeks after carotid artery stenting presenting as status epilepticus. J. Korean Neurosurg. Soc. 2014; 56 (5): 441–3. DOI: 10.3340/jkns.2014.56.5.441
  48. Wagner W.H., Cossman D.V., Farber A., Levin P.M., Cohen J.L. Hyperperfusion syndrome after carotid endarterectomy. Ann. Vasc. Surg. 2005; 19: 479–86. DOI: 10.1007/s10016-005-4644-3
  49. Adhiyaman V., Alexander S. Cerebral hyperperfusion syndrome following carotid endarterectomy. QJM. 2007; 100: 239–44. DOI: 10.1093/qjmed/hcm009
  50. Buhk J.H., Cepek L., Knauth M. Hyperacute intracerebral hemorrhage complicating carotid stenting should be distinguished from hyperperfusion syndrome. Am. J. Neuroradiol. 2006; 27 (7): 1508–13.
  51. Dua A., Romanelli M., Upchurch G.R.Jr., Pan J., Hood D., Hodgson K.J. et al. Predictors of poor outcome after carotid intervention. J. Vasc. Surg. 2016; 64: 663–70. DOI: 10.1016/j.jvs.2016.03.428
  52. Jovic M., Unic-Stojanovic D., Isenovic E., Manfredi R., Cekic O., Ilijevski N. et al. Anesthetics and cerebral protection in patients undergoing carotid endarterectomy. J. Cardiothorac. Vasc. Anesth. 2015; 29 (1): 178–84. DOI: 10.1053/j.jvca.2014.05.019
  53. Zhang L., Dai D., Li Z., Duan G., Zhang Y.-W., Yang P. et al. Risk factors for hyperperfusion-induced intracranial hemorrhage after carotid artery stenting in patients with symptomatic severe carotid stenosis evaluation. J. Neurointerv. Surg. 2019; 11: 474–8. DOI: 10.1136/neurintsurg-2018-013998
  54. Ito K., Yonaha H., Kai Y., Hokama Y., Nagamine H., Miyagi T. et al. Hyperperfusion syndrome after stent placement for subclavian artery stenosis: case report. Neurol. Med. Chir. (Tokyo). 2012; 52 (12): 902–5. DOI: 10.2176/nmc.52.902
  55. Fu C., Xu Z., Hu Z., Yao S., Liu F., Feng B. et al. Cortical blindness as a rare presentation of hemorrhagic cerebral hyperperfusion syndrome following vertebral angioplasty. J. Neurointerv. Surg. 2018; 10: e21. DOI: 10.1136/bcr-2017-013412
  56. Chiu A.H.Y., Wenderoth J. Cerebral hyperperfusion after flow diversion of large intracranial aneurysms. J. Neurointerv. Surg. 2013; 5: e48. DOI: 10.1136/neurintsurg-2012-010479.rep
  57. Ecker R.D., Murray R.D., Seder D.B. Hyperperfusion syndrome after stent/coiling of a ruptured carotid bifurcation aneurysm. Neurocrit. Care. 2013; 18: 54–8. DOI: 10.1007/s12028-012-9733-x
****
  1. Radak D.M., Ševković M., Babić S. How to identify risk for cerebral hyperperfusion syndrome after carotid revascularization procedures? Vojnosanit. Pregl. 2019; 76 (8): 834–8. DOI: 10.2298/VSP170910154R
  2. Radak D., Ilijevski N., Djukic N. Carotid surgery today: an update after 14000 carotid endarterectomy procedures. Vojnosanit. Pregl. 2016; 73 (5): 472–9. DOI: 10.2298/vsp160305060r
  3. Abou-Chebl A., Yadav J.S., Reginelli J.P., Bajzer C., Bhatt D., Krieger D.W. Intracranial haemorrhage and hyperperfusion syndrome following carotid artery stenting. J. Am. Coll. Cardiol. 2004; 43 (9): 1596–601. DOI: 10.1016/j.jacc.2003.12.039
  4. Ogasawara K., Sakai N., Kuroiwa T., Hosoda K., Iihara K., Toyoda K. et al. Japanese Society for Treatment at Neck in Cerebrovascular Disease Study Group. Intracranial hemorrhage associated with cerebral hyperperfusion syndrome following carotid endarterectomy and carotid artery stenting: retrospective review of 4494 patients. J. Neurosurg. 2007; 107 (6): 1130–6. DOI: 10.3171/JNS-07/12/1130
  5. Hobson R.W. 2nd, Mackey W.C., Ascher E., Murad M.H., Calligaro K.D., Comerota A.J. et al. Society for Vascular Surgery. Management of atherosclerotic carotid artery disease: clinical practice guidelines of the Society for Vascular Surgery. J. Vasc. Surg. 2008; 48 (2): 480–6. DOI: 10.1016/j.jvs.2008.05.036
  6. Sundt T.M., Sandok B.A., Whisnant J.P. Carotid endarterectomy. Complications and preoperative assessment of risk. Mayo Clin. Proc. 1975; 50 (1): 301–6.
  7. Lin Y.-H., Liu H.-M. Update on cerebral hyperperfusion syndrome. J. Neurointervent. Surg. 2020; 12: 788–93. DOI: 10.1136/neurintsurg-2019-015621
  8. Delgado M.G., Bogousslavsky J. Cerebral hyperperfusion syndrome and related conditions. Eur. Neurol. 2020; 83: 453–7. DOI: 10.1159/000511307
  9. Lassen N.A. The luxury-perfusion syndrome and its possible relation to acute metabolic acidosis localised within the brain. Lancet. 1966; 2 (7473): 1113–5. DOI: 10.1016/s0140-6736(66)92199-4
  10. Cho A.H., Cho Y.P., Lee D.H., Kwon T.W., Kwon S.U., Suh D.C. et al. Reperfusion injury on magnetic resonance imaging after carotid revascularization. Stroke. 2014; 45 (2): 602–4. DOI: 10.1161/STROKEAHA. 113.003792
  11. Oppenheimer B.S., Fishbery A.M. Hypertensive encephalopathy. Arch. Intern. Med. 1928; 41 (2): 264–78. DOI: 10.1001/archinte.1928.00130140126010
  12. Bernstein M., Fleming J.F., Deck J.H. Cerebral hyperperfusion after carotid endarterectomy: a cause of cerebral hemorrhage. Neurosurgery. 1984; 15 (1): 50–6. DOI: 10.1227/00006123-198407000-00010
  13. Moulakakis K.G., Mylonas S.N., Sfyroeras G.S., Andrikopoulos V. Hyperperfusion syndrome after carotid revascularization. J. Vasc. Surg. 2009; 49 (4): 1060–68. DOI: 10.1016/j.jvs.2008.11.026
  14. Spetzler R.F., Wilson C.B., Weinstein P., Mehdorn M., Townsend J., Telles D. Normal perfusion pressure breakthrough theory. Clin. Neurosurg. 1978; 25: 651–72. DOI: 10.1093/neurosurgery/25.cn_suppl_1.651
  15. Naylor A.R., Evans J., Thompson M.M., London N.J., Abbott R.J., Cherryman G. et al. Seizures after carotid endarterectomy: hyperperfusion, dysautoregulation or hypertensive encephalopathy? Eur. J. Vasc. Endovasc. Surg. 2003; 26 (1): 39–44. DOI: 10.1053/ejvs.2002.1925
  16. Hinchey J., Chaves C., Appignani B., Breen J., Pao L., Wang A. et al. A reversible posterior leukoencephalopathy syndrome. N. Engl. J. Med. 1996; 334 (8): 494–500. DOI: 10.1056/NEJM199602223340803
  17. Ay H., Buonanno F.S., Schaefer P.W., Le D.A., Wang B., Gonzalez R.G. et al. Posterior leukoencephalopathy without severe hypertension: utility of diffusion-weighted MRI. Neurology. 1998; 51 (5): 1369–76. DOI: 10.1212/wnl.51.5.1369
  18. Bartynski W.S. Posterior reversible encephalopathy syndrome. Part 2: controversies surrounding pathophysiology of vasogenic edema. Am. J. Neurorad. 2008; 29: 1043–9. DOI: 10.3174/ajnr.A0929
  19. Fugate J.E., Rabinstein A.A. Posterior reversible encephalopathy syndrome: clinical and radiological manifestations, pathophysiology, and outstanding questions. Lancet Neurol. 2015; 14 (9): 914–25. DOI: 10.1007/s12028-012-9733-x
  20. Levitt A., Zampolin R., Burns J., Bello J.A., Slasky S.E. Posterior reversible encephalopathy syndrome and reversible cerebral vasoconstriction syndrome. Distinct clinical entities with overlapping pathophysiology. Radiol. Clin. North Am. 2019; 57 (6): 1133–46. DOI: 10.1016/j.rcl.2019.07.001
  21. Calabrese L.H., Dodick D.W., Schwedt T.J., Singhal A.B. Narrative review: reversible cerebral vasoconstriction syndromes. Ann. Intern. Med. 2007; 146 (1): 34–44. DOI: 10.7326/0003-4819-146-1-200701020-00007
  22. Ducros A. Reversible cerebral vasoconstriction syndrome. Lancet Neurol. 2012; 11 (10): 906–17. DOI: 10.1016/S1474-4422(12)70135-7
  23. Ducros A., Bousser M.G. Reversible cerebral vasoconstriction syndrome. Pract. Neurol. 2009; 9 (5): 256–67. DOI: 10.1136/jnnp.2009.187856
  24. Ogasawara K., Inoue T., Kobayashi M., Endo H., Yoshida K., Fukuda T. et al. Cerebral hyperperfusion following carotid endarterectomy: diagnostic utility of intraoperative transcranial Doppler ultrasonography compared with single-photon emission computed tomography study. Am. J. Neuroradiol. 2005; 26 (2): 252–7.
  25. Mitrasinović A., Kolar J., Radak S., Nenezić D., Kupresanin I., Aleksić N. Ultrasonografic monitoring of hemodynamic parameters in symptomatic and asymptomatic patients with high-grade carotid stenosis prior and following carotid endarterectomy. Vojnosanit. Pregl. 2012; 69 (5): 399–404 (Serbian). DOI: 10.2298/VSP1205399M
  26. Henderson R.D., Phan T.G., Piepgras D.G., Wijdicks E.F. Mechanisms of intracerebral hemorrhage after carotid endarterectomy. J. Neurosurg. 2001; 95 (6): 964–9. DOI: 10.3171/jns.2001.95.6.0964
  27. Huibers A., Calvet D., Kennedy F., Czuriga-Kovács K.R., Featherstone R.L., Moll F.L. et al. Mechanism of procedural stroke following carotid endarterectomy or carotid artery stenting within the International Carotid Stenting Study (ICSS) randomised trial. Eur. J. Vasc. Endovasc. Surg. 2015; 50: 281–8. DOI: 10.1016/j.ejvs.2015.05.017
  28. Tang S., Huang Y., Shieh J., Huang S., Yip P., Jeng J. Dynamic cerebral autoregulation in carotid stenosis before and after carotid stenting. J. Vasc. Surg. 2008; 48: 88–92. DOI: 10.1016/j.jvs.2008.02.025
  29. Guo Z.-N., Xing Y., Wang S., Ma H., Liu J., Yang Y. Characteristics of dynamic cerebral autoregulation in cerebral small vessel disease: diffuse and sustained. Sci. Rep. 2015; 5: 15269. DOI: 10.1038/srep15269
  30. Liang F., Fukasaku K., Liu H., Takagi Sh. A computational model study of the influence of the anatomy of the circle of Willis on cerebral hyperperfusion following carotid artery surgery. Biomed. Eng. Online. 2011; 10: 84. DOI: 10.1186/1475-925X-10-84
  31. Shimamura N., Naraoka M., Matsuda N., Katayama K., Kakuta K., Katagai T. et al. Intra-arterial oxidative stress correlates negatively with cognitive function and positively with postoperative ischemic lesions in carotid artery stenosis stenting. J. Neurointerv. Surg. 2018; 10: 440–5. DOI: 10.1136/neurintsurg-2017-013465
  32. Suga Y., Ogasawara K., Saito H., Komoribayashi N., Kobayashi M., Inoue T. et al. Preoperative cerebral hemodynamic impairment and reactive oxygen species produced during carotid endarterectomy correlate with development of postoperative cerebral hyperperfusion. Stroke. 2007; 38 (10): 2712–7. DOI: 10.1161/STROKEAHA.107.483495
  33. Soong C.V., Young I.S., Hood J.M., Rowlands B.J., Trimble E.R., Barros D’Sa A.A. The generation of byproducts of lipid peroxidation following carotid endarterectomy. Eur. J. Vasc. Endovasc. Surg. 1996; 12 (4): 455–8. DOI: 10.1016/s1078-5884(96)80014-1
  34. Nouraei S.A.R., Al-Rawi P.G., Sigaudo-Roussel D., Giussani D.A., Gaunt M.E. Carotid endarterectomy impairs blood pressure homeostasis by reducing the physiologic baroreflex reserve. J. Vasc. Surg. 2005; 41: 631–7. DOI: 10.1016/j.jvs.2005.01.009
  35. Macfarlane R., Moskowitz M.A., Sakas D.E., Tasdemiroglu E., Wei E.P., Kontos H.A. The role of neuroeffector mechanisms in cerebral hyperperfusion syndromes. J. Neurosurg. 1991; 75: 845–55. DOI: 10.3171/jns.1991.75.6.0845
  36. Shumilina M.V. Disorder venous circulation in patients with cardiovascular disease. Clinical Physiology of Circulation. 2013; 3: 5–16 (in Russ.).
  37. Shumilina M.V., Ayroyan A.G. Cerbral hyperperfusion syndrome. The Byulletin of Bakoulev Center. Cardiovascular Disiases. 2015; 16 (S3): 77 (in Russ.).
  38. Strelkova T.V., Ayroyan A.G. Cerbral hyperperfusion syndrome. Clinical Physiology of Circulation. 2015; 3: 5–16 (in Russ.).
  39. Czosnyka M. Brain venous blood outfow. Neurocrit. Care. 2019; 31: 249–50. DOI: 10.1007/s12028-019- 00744-1
  40. Wang Z., Ding J., Bai C., Ding Y., Ji X., Meng R. Clinical classification and collateral circulation in chronic cerebrospinal venous insufficiency. Front. Neurol. 2020; 11: 913. DOI: 10.3389/fneur.2020.00913
  41. Bateman A.R., Bateman G.A., Barber T. The relationship between cerebral blood flow and venous sinus pressure: can hyperemia induce idiopathic intracranial hypertension? Fluids Barriers CNS. 2021; 18: 5. DOI: 10.1186/s12987-021-00239-2
  42. Huibers A.E., Westerink J., de Vries E.E., Hoskam A., den Ruijter H.M., Moll F.L. et al. Editor’s choice – cerebral hyperperfusion syndrome after carotid artery stenting: a systematic review and meta-analysis. Eur. J. Vasc. Endovasc. Surg. 2018; 56: 322–33. DOI: 10.1016/j.ejvs.2018.05.012
  43. Galyfos G., Sianou A., Filis K. Cerebral hyperperfusion syndrome and intracranial hemorrhage after carotid endarterectomy or carotid stenting: a meta-analysis. J. Neurol. Sci. 2017; 381: 74–82. DOI: 10.1016/j.jns.2017.08.020
  44. Hussain M.A., Alali A.S., Mamdani M., Tu J.V., Saposnik G., Salata K. et al. Risk of intracranial hemorrhage after carotid artery stenting versus endarterectomy: a population-based study. J. Neurosurg. 2018; 129: 1522–9. DOI: 10.3171/2017.8.JNS171142
  45. González G.A., Moniche F., Escudero-Martinez I., Mancha F., Tomasello A., Ribó M. et al. Clinical predictors of hyperperfusion syndrome following carotid stenting: results from a national prospective multicenter study. JACC Cardiovasc Interv. 2019; 12: 873–82. DOI: 10.1016/j.jcin.2019.01.247
  46. Mondel P.K., Udare A.S., Anand S., Kulkarni A.V., Kapadia F.N., Modhe J.M. et al. Cerebral hyperperfusion syndrome after endovascular reconstruction of carotid artery in high-flow carotid-jugular fistula. Cardiovasc. Intervent. Radiol. 2014; 37 (5): 1369–75.
  47. Oh S.I., Lee S.J., Lee Y.J., Kim H.J. Delayed cerebral hyperperfusion syndrome three weeks after carotid artery stenting presenting as status epilepticus. J. Korean Neurosurg. Soc. 2014; 56 (5): 441–3. DOI: 10.3340/jkns.2014.56.5.441
  48. Wagner W.H., Cossman D.V., Farber A., Levin P.M., Cohen J.L. Hyperperfusion syndrome after carotid endarterectomy. Ann. Vasc. Surg. 2005; 19: 479–86. DOI: 10.1007/s10016-005-4644-3
  49. Adhiyaman V., Alexander S. Cerebral hyperperfusion syndrome following carotid endarterectomy. QJM. 2007; 100: 239–44. DOI: 10.1093/qjmed/hcm009
  50. Buhk J.H., Cepek L., Knauth M. Hyperacute intracerebral hemorrhage complicating carotid stenting should be distinguished from hyperperfusion syndrome. Am. J. Neuroradiol. 2006; 27 (7): 1508–13.
  51. Dua A., Romanelli M., Upchurch G.R.Jr., Pan J., Hood D., Hodgson K.J. et al. Predictors of poor outcome after carotid intervention. J. Vasc. Surg. 2016; 64: 663–70. DOI: 10.1016/j.jvs.2016.03.428
  52. Jovic M., Unic-Stojanovic D., Isenovic E., Manfredi R., Cekic O., Ilijevski N. et al. Anesthetics and cerebral protection in patients undergoing carotid endarterectomy. J. Cardiothorac. Vasc. Anesth. 2015; 29 (1): 178–84. DOI: 10.1053/j.jvca.2014.05.019
  53. Zhang L., Dai D., Li Z., Duan G., Zhang Y.-W., Yang P. et al. Risk factors for hyperperfusion-induced intracranial hemorrhage after carotid artery stenting in patients with symptomatic severe carotid stenosis evaluation. J. Neurointerv. Surg. 2019; 11: 474–8. DOI: 10.1136/neurintsurg-2018-013998
  54. Ito K., Yonaha H., Kai Y., Hokama Y., Nagamine H., Miyagi T. et al. Hyperperfusion syndrome after stent placement for subclavian artery stenosis: case report. Neurol. Med. Chir. (Tokyo). 2012; 52 (12): 902–5. DOI: 10.2176/nmc.52.902
  55. Fu C., Xu Z., Hu Z., Yao S., Liu F., Feng B. et al. Cortical blindness as a rare presentation of hemorrhagic cerebral hyperperfusion syndrome following vertebral angioplasty. J. Neurointerv. Surg. 2018; 10: e21. DOI: 10.1136/bcr-2017-013412
  56. Chiu A.H.Y., Wenderoth J. Cerebral hyperperfusion after flow diversion of large intracranial aneurysms. J. Neurointerv. Surg. 2013; 5: e48. DOI: 10.1136/neurintsurg-2012-010479.rep
  57. Ecker R.D., Murray R.D., Seder D.B. Hyperperfusion syndrome after stent/coiling of a ruptured carotid bifurcation aneurysm. Neurocrit. Care. 2013; 18: 54–8. DOI: 10.1007/s12028-012-9733-x

About Authors

  • Ekaterina V. Emets, Functional Diagnostician; ORCID
  • Margarita V. Shumilina, Dr. Med. Sc., Professor of Chair of Cardiology and Functional Diagnostics, Head of Group of Ultrasound Studies of Cardiovascular and Organ Pathology ORCID

 If you found mistakes, select text and press Alt+A