J Neurol Surg A Cent Eur Neurosurg
DOI: 10.1055/a-2273-5418
Original Article

Intimal Hemorrhage of Basilar Artery Induced by Severe Vasospasm Following Subarachnoid Hemorrhage: The Experimental Analysis

1   Department of Neurosurgery, Amasya University Faculty of Medicine, Amasya, Turkey
,
Mehmet Hakan Şahin
2   Department of Neurosurgery, Ataturk University Faculty of Medicine, Erzurum, Turkey
,
Mehmet Kürşat Karadağ
2   Department of Neurosurgery, Ataturk University Faculty of Medicine, Erzurum, Turkey
,
1   Department of Neurosurgery, Amasya University Faculty of Medicine, Amasya, Turkey
,
Mete Zeynal
2   Department of Neurosurgery, Ataturk University Faculty of Medicine, Erzurum, Turkey
,
Sare Altas Sipal
3   Department of Pathology, Ataturk University Faculty of Medicine, Erzurum, Turkey
,
Mehmet D. Aydin
2   Department of Neurosurgery, Ataturk University Faculty of Medicine, Erzurum, Turkey
› Author Affiliations
Funding None.

Abstract

Background Cerebral vasospasm, a serious complication of subarachnoid hemorrhage (SAH), has been extensively studied for its neurochemical and pathophysiologic mechanisms. However, the contribution of inner elastic membrane dissection and subintimal hemorrhage to basilar artery occlusion remains underexplored. This study investigates inner elastic membrane-related changes in the basilar artery after SAH.

Methods Twenty-four hybrid rabbits were divided into control, sham, and SAH groups, with SAH induced by autologous blood injection. After 2 weeks, basilar artery changes, vasospasm indexes (VSIs), and dissections were evaluated.

Results The SAH group showed significantly higher VSI, with vascular wall thickening, luminal narrowing, convoluted smooth muscle cells, intimal elastic membrane disruption, endothelial cell desquamation, and apoptosis. Some SAH animals exhibited subintimal hemorrhage, inner elastic membrane dissection, and ruptures. Basilar arteries with subintimal hemorrhage had notably higher VSI.

Conclusions These findings highlight the role of subintimal hemorrhage and inner elastic membrane dissection in basilar artery occlusion post-SAH, offering valuable insights into vasospasm pathophysiology.

Ethical Approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.




Publication History

Received: 02 November 2023

Accepted: 19 February 2024

Accepted Manuscript online:
21 February 2024

Article published online:
22 May 2024

© 2024. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Ecker A, Riemenschneider PA. Arteriographic demonstration of spasm of the intracranial arteries, with special reference to saccular arterial aneurysms. J Neurosurg 1951; 8 (06) 660-667
  • 2 Weir B, Grace M, Hansen J, Rothberg C. Time course of vasospasm in man. J Neurosurg 1978; 48 (02) 173-178
  • 3 Sehba FA, Hou J, Pluta RM, Zhang JH. The importance of early brain injury after subarachnoid hemorrhage. Prog Neurobiol 2012; 97 (01) 14-37
  • 4 Peeyush Kumar T, McBride DW, Dash PK, Matsumura K, Rubi A, Blackburn SL. Endothelial cell dysfunction and injury in subarachnoid hemorrhage. Mol Neurobiol 2019; 56 (03) 1992-2006
  • 5 Findlay JM, Weir BK, Kanamaru K, Espinosa F. Arterial wall changes in cerebral vasospasm. Neurosurgery 1989; 25 (05) 736-745 , discussion 745–746
  • 6 Jung KH. New pathophysiological considerations on cerebral aneurysms. Neurointervention 2018; 13 (02) 73-83
  • 7 van Lieshout JH, Dibué-Adjei M, Cornelius JF. et al. An introduction to the pathophysiology of aneurysmal subarachnoid hemorrhage. Neurosurg Rev 2018; 41 (04) 917-930
  • 8 Zemke D, Farooq MU, Mohammed Yahia A, Majid A. Delayed ischemia after subarachnoid hemorrhage: result of vasospasm alone or a broader vasculopathy?. Vasc Med 2007; 12 (03) 243-249
  • 9 Alkan T, Tureyen K, Ulutas M. et al. Acute and delayed vasoconstriction after subarachnoid hemorrhage: local cerebral blood flow, histopathology, and morphology in the rat basilar artery. Arch Physiol Biochem 2001; 109 (02) 145-153
  • 10 Krings T, Choi IS. The many faces of intracranial arterial dissections. Interv Neuroradiol 2010; 16 (02) 151-160
  • 11 Bederson JB, Levy AL, Ding WH. et al. Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 1998; 42 (02) 352-360 , discussion 360–362
  • 12 Sobey CG, Faraci FM. Subarachnoid haemorrhage: what happens to the cerebral arteries?. Clin Exp Pharmacol Physiol 1998; 25 (11) 867-876
  • 13 Zeynal M, Sahin MH, Kanat A. et al. The enigma of basilar artery dissections secondary to vasospasm following subarachnoid hemorrhage; exploration of the unknown effect of superior cervical ganglia: a preliminary experimental study. J Neurol Surg A Cent Eur Neurosurg 2023; (e-pub ahead of print)
  • 14 Pluta RM, Hansen-Schwartz J, Dreier J. et al. Cerebral vasospasm following subarachnoid hemorrhage: time for a new world of thought. Neurol Res 2009; 31 (02) 151-158
  • 15 Schweizer TA, Al-Khindi T, Macdonald RL. Mini-Mental State Examination versus Montreal Cognitive Assessment: rapid assessment tools for cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. J Neurol Sci 2012; 316 (1–2): 137-140
  • 16 Francoeur CL, Mayer SA. Management of delayed cerebral ischemia after subarachnoid hemorrhage. Crit Care 2016; 20 (01) 277
  • 17 Woitzik J, Dreier JP, Hecht N. et al; COSBID study group. Delayed cerebral ischemia and spreading depolarization in absence of angiographic vasospasm after subarachnoid hemorrhage. J Cereb Blood Flow Metab 2012; 32 (02) 203-212
  • 18 Vergouwen MD, Vermeulen M, Coert BA, Stroes ES, Roos YB. Microthrombosis after aneurysmal subarachnoid hemorrhage: an additional explanation for delayed cerebral ischemia. J Cereb Blood Flow Metab 2008; 28 (11) 1761-1770
  • 19 Crowley RW, Medel R, Dumont AS. et al. Angiographic vasospasm is strongly correlated with cerebral infarction after subarachnoid hemorrhage. Stroke 2011; 42 (04) 919-923
  • 20 Seifert V, Stolke D, Reale E. Ultrastructural changes of the basilar artery following experimental subarachnoid haemorrhage. A morphological study on the pathogenesis of delayed cerebral vasospasm. Acta Neurochir (Wien) 1989; 100 (3–4): 164-171
  • 21 Friedrich V, Flores R, Muller A, Sehba FA. Escape of intraluminal platelets into brain parenchyma after subarachnoid hemorrhage. Neuroscience 2010; 165 (03) 968-975
  • 22 Iuliano BA, Pluta RM, Jung C, Oldfield EH. Endothelial dysfunction in a primate model of cerebral vasospasm. J Neurosurg 2004; 100 (02) 287-294
  • 23 Pluta RM. Dysfunction of nitric oxide synthases as a cause and therapeutic target in delayed cerebral vasospasm after SAH. Acta Neurochir Suppl (Wien) 2008; 104: 139-147
  • 24 Mizutani T, Kojima H, Asamoto S. Healing process for cerebral dissecting aneurysms presenting with subarachnoid hemorrhage. Neurosurgery 2004; 54 (02) 342-347 , discussion 347–348
  • 25 Drăghia F, Drăghia AC, Onicescu D. Electron microscopic study of the arterial wall in the cerebral aneurysms. Rom J Morphol Embryol 2008; 49 (01) 101-103
  • 26 Chung YS, Han DH. Vertebrobasilar dissection: a possible role of whiplash injury in its pathogenesis. Neurol Res 2002; 24 (02) 129-138
  • 27 Endo S, Nishijima M, Nomura H, Takaku A, Okada E. A pathological study of intracranial posterior circulation dissecting aneurysms with subarachnoid hemorrhage: report of three autopsied cases and review of the literature. Neurosurgery 1993; 33 (04) 732-738
  • 28 Sasaki O, Ogawa H, Koike T, Koizumi T, Tanaka R. A clinicopathological study of dissecting aneurysms of the intracranial vertebral artery. J Neurosurg 1991; 75 (06) 874-882
  • 29 Yoshimoto Y, Hoya K, Tanaka Y, Uchida T. Basilar artery dissection. J Neurosurg 2005; 102 (03) 476-481
  • 30 Zubkov AY, Sanghvi AN, Cloft HJ, Wijdicks EF, Rabinstein AA. Subarachnoid hemorrhage as a presentation of basilar artery dissection. Neurocrit Care 2007; 7 (02) 165-168
  • 31 Caplan LR, Baquis GD, Pessin MS. et al. Dissection of the intracranial vertebral artery. Neurology 1988; 38 (06) 868-877
  • 32 Nakajima H, Ishiguro T, Komiyama M. Basilar artery dissection presenting with subarachnoid hemorrhage: report of two cases. NMC Case Rep J 2015; 2 (03) 97-100